Tese Alinne Rezende

INSTITUTO NACIONAL DE PESQUISAS DA
AMAZÔNIA-INPA
PROGRAMA DE PÓS-GRADUAÇÃO EM
BIODIVERSIDADE E BIOTECNOLOGIA DA REDE BIONORTE
CARACTERIZAÇÃO DAS FONTES DE RECURSOS TRÓFICOS PARA

ABELHAS DOS GÊNEROS MELIPONA E SCAPTOTRIGONA NAS
ÁREAS DA COMUNIDADE INDÍGENA SATERÉ MAWÉ, AMAZONAS
ALINNE COSTA CAVALCANTE REZENDE
MANAUS-AM
MARÇO/2020
ALINNE COSTA CAVALCANTE REZENDE
CARACTERIZAÇÃO DAS FONTES DE RECURSOS TRÓFICOS PARA

ABELHAS DOS GÊNEROS MELIPONA E SCAPTOTRIGONA NAS
ÁREAS DA COMUNIDADE INDÍGENA SATERÉ MAWÉ, AMAZONAS
Tese de doutorado apresentada ao Programa de Pós-

Graduação em Biodiversidade e Biotecnologia da
Rede BIONORTE, no Instituto Nacional de Pesquisas
da Amazônia-INPA, como requisito parcial para a
obtenção do Título de Doutor em Biodiversidade e
Conservação e Biotecnologia.
Orientadora: Dra. Maria Lúcia Absy

Coorientador: Dr. Marcos Gonçalves Ferreira
MANAUS/AM
MARÇO/2020
SEDAB/INPA © 2019 - Ficha Catalográfica Automática gerada com dados fornecidos pelo(a) autor(a)
Bibliotecário responsável: Jorge Luiz Cativo Alauzo - CRB11/908
R467c Rezende, Alinne Costa Cavalcante

Caracterização das fontes de recursos tróficos
para abelhas dos gêneros Melipona e Scaptotrigona
nas áreas da comunidade indígena Sateré Sawé,
Amazonas / Alinne Costa Cavalcante Rezende;
orientadora Maria Lúcia Absy; coorientador Marcos
Gonçalves Ferreira. -- Manaus:[s.l], 2020.
106 f.
Tese (Doutorado - Programa de Pós Graduação em

Botânica) -- Coordenação do Programa de Pós-Graduação,
INPA, 2020.
1. Palinologia. 2. Melissopalinologia. 3. Rede

de interação. 4. Meliponini. I. Absy, Maria Lúcia,
orient. II. Ferreira, Marcos Gonçalves, coorient.
III. Título.
CDD: 580
ii
Dedico!
A Deus, meus pais Daniel e Marlene Cavalcante, meu

marido Helton Marshall e querido filho Arthur Marshall
e em especial minha vovó Conceição.
iii
AGRADECIMENTOS
Em primeiro lugar eu agradeço a Deus em quem eu acredito e que me ajudou em toda

a jornada e tem realizado meus sonhos.
Ao Programa de Pós-Graduação em Biotecnologia e Biodiversidade da Bionorte por
todo o apoio recebido, em especial ao Coordenador Dr. Jair Max Furtunato Maia e a secretária
Tânia pelo esforço e carinho.
A Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM) pela
concessão da bolsa de estudos.
Ao Laboratório de Palinologia do Instituto Nacional de Pesquisas da Amazônia
(INPA) por toda a infraestrutura para a realização deste trabalho.
A minha orientadora Profa. Dra. Maria Lúcia Absy que dedicou seu tempo para me
orientar e que além disso tornou-se uma grande amiga e serei eternamente grata por tudo.
Ao meu querido amigo, irmão e coorientador Prof. Dr. Marcos Gonçalves Ferreira que
me ensinou com muita paciência o mundo das abelhas e pólen. Muito obrigada por tudo que
fez por mim, eu nem tenho palavras para agradecer. Você é fera!
A Dra. Helyde Albuquerque Marinho e Otilene dos Anjos Santos pela coleta de todo
o material.
Aos amigos do Laboratório de Palinologia pela amizade e companheirismo, Bianca,
Alyne, Mayra, Natália. Com vocês o dia a dia no laboratório é sempre mais divertido. Valeu
amigas!
Aos docentes do Programa de Pós-Graduação em Biotecnologia e Biodiversidade da
Bionorte por todo conhecimento transmitido.
Aos discentes do Programa de Pós-Graduação em Biotecnologia e Biodiversidade da
Bionorte 2016 pela amizade.
Aos meus pais Daniel e Marlene que sempre acreditaram em mim (mesmo eu não
acreditando), sou grata por tudo o que fizeram por mim. Amo vocês!
Ao meu marido Helton Marshall que me apoiou em todo o momento e esteve ao meu
lado nas alegrias e nos momentos mais tristes. Também ao meu filho amado Arthur Marshall
que sempre entendeu meu trabalho e minhas ausências. Amo muito vocês!
A minha querida vovó Conceição (ursinho) que me sustentou com suas orações e
conselhos. Te amo vozinha!
Aos meus irmãos Danielle, Eduardo, cunhados Iellen e Aninha e sobrinhos Felipe e
Daniel que são meu porto seguro e me deram força nessa caminhada. Vocês são demais!
iv
Aos meus sogros Vicente Marçal e Eliminair (in memoriam) que me apoiaram nessa
caminhada. Sou grata pelas orações.
A todos meus familiares e amigos (tios, tias, primos e primas) que sempre torceram
por mim, em especial a minha amiga Jéssica Cardeal e Quezia Yasugui pela amizade e apoio.
Agradeço por esse privilégio de atuar na pesquisa, um trabalho que amo e aprendi
muito. Deus proporcionou amizades que guardarei para sempre no meu coração.
v
Então disse Deus: "Cubra-se a terra de vegetação:

plantas que dêem sementes e árvores cujos frutos
produzam sementes de acordo com as suas espécies".
Gênesis 1:11
vi
RESUMO
Abelhas da tribo Meliponini formam um grupo bastante diverso de abelhas sociais e exibem
enorme plasticidade, nichos e comportamentos. Para compreender esse universo entre abelha e
planta, a palinologia é uma ferramenta eficaz que gera informações importantes desta interação.
O objetivo deste trabalho foi analisar os recursos tróficos sob o ponto de vista palinológico das
colônias de diferentes espécies de abelhas dos gêneros Melipona e Scaptotrigona. Foram
identificadas amostras de pólen e mel coletados por abelhas dos gêneros Melipona Illiger, 1806
e Scaptotrigona Moure, 1942 criadas em comunidades da tribo indígena Sateré Mawé. As
amostras foram coletadas nas comunidades Ilha Michiles, Nova Esperança, Monte Horeb, Nova
América e Vila Nova II localizadas ao longo do Rio Marau no município de Maués, Amazonas,
Brasil (3°39'45.00"S, 57°20'17.99''W). As coletas deste trabalho fizeram parte do projeto
“Abelhas Nativas da Área Indígena Sateré Mawé: Mapeamento da Polinização e Caracterização
dos Produtos Meliponícolas”. Foram coletados amostras de mel (potes) na comuinidade Ilha
Michiles com a abelha Scaptotrigona nigrohirta (4 potes), Nova Esperança com Scaptotigona
sp. (9 potes) e Melipona seminigra (6 potes), Monte Horeb com Melipona seminigra (8 potes),
Nova América com Melipona seminigra (5 potes), Melipona dubia (4 potes), Melipona sp. (6
potes) e Scaptotrigona sp. (7 potes), totalizando 49 amostras de mel. Para as amostras de pólen,
foram coletados na comunidade Vila Nova II com Melipona dubia (8 potes), Nova Esperança
com Melipona seminigra (21 potes) e Nova América com Scaptotrigona sp. (22 potes),
totalizando 51 amostras. Em relação as amostras de mel, as famílias de plantas mais importantes
neste estudo foram: Anacardiaceae, Arecaceae, Burseraceae, Dichapetalaceae, Dilleniaceae,
Eufhorbiaceae, Fabaceae, Lecythidaceae, Polygalaceae, Myrtaceae, Melastomataceae,
Rhamnaceae e Salicaceae. Para as amostras de pólen as famílias de plantas mais representativas
foram: Melastomataceae, Anacardiaceae, Euphorbiaceae, Dilleniaceae, Myrtaceae e Fabaceae
(Mimosoideae e Caesalpinioideae). Mesmos sendo abelhas generalistas, este estudo observou
preferência de tipos polínicos relacionados ao gênero de abelha, por exemplo em amostras de
pólen o gênero Melipona possui alta atratividade com Miconia tipo, Já Scaptotrigona possui
preferência por Croton cajucara. Foi observado também que abelhas de espécies diferentes na
mesma comunidade apresentaram índices de sobreposição significativos. Outro fator
importante foi que em todas as amostras de mel e pólen, a formação de dois grupamentos (um
para espécies de Melipona e outro para espécies de Scaptotrigona). Apesar das particularidades
de cada grupo de abelha, o terceiro capítulo mostrou um alto grau de aninhamento e uma alta
generalização de rede que foi constatado pelo índice de conectância. Este estudo demonstra a
vii
importância dessas plantas para a manutenção dessas abelhas e para o desenvolvimento da

meliponicultura do Amazonas.
viii
ABSTRAT
Bees from the Meliponini tribe form a fairly diverse group of social bees and exhibit enormous
plasticity, niches and behaviors. To understand this universe between bee and plant, palynology
is the tool capable of providing important information about this interaction. The objective of
this work was to analyze the trophic resources from a palynological point of view for different
bee species colonies of the genera Melipona and Scaptotrigona. Pollen and honey samples
collected by bees from the genera Melipona Illiger, 1806 and Scaptotrigona Moure, 1942
were identified from communities of the Sateré Mawé indigenous tribe. The samples were
collected in the Ilha Michiles, Nova Esperança, Monte Horeb, Nova América and Vila Nova II
communities located along the Marau River in the municipality of Maués, Amazonas, Brazil
(3°39'45.00"S, 57°20'17.99''W). The collections of this work were part of the project "Native
Bees of the Sateré Mawé Indigenous Area: Mapping Pollination and Characterizing
Meliponiculture Products. Honey samples (pots) were collected from Scaptotrigona nigrohirta
bees (4 pots) from the Michiles Island bee community, Scaptotigona sp. (9 pots) and Melipona
seminigra (6 pots) from Nova Esperança, Melipona seminigra (8 pots) from Monte Horeb,
and Melipona seminigra (5 pots), Melipona dubia (4 pots), Melipona sp. (6 pots) and
Scaptotrigona sp. (7 pots) from Nova America, totaling 49 honey samples. Pollen samples
were collected from Melipona dubia (8 pots) in the Vila Nova II community, Melipona
seminigra (21 pots) from Nova Esperanca and Scaptotrigona sp. (22 pots) from Nova
America, totaling 51 samples. Regarding honey samples, the most important plant families in
this study were: Anacardiaceae, Arecaceae, Burseraceae, Dichapetalaceae, Dilleniaceae,
Eufhorbiaceae, Fabaceae, Lecythidaceae, Polygalaceae, Myrtaceae, Melastomataceae,
Rhamnaceae and Sacelicaae. For pollen samples, the most representative plant families were:
Melastomataceae, Anacardiaceae, Euphorbiaceae, Dilleniaceae, Myrtaceae and Fabaceae
(Mimosoideae and Caesalpinioideae). Even though all bees were generalists, a preference for
pollen type in relation to bee genus was found, ex. pollen samples demonstrated that the genus
Melipona has high affinity to Myconia type pollen, while Scaptotrigona prefers Croton
cajucara. Additionally, different bee species in the same community presented significant
overlapping indices. Another important factor was that two groups (one for Melipona species
and another for Scaptotrigona species) formed from all honey and pollen samples. Despite the
particularities of each bee group, the third chapter showed a high degree of nesting and a high
generalization of the network which was supported by the connectance index. This study
demonstrates the importance of these plants for maintaining these bees and for the development
of meliponiculture in Amazonas.
ix
LISTA DE FIGURAS
Figura 1: Mapa das comunidades Sateré Mawé localizadas no município de Maués,

Amazônia, Brasil. Legenda: Ocas destacadas em preto identifica as cinco comunidades
onde foram feitas as coletas. (MH: Monte Horeb, VN: Vila Nova II, NE: Nova Esperança,
IM: Ilha Michiles e NA: Nova América). Fonte: Adaptado de Teixeira (2005) ............... 8
Figura 2: Mapa com a distribuição geográfica das espécies de abelhas sem ferrão utilizadas
nesse estudo. Fonte: http://moure.cria.org.br/catalogue......................................................8
Capítulo I
Figure 1- General location of the study area, encompassing three indigenous communities
(Ilha Michiles, Nova Esperança, and Monte Horeb), located along the edges of the Marau
River in the municipality of Maués, state of Amazonas, Brazil (Source: Qgis). .............. 15
Plate 1- Photomicrographs of predominant pollen types found in honey samples of

Melipona seminigra, Scaptotrigona sp., and Scaptotrigona nigrohirta from three
communities (Ilha Michiles, Nova Esperança, and Monte Horeb). Alchornea type (1, 2);
Alchornea triplinervia (3, 4); Amanoa guianensis (5, 6); Bredemeyera floribunda (7, 8);
Diplotropis purpurea (9, 10); Doliocarpus type (11, 12); Eschweilera tenuifolia (13, 14);
Eugenia type (15, 16). Scale bars: 10 µm. ........................................................................ 26
Plate 2- Photomicrographs of predominant pollen types found in honey samples of

Melipona seminigra, Scaptotrigona sp., and Scaptotrigona nigrohirta from three
communities (Ilha Michiles, Nova Esperança, and Monte Horeb). Miconia type (1, 2);
Protium heptaphyllum (3, 4); Sclerolobium hypoleucum (5, 6); Tapirira guianensis (7, 8).
Scale bars: 10 µm. ............................................................................................................. 27
Figure 2- Bipartite graph showing the presence or absence of trophic interactions between
four bee colonies from three indigenous communities and the pollen types present in the
honey samples. NE-S (Nova Esperança-Scaptotrigona sp.), NE-Ms (Nova Esperança-
Melipona seminigra), MH-Ms (Monte Horeb–Melipona seminigra), IM-Sn (Ilha Michiles-
Scaptotrigona nigrohirta). ................................................................................................. 28
x
Figure 3- Bipartite graph showing the proportion of trophic interactions between four bee
colonies from three indigenous communities, and the main pollen types present in honey
samples. NE-S (Nova Esperança-Scaptotrigona sp.), NE-Ms (Nova Esperança-Melipona
seminigra), MH-Ms (Monte Horeb–Melipona seminigra), IM-Sn (Ilha Michiles-
Scaptotrigona nigrohirta). ................................................................................................. 29
Figure 4- Cluster analysis of bee species per community, according to pollen type
similarity, based on Euclidian distances. Legend: NE-S (Nova Esperança-Scaptotrigona
sp.), NE-Ms (Nova Esperança-Melipona seminigra), MH (Monte Horeb–Melipona
seminigra), IM-Sn (Ilha Michiles-Scaptotrigona nigrohirta). .......................................... 30
Capítulo II
Figure 1- Nova América indigenous community, located on the lands of the indigenous
Sateré Mawé people, on the banks of the Marau River, Maués municipality, Amazonas
state, Brazil (Qgis). ............................................................................................................ 43
Figure 2- Photomicrographs of predominant pollen types found in honey samples of

Melipona seminigra, Melipona dubia, Melipona sp. and Scaptotrigona sp. from Nova
América community. Alchornea type (A,B); Alchornea triplinervia (C,D); Croton type
(E,F); Dicorynia paraenses (G,H); Doliocarpus type (I,J); Eugenia type (K,L). Scale bars:
10 mm. ............................................................................................................................... 47
Figure 3- Photomicrographs of predominant pollen types found in honey samples of

Melipona seminigra, Melipona dubia, Melipona sp. and Scaptotrigona sp. from Nova
América community. Gouania blanchetiana (A,B); Miconia type (C,D); Protium
heptaphyllum (E,F); Stryphnodendron guianense (G,H); Tapirira guianensis (I,J); Tapura
lanceolata (K,L). Scale bars: 10 mm................................................................................. 48
Figure 4- A) Values of diversity (H’) and evenness (J’) of the four species of bees; B)
Overlapping values for the four bee species. Captions: Scaptotrigona sp. (S), Melipona
dubia (Md), Melipona sp. (M) and Melipona seminigra (Ms). ......................................... 52
Figure 5- Pollen diagram showing the frequencies of pollen types for each bee. Ms:
Melipona seminigra; Md: Melipona dubia; M: Melipona sp.; S: Scaptotrigona sp. ........ 53
xi
Figure 6- Bipartite graph showing the presence or absence of trophic interactions between
four stingless bee species at the Nova América indigenous community and the pollen types
present in the honey samples. ............................................................................................ 54
Capítulo III
Figure 1: Collection site with the three communities: Nova América, Nova Esperança and
Vila Nova II, located on the banks of the Marau River in the municipality of Maués,
Amazonas State, Brazil (Source: Qgis)…………………………………………………...68
Figure 2: Photomicrographs of predominant pollen types found in pollen samples from

Melipona dubia, Melipona seminigra and Scaptotrigona sp. in the Nova América, Nova
Esperança and Vila Nova II indigenous communities. Alchornea type (A,B); Amanoa
guianensis (C,D); Cassia type (E,F); Croton cajucara (G,H); Doliocarpus type (I,J);
Eugenia type (K,L); Maximiliana maripa (M,N); Miconia type (O,P). Scale bars: 10 mm.
........................................................................................................................................... 73
Figure 3: Photomicrographs of predominant pollen types found in pollen samples of
Melipona dubia, Melipona seminigra and Scaptotrigona sp. in the Nova América, Nova
Esperança and Vila Nova II indigenous communities. Mimosa pudica (A,B); Protium
heptaphyllum (C,D); Sclerolobium hypoleucum (E,F); Sebastiana brasiliensis (G,H);
Spondias mombin (I,J); Stryphnodendron guianense (K,L). Scale bars: 10
mm……………………………………………………………………………………….74
Figure 4: Diversity (H') and similarity (J') values for the three bee species: Melipona
dubia, Melipona seminigra and Scaptotrigona sp………………………………………..83
Figure 5: A) Bipartite graph showing the presence and absence of trophic interaction
between the three bee species in three indigenous communities (Nova América, Nova
Esperança and Vila Nova II). B) NODF graph based on the presence and absence matrix
of pollen samples from the three bee species in three indigenous communities. C) WNODF
graph based on quantitative matrix of pollen samples from three bee species in three
indigenous communities………………………………………………………………….84
xii
Figure 6: Pollen and cluster diagram showing the frequency of pollen types and the
formation of each bee group. Key: Md: Melipona dubia; Ms: Melipona seminigra; S:
Scaptotrigona sp.................................................................................................................85
LISTA DE TABELAS
Capítulo I
Table 1- Table 1: Frequency of pollen types present in honey from Scaptotrigona

nigrohirta bees from the Ilha Michiles community, located along the edges of the Marau
River in the municipality of Maués, state of Amazonas, Brazil. P (Pot)........................... 18
Table 2- Frequency of pollen types present in honey from Scaptotrigona sp. bees from the
Nova Esperança community, located along the edges of the Marau River in the
municipality of Maués, state of Amazonas, Brazil. P (pot). .............................................. 19
Table 3- Frequency of pollen types present in honey from Melipona seminigra from the
Nova Esperança community, located along the edges of the Marau River in the
municipality of Maués, state of Amazonas, Brazil. P (Pot). ............................................. 21
Table 4- Frequency of pollen types present in honey from Melipona seminigra bees from
the Monte Horeb community, located along the edges of the Marau River in the
Capítulo II
Table 1- Frequency of pollen types present in honey from Melipona seminigra bees from
the Nova América community, located along the edges of the Marau River in the
Table II- Frequency of pollen types present in honey from Melipona dubia bees from the
Nova América community, located along the edges of the Marau River in the municipality
of Maués, state of Amazonas, Brazil. P (Pot). ................................................................... 49
Table III- Frequency of pollen types present in honey from Melipona sp. bees from the
Nova América community, located along the edges of the Marau River in the municipality
of Maués, state of Amazonas, Brazil. P (Pot). ................................................................... 50
xiii
Table IV- Frequency of pollen types present in honey from Scaptotrigona sp. bees from
the Nova América community, located along the edges of the Marau River in the
Capítulo III
Tab1e 1- Frequency of pollen types in pollen pots collected by Melipona dubia in the Vila
Nova II indigenous Community, located between the Marau river in the municipality of
Maués, Amazonas, Brazil. P (Pots)....................................................................................71
Table 2- Frequency of pollen types in pollen pots collected by Melipona seminigra in the
Nova Esperança indigenous community, located between the Marau river in the
municipality of Maués, Amazonas, Brazil. P (Pots).........................................................76
Table 3: Frequency of pollen types in pollen pots collected by Scaptotrigona sp. in the
Nova América indigenous, located between the Marau river in the municipality of Maués,
Amazonas, Brazil. P (Pots)...............................................................................................80
xiv
SUMÁRIO
RESUMO.......................................................................................................................... vi
ABSTRACT ..................................................................................................................... viii
LISTA DE FIGURAS...................................................................................................... ix
LISTA DE TABELAS ..................................................................................................... xii
1 INTRODUÇÃO ............................................................................................................ 1
2 OBJETIVOS ................................................................................................................. 2
3 REVISÃO BIBLIOGRÁFICA .................................................................................... 3

3.1 Abelhas sem ferrão .................................................................................................. 3
3.2 Déficit de polinizadores........................................................................................... 4
3.3 Palinologia ................................................................................................................ 5
3.4 Tribo indígena Sateré Mawé .................................................................................. 6
4 MATERIAL E MÉTODOS.......................................................................................7
4.1 Área de estudo..........................................................................................................7
4.2 Espécies de abelhas..................................................................................................8
4.3 Coleta e preparação das amostras de pólen e mel................................................9
4.4 Processamento químico e identificação polínica...................................................9
4.5 Análise estatística....................................................................................................10
Capítulo I. Pollen of honey from Melipona seminigra merrillae Cockerell, 1919,

Scaptotrigona nigrohirta Moure, 1968 and Scaptotrigona sp. Moure, 1942 (Apidae:
Meliponini) reared in Sateré Mawé indigenous communities, Amazon, Brazil. .............. 12
Capítulo II. Honey botanical origin of stingless bees (Apidae: Meliponini) in the nova américa
community of the sateré mawé indigenous tribe, Amazon, Brazil. ................................... 39
Capítulo III. Pollen niche of Melipona dubia Moure & Kerr, 1950, Melipona seminigra
Cockerell, 1919 and Scaptotrigona sp. Moure, 1942 (Apidae:Meliponini) kept in indigenous
communities of the Sateré Mawé tribe, Amazonas, Brazil…….........................................65
xv
4 CONCLUSÃO............................................................................................................... 96
5 REFERÊNCIAS ........................................................................................................... 98
6 ANEXOS ....................................................................................................................... 106

1
1 INTRODUÇÃO
A Amazônia possui a maior biodiversidade do mundo, entretanto, nos últimos anos, esse
ecossistema vem sendo explorado intensamente afetando a cobertura vegetal e
consequentemente, os polinizadores, principalmente as abelhas sem ferrão (Ferreira et al.,
2005; Biesmeijer et al., 2006). Essas abelhas, consideradas como importantes visitantes florais
de várias espécies botânicas, constituem um elemento importante na manutenção da
biodiversidade (Kerr 1996).
As abelhas têm sofrido um declínio alarmante, entre as principais causas desse declínio
estão o desmatamento (perda do habitat), agroquímica, patógenos e mudanças climáticas (Potts
et al., 2010a; Breeze et al., 2011; Giannini et al., 2012). Na Europa, por exemplo, desde 1965,
vem ocorrendo esse declínio, trazendo consequências negativas para a produção na agricultura,
sendo que 84% da colheita de espécies cultivadas dependem principalmente das abelhas (Gallai
et al., 2009; Potts et al., 2010b). No Brasil, este cenário não é diferente, pois as populações de
abelhas nativas vêm diminuindo devido à perda de habitat, invasão de espécies exóticas,
poluição e mudanças climáticas (Lopes 2005; Antunes 2012).
Além da importância dos processos ecológicos da interação inseto e planta, as abelhas
sem ferrão possuem, também, uma importância econômica verificada na meliponicultura, uma
atividade sustentável e rentável que sustenta muitas comunidades (Nogueira-Neto 1997). A
produção de mel da região amazônica vem se destacando com a criação de abelhas nativas
manejadas por comunidades tradicionais e indígenas, contribuindo também na preservação
vegetal, pois está relacionada com a oferta de recursos (néctar e pólen) (Costa et al., 2012).
Nesse contexto, estudos palinológicos são essenciais, pois podem contribuir para
elucidar as interações entre polinizadores e espécies de plantas nativas (Novais et al., 2012;
Vossler et al., 2014). Na Amazônia foram realizados vários estudos demonstrando que a
utilização de recursos das abelhas depende da disponibilidade de alimento (pólen e néctar),
reforçando a importância da preservação da flora para a manutenção das abelhas (Oliveira et
al., 2009; Novaes e Absy 2013).
As comunidades indígenas da tribo Sateré Mawé possuem como atividade principal a
cultura agrícola, sendo que 97% do destino da produção é para o consumo pessoal e a outra
parcela é comercializada (Teixeira 2005). A meliponicultura vem ganhando um espaço
significativo, gerando benefícios econômicos para a população dessas comunidades (Belém et
al., 2011; Marinho et al., 2013).
O conhecimento sobre a flora explorada pelas abelhas na Amazônia é fundamental para
programas de manejo, extensão da atividade meliponícola e caracterização botânica (origem do
2
pólen). Dessa forma, através do conhecimento botânico, o meliponicultor poderá adquirir

informações sobre as plantas que manterão a sua produção, como também a conservação das
colônias (Ferreira e Absy 2013).
Portanto, o presente trabalho visou ampliar o conhecimento sobre as espécies de plantas
visitadas por espécies de abelhas dos gêneros Melipona e Scaptotrigona das comunidades da
tribo Sateré Mawé fornecendo informações que serão estratégicas para constituição de uma
pastagem meliponícola apropriada que é utilizada por espécies de abelhas criadas em diferentes
comunidades.
2 OBJETIVOS
2.1 Geral
Analisar os recursos tróficos sob o ponto de vista palinológico das colônias de
diferentes espécies de abelhas dos gêneros Melipona e Scaptotrigona (Apidae: Meliponini)
em comunidades da tribo indígena Sateré Mawé.
2.2 Específicos
• Identificar os tipos polínicos em amostras de mel coletadas em colônias de abelhas dos
gêneros Melipona e Scaptotrigona provenientes das comunidades indígenas Sateré Mawé.
• Identificar os tipos polínicos em amostras de pólen coletadas em colônias de abelhas
dos gêneros Melipona e Scaptotrigona provenientes das comunidades indígenas Sateré
Mawé.
• Analisar a partir dos índices ecológicos, a diversidade e uniformidade na utilização dos
recursos tróficos relacionados às espécies dos gêneros Melipona e Scaptotrigona em
comunidades indígenas Sateré Mawé, localizadas a margem do rio Marau.
• Avaliar o nível de sobreposição trófica em amostras de pólen e mel de espécies dos
gêneros Melipona e Scaptotrigona provenientes das comunidades indígenas Sateré Mawé.
• Representar e analisar a estrutura de rede de interações entre abelhas sem ferrão
(Melipona e Scaptotrigona) e o grupo de plantas que ocorrem em diferentes comunidades
indígenas da tribo Sateré Mawé.
3
3 REVISÃO BIBLIOGRÁFICA
3.1 Abelhas sem ferrão
De uma forma geral, as abelhas possuem comportamento solitário ou social, em que

abelhas solitárias são caracterizadas pela independência da fêmea na nidificação, ou seja, elas
constroem e cuidam dos seus próprios ninhos, diferentemente das abelhas sociais que
apresentam sociabilidade, desempenhando uma divisão de trabalho (Batra 1984; Michener
2007). A escolha de um local é um fator limitante para o aumento da espécie de uma abelha,
pois no processo de nidificação, as abelhas utilizam uma variedade de substratos (árvores,
cavidades do solo, termiteiros e pedras) que servem para proteção e nutrição de sua prole
(Barreto e Castro 2007; Oliveira et al., 2012).
A tribo Meliponini, conhecida popularmente como abelhas sem ferrão, compreende
cerca de 60 gêneros com aproximadamente 600 espécies descritas, sendo que na Amazônia
concentra um maior número de espécies (Silveira 2002; Michener 2007; Rasmussen e Cameron
2010). Os meliponínios estão distribuídos nas regiões tropicais e subtropicais e possuem
características biológicas (morfologia, nidificação e interações comportamentais)
diferenciadas, variam de tamanho, possuem um corpo geralmente robusto e com mais pelagem
para o gênero Melipona Illiger, 1806 e, geralmente delgado e com menos pelos para os demais
gêneros. Os ninhos são construídos com materiais encontrados na natureza e a cera, substância
produzida pela própria abelha (Imperatriz-Fonseca et al., 1993; Oliveira et al., 2013). Além da
diferença de tamanho, outra característica que difere entre abelhas Melipona e Scaptotrigona é
a formação da rainha, em que para Melipona, as rainhas possui uma determinação trofo-
genética, ou seja, por predisposição genética interligada com a alimenentação (quantidade)
(Michener 1974). Já Scaptotrigona, o fator alimentar exerce uma grande importância, não só
na manutenção da prole, como na formação de rainhas, que nesse caso é exclusivamente
alimentar (Camargo 1972; Nogueira-Neto 1997).
Abelhas do gênero Melipona diferenciam-se de outros Meliponini, inclusive da maioria
dos Apidae, pela capacidade de extração de pólen por vibração da musculatura de vôo,
comportamento muito eficiente na coleta de pólen, tanto em anteras poricidas como anteras não
poricidas (Buchmann 1983, Proença 1992). Tal comportamento pode ser observado em várias
espécies botânicas melitófilas das famílias Myrtaceae, Fabaceae/Mimosoideae,
Melastomataceae, Solanaceae, além do gênero Cassia da família Fabaceae/Caesalpinioideae
(Roubik 1989, Ramalho et al., 1989, Endress 1996). Este gênero distribui-se em regiões
4
tropicais e subtropicais, sendo que 70% do total de espécies existentes encontram-se no Brasil
(Velthuis 1997).
Já o gênero Scaptotrigona apresenta na colmeia uma população que varia de 2.000 a
50.000 abelhas, sendo que elas alcançam uma amplitude maior na coleta devido a quantidade
de abelhas (Lindauer e Kerr 1960). Compreende aproximadamente 22 espécies distribuídas na
região neotropical, sendo muito utilizadas na produção de mel na região norte (Camargo e Pedro
2007; Marques-Souza et al., 2007).
A prática na criação dessas abelhas tem sido desenvolvida a bastante tempo em
diferentes regiões do Brasil, especialmente no norte e nordeste com meliponicultores em
comunidades tradicionais (Jaffé et al., 2015). O termo meliponicultura foi criado por Paulo
Nogueira Neto (1953), designando a criação de abelhas sem ferrão, possuindo características e
técnicas diferentes comparado a Apicultura (Criação de abelhas melíferas do gênero Apis).
Essas comunidades utilizam o mel e outras compostos (própolis e geoprópolis) que ajudam na
economia e também na sua própria subsistência (Peralta 1999; Belém et al., 2011).
3.2 Déficit de polinizadores
As interações entre inseto-planta são cruciais para a harmonia do ambiente, porém, nos
últimos anos, preocupações têm sido levantadas sobre o declínio das abelhas (Ghazoul 2005;
Solga et al., 2014). A perda e, consequentemente, a diminuição dos serviços de polinização são
causadas, principalmente pelas ações antrópicas, como por exemplo, a utilização exagerada de
inseticidas no combate as pragas que atacam as plantações, provocando a morte ou a mudança
no comportamento de abelhas (Freitas et al., 2009; Freitas e Pinheiro 2010).
Atividades como desmatamentos, fragmentação e queimadas provocam a destruição dos
ninhos das abelhas pois grande parte delas constroem seus ninhos em ocos de árvores, outras
preferem construir seus ninhos em cavidades pré-existentes no solo e essas ações antrópicas
tornam os locais de nidificação mais escassos (Oliveira et al., 1995). Outro fator preocupante
está relacionado com as mudanças climáticas, poisas abelhas são sensíveis a essas alterações
provocando a diminuição das mesmas (VanEngelsdorp et al., 2008; 2010).
O resultado desse declínio reflete negativamente na produção agrícola mundial, pois a
grande maioria das frutas consumidas é resultado do processo de polinização por insetos.
Economicamente, o valor total de culturas polinizadas por insetos é estimado em 510 milhões
de libras por ano no Reino Unido (Breeze et al., 2011). O custo real de substituir os serviços de
polinização prestados por esses insetos por polinização manual é estimado em R$ 1,8 bilhão
por ano (Breeze et al., 2011).
5
Nos Estados Unidos, houve uma perda de 35,9% de colônias de abelhas durante o
inverno de 2007-2009 (VanEngelsdorp et al., 2008; 2010). Também na Grã-Bretanhae Holanda
foram registradas a diminuição de abelhas ocasionadas pelas extinções locais de espécies
vegetais, resultando no declínio dos polinizadores (Biesmeijer et al., 2006).
No Brasil, também vem ocorrendo a diminuição acelerada de abelhas sem ferrão,
principalmente devido ao desmatamento de florestas nativas, onde estas abelhas
preferencialmente se instalam (Lopes et al., 2005). Estudo com abelhas nativas e seus recursos
florais em um fragmento de mata na região sudeste no Brasil, demonstrou que no local de estudo
existia pouca diversidade de espécies e de árvores de tronco oco, essencial para a nidificação,
promovendo a escassez de algumas espécies de abelhas (Antunes et al., 2012).
Com a preocupação desta perda de polinizadores, estudos de Gianne et al., (2012),
constataram que, futuramente áreas que abrigam abelhas polinizadoras no Brasil, poderão sofrer
uma redução drástica entre os anos de 2050 e 2080, representando um impacto negativo na
polinização.
3.3 Palinologia
A análise do pólen auxilia no entendimento sobre mecanismo de polinização, recursos

de forrageamento, rotas de migração, história evolutiva das plantas, ligações tróficas entre
outros (Jones e Jones 2001; Novais e Absy 2013).
Dentro da palinologia, a melissopalinologia é uma área que estuda os grãos de pólen
coletados e transportados por abelhas. Como exemplo, o conteúdo polínico do mel que pode
revelar características da flora visitada em diferentes ambientes (Oliveira 2009).
Alguns estudos da análise do pólen relacionados com a tribo Meliponini no mundo,
destacaram que essas abelhas sem ferrão demonstram preferências para determinadas espécies
de plantas e tendem a ser generalistas, também destacaram a importância de estudar essas
abelhas por seu valor ecológico e econômico (Sommeijeret al., 1983; Imperatriz-Fonseca et
al.,1989; Vit e D’albore 1994).
Na Amazônia, Absy e Kerr (1977) iniciaram o estudo com abelhas sem ferrão
identificando o pólen transportado pelas patas da espécie Melipona seminigra identificando 32
tipos polínicos. Continuando estudos relacionados ao gênero Melipona, Absy et al,. (1980)
analisaram o néctar de duas espécies (Melipona seminigra e Melipona rufiventris paraense) e
criaram tabelas mostrando as plantas visitadas por essas abelhas. Anos depois, Absy et al.,
(1984) estudaram em colônias de 22 espécies de abelhas (Meliponini) sendo identificados em
6
amostras de pólen 122 tipos polínicos com preferência de visita para as famílias Myrtaceae,
Arecaceae e Anacardiaceae.
Marques-Souza (1996) estudou o pólen transportado por Melipona compressipes
manaosensis e identificou 30 tipos polínicos distribuídos em 19 famílias e 22 gêneros.
Destacando, Cassia (Fabaceae/Caesalpinioideae) como à principal fonte de pólen, seguida por
Miconia (Melastomaceae) e Solanum (Solanaceae). Já em Marques-Souza (1999), analisou o
nicho trófico de duas espécies de Melipona na Amazônia, mostrando que essas abelhas possuem
preferências alimentares, sendo Fabaceae (Mimosoideae), Myrtaceae e Melastomataceae as
famílias mais visitadas. No entanto, Scaptotrigona sp. demonstrou ser mais generalista,
coletando 97 espécies distribuídas em 73 gêneros e 36 famílias.. Depois em 2007, Marques-
Souza et al., avaliaram o pólen transportado por Scaptotrigona fulvicutis, e verificaram a
preferência dessa abelha por plantas das famílias Fabaceae (Mimosoideae), Myrtaceae e
Sapindaceae.
Em Reck e Absy (2011a ; 2011b) , além de identificarem os tipos polínicos coletados
por abelhas sem ferrão ao longo do Rio Negro, onde estudaram sob o ponto de vista ecológico
a sobreposição desse nicho trófico e o agrupamento das espécies de abelhas através da
similaridade de coleta por cada espécie de abelha.
Da mesma forma Ferreira e Absy (2013; 2014; 2015; 2017a; 2017b) avaliaram o nicho
polínico e interações tróficas de abelhas do gênero Melipona na Amazônia, trabalharam com o
foco na meliponicultura tradicional. Mais recentemente, Absy et al., (2018), apresentaram uma
contribuição sobre o conhecimento da biodiversidade da Amazônia através do pólen coletado
pelas abelhas sem ferrão. Neste mesmo trabalho mostraram diversos protocolos de coletas de
pólen e a importância da identificação polinica para os meliponicultores, visando a criação de
abelhas como atividade sustentável.
3.4 Tribo indígena Sateré Mawé
A região onde se situa a tribo Sateré Mawé, está localizada em terra indígena na região
do médio do rio Amazonas. Possui cerca de 90 aldeias ao longo dos rios principais Marau e
Andirá com aproximadamente 1.600 famílias, sendo que a região que possui a maior ocupação
é Barreirinha com 50 aldeias e Maués com 37 aldeias (Teixeira 2005).
Entre as formas de subsistência das comunidades de Sateré Mawé estão à agricultura
com plantação de verduras, legumes e tubérculos, caça e pesca e a criação de animais, sendo
7
que em relação à caça e pesca, vem acontecendo o desaparecimento de animais e peixes devido
principalmente ao aumento populacional (Teixeira 2005).
A criação de abelhas sem ferrão vem ganhando grande importância entre os povos
amazônicos. Nesse sentido, nota-se a necessidade de introduzir informações que visam
beneficiar a prática da meliponicultura nas comunidades da tribo Sateré Mawé. Uma iniciativa
foi a publicação de uma cartilha sobre o manejo e a produção de mel por abelhas sem ferrão em
duas línguas (português e Sateré Mawé), facilitando a compressão e disseminação desses
conhecimentos (Marinho et al., 2013). Além disso, estudo palinológico realizado em três
comunidades da Tribo Sateré Mawé (Nova União, Vila Nova e Simão), mostrou que em 17
amostras de mel foram identificados 25 tipos polínicos, distribuídos em 17 gêneros e 12 famílias
botânicas, em que o tipo polínico mais representativo foi Tapirira guianensis, o qual foi
coletado pela abelhas Scaptotrigona sp. e Trigona sp. (Belém et al., 2011).
4 MATERIAL E MÉTODOS
4.1 Área de estudo
O Amazonas abrange uma região com 11.458,5km2 de extensão (Saraiva et al.,2009).

O clima é do tipo equatorial úmido, com temperatura média anual de 26,7º C, variando entre
23,3º C e 31,4º C. Há alternância de uma estação úmida chuvosa, de novembro a maio, e de
uma estação seca, de junho a outubro (Alvares 2013).
O material polínico e botânico analisados foram coletados durante a expedição
científica realizada no período de 23 a 31 de novembro de 2009 no âmbito do projeto, “Abelhas
Nativas da Área Indígena Sateré Mawé: Mapeamento da Polinização e Caracterização dos
Produtos Meliponícolas”coordenado pela Dra. Helyde Albuquerque Marinho. A coleta foi
realizada nas comunidades indígenas da Tribo Sateré Mawé localizada ao longo do Rio Maruá
3°39’45’’Se 57°20’17’’W que compreende a região do Médio rio Amazonas, na divisa dos
estados do Amazonas e do Pará. Possui cerca de 788.528 hectares de terras contínuas que
pertencem geograficamente a três municípios do Amazonas: Maués, Barreirinha e Parintins e
dois no Pará: Itaituba e Aveiro (Teixeira 2005). Neste estudo foram escolhidas cinco
comunidades (Ilha Michiles, Nova Esperança,Vila Nova II, Monte Horeb, Nova América)
(Figura 1).
8
Figura 1: Comunidades Sateré Mawé localizadas no município de Maués, Amazônia, Brasil. Legenda: Ocas
destacadas em preto identifica as cinco comunidades onde foram feitas as coletas. (MR:Monte Horeb, VN: Vila
Nova II, NE: Nova Esperança, IM: Ilha Michiles e NA: Nova América). Fonte: Adaptado de Teixeira (2005).
Essa área tem como característica vegetal campos de várzea alagáveis no período de
cheia, sendo que a vazante serve como campo de pastagem predominando espécies herbáceas
da família Poaceae.(Aquino et al.,1978; Nascimento e Laurance 2006).
4.2 Espécies de abelhas
Para o gênero Melipona Illiger, 1806, as espécies para esse estudo são: Melipona
seminigra e Melipona dubia que possuem distribuição na região Neotropical do Brasil com
predominância na Amazônia (Camargo e Pedro 2013). Para o gênero Scaptotrigona Moure
1942, aqui representado por Scaptotrigona sp. e Scaptotrigona nigrohirta, a sua distribuição
ocorre desde o México e toda região Neotropical (Figura 2).
Figura 2: Distribuição geográfica das espécies de abelhas sem ferrão utilizadas nesse estudo. Fonte:
http://moure.cria.org.br/catalogue.
9
4.3 Coleta e preparação das amostras de pólen e mel
Um total de 52 amostras de pólen e 48 de mel das cinco comunidades foram estudadas.

As amostras foram coletadas, período matutino das 07h00mn as 12h00mn, diretamente nos
potes (mel e pólen). O pólen foi obtido nos potes em ninhos naturais com o auxílio de canudos
plásticos que foram introduzidos em várias inserções em cada pote retirando uma quantidade.
Em seguida, foram armazenados separadamente em tubos (Eppendorf) de 2mL e/ou sacos
plásticos hermeticamente fechados e esterilizados. As amostras de mel foram coletadas com o
auxílio de uma seringa e posteriormente acondicionadas em tubos falcon de 50mL.
Paralelamente, foi coletado material botânico em floração ou frutificação em cada
comunidade. Esse material auxiliou como referência para as análises palinológicas das amostras
de mel e de pólen coletadas nas colmeias. Foram coletadas plantas frutíferas introduzidas e
nativas cultivadas ao redor das casas: ervas, arbustos e árvores que ocorrem na capoeira e na
vegetação da várzea. Todo o material botânico foi prensado em folhas de jornal e acondicionado
em sacos plásticos. Posteriormente, foi adicionado álcool etílico ao material para assegurar a
integridade das folhas, flores e frutos e evitar a proliferação de fungos. O material botânico foi
incorporado ao acervo do herbário do INPA.
4.4 Processamento químico e identificação polínica
As amostras de pólen foram acondicionadas em tubos falcon de 15mL contendo 5mL

de ácido acético e mantidas por um período mínimo de 24 horas. Posteriormente, foram
submetidas ao processo de acetólise (Erdtman 1960). Para a separação do pólen contido no mel,
a acetólise foi precedida pela diluição de 10mL das amostras de mel em 20 mL de água destilada
e álcool (1:1) e levemente aquecida (40°C), seguida de duas centrifugações (10mn, 3500rpm)
e a completa separação do sedimento polínico (Louveaux et al., 1978). Por fim, os grãos de
pólen foram montados em gelatina glicerinada e as lâminas lutadas com parafina (Kisser 1935).
Para cada amostra, quando necessário, foi confeccionado um conjunto de três lâminas de pólen.
As identificações e fotomicrografias dos grãos de pólen foram realizadas com o auxilio
de um microscópio Zeiss modelo “Primo Star” contendo uma câmera Canon “Power Shot
A650IS” e ocular micrométrica acoplados. Para comparações palinológicas foi utilizado a
Palinoteca de referência do Laboratório de Palinologia do INPA (Instituto Nacional de
Pesquisas da Amazônia) e consultada bibliografia especializada (Roubick e Moreno 1991).
10
4.5 Análise estatística
Para a análise quantitativa, foram contabilizados 600 grãos para cada amostra (Vergeron
1964). Nas amostras de pólen foram utilizadas duas categorias de porcentagem propostas por
Ramalho et al., (1985), onde 10% representa a quantidade mínima para que a planta seja
considerada atrativa para a abelha e a outra para inferência de eventos de “especialização
temporária” (coleta concentrada a partir de uma fonte específica de pólen) onde a representação
mínima será 90%.
Já para o pólen contido no mel foi utilizada a caracterização proposta por Louveaux et
al., (1978) e Novais et al., (2012) em que as frequências serão determinadas em pólen
dominante (>45%); pólen secundário (≤45%–>15%); pólen de menor importância (≤15% –
≥3%) e pólen raro (<3%).
Para os índices ecológicos, foi calculado o índice de diversidade (H’) de Shannon-
Weaver (1949) em H’= ∑(pi.lnpi), onde H’ é o índice de diversidade, (pi) é a proporção de cada
tipo polínico encontrado nas amostras e (ln) o logaritmo natural. O índice de Pielou (1977) foi
utilizado para indicar a homogeneidade ou heterogeneidade de coleta das abelhas em cada
comunidade pela fórmula J’ = H’/H’max, sendo H’ o índice diversidade e H’max o logaritmo
natural do total de número de tipos polínicos presentes nas amostras. O teste t foi aplicado para
comparar a diversidade entre as amostras e entre comunidades distintas. O índices ecológicos
e testes foram gerados através do programa Past.
O índice de sobreposição foi utilizado para espécies de abelhas criadas em uma mesma
comunidade, sendo calculado a partir de Pianka (1973) em que Oik= ∑pijpik / √pij2 ∑ pik2, onde
pij é a proporção de tipos de polínicos na amostra para uma espécie e pik é o valor
correspondente à outra espécie de abelha. O índice de sobreposição varia de 0 a 1 e é
considerado biologicamente significativo ao atingir um valor maior ou igual a 0,6 (Zaret e Rand
1971; Wallace 1981).
O conjunto de interações entre as abelhas sem ferrão estudadas e os recursos coletados
foram representados através de grafos bipartidos gerados através do programa R (pacote:
bipartite). A fim de determinar a similaridade e frequência dos tipos polínicos, foi realizada
uma análise de cluster (sinal filogenético) juntamente com um diagrama polínico, a partir das
famílias botânicas mais representativas nas amostras foi obtida através programa R.
As métricas de rede foram verificadas a partir da conectância e do grau de aninhamento,
em que a conectância foi obtida pela fórmula C = E/AP, em que C é a razão entre o número de
interações observadas, E os tipos polínicos identificados e AP o universo de interações
possíveis (A= número de espécies de abelhas envolvidas e P= quantidade de plantas com
11
potencial melíferas do local). Já o aninhamento foi determinado a partir do NODF (Nestedness

Metric Based On Overlap And Decreasing Fill), usando o modelo nulo CC (cored rows, cored
columns), estimulado devido sua consistência teórica (Guimarães & Guimarães, 2006).
Também foi utilizadoo WNODF, a partir do modelo nulo RCTA (Row and Column Totals
Average) baseado na matriz quantitativa dos dados (Almeida-Neto & Ulrich, 2011). Para
ambas as métricas, foi utilizado o software FALCON (a software package for analysis of
nestedness in bipartite networks) carregado através da plataforma R (Beckett et al., 2014).
12
CAPÍTULO I
REZENDE, A.C.C; ABSY, M.L.; FERREIRA, M.G;

MARINHO, H.M; SANTOS, O.A. Pollen of honey from
Melipona seminigra merrillae Cockerell, 1919, Scaptotrigona
nigrohirta Moure, 1968 and Scaptotrigona sp. Moure, 1942
(Apidae: Meliponini) reared in Sateré Mawé indigenous
communities, Amazon, Brazil
In: Palynology 42(2): 255-267
doi:10.1080/01916122.2018.1458664
13
Pollen of honey from Melipona seminigra merrillae Cockerell, 1919; Scaptotrigona

nigrohirta Moure, 1968; and Scaptotrigona sp. Moure, 1942 (Apidae: Meliponini) reared
in Sateré Mawé indigenous communities, Amazon, Brazil
Abstract: Honey samples from stingless bees (tribe Meliponini) were analyzed in three Sateré
Mawé indigenous communities located along the edges of the Marau River in the state of
Amazonas, Brazil. Twenty-nine pollen types were identified for the Scaptotrigona nigrohirta
colonies from the Ilha Michiles community, 43 for the Scaptotrigona sp. colonies and 39 for
the Melipona seminigra colonies from the Nova Esperança community, and 34 for the M.
seminigra colonies from the Monte Horeb community. Regarding the presence or absence of
different pollen types in the samples, from the 65 pollen types identified, five were exclusive
for the Scaptotrigona sp. from Nova Esperança, five for M. seminigra from Monte Horeb, six
for Scaptotrigona from Ilha Michiles, and 13 for M. seminigra from Nova Esperança. Of the
main pollen types identified (n=22), the Miconia type had the highest proportion and was the
only type shared by the bees from the three communities. The present study indicates a list of
important plants to be included in bee pastures for the studied bees in the Amazon, with the aim
of developing stingless beekeeping as a subsistence activity in indigenous communities.
Keywords: Amazon, meliponiculture, pot honey, trophic resources, stingless bee.

14
Introduction
Meliponini bees are commonly known as stingless bees and are strongly connected to
tropical forest plant species, performing pollination while collecting for resources such as nectar
and pollen (Absy et al. 2018). Studies have shown that these bees have food preferences (Rech
and Absy 2011a,b) and depend on these resources to maintain their colonies (Absy and Kerr
1977; Ferreira and Absy 2015, 2017a, 2017b).
In addition to the ecological importance of plant/insect interactions, beekeeping of
stingless bees (also known as meliponiculture) is a sustainable and profitable activity of great
economic value that can support many traditional communities (Nogueira-Neto 1997). Honey
from stingless bees is a carbohydrate-rich food with a different, but also highly liked, flavor
from the honey produced by Apis melifera bees (Souza et al. 2009; Souza et al. 2013).
Empirical knowledge about stingless beekeeping is transmitted across generations in
traditional indigenous communities. This knowledge shows the importance of stingless
beekeeping, making beekeepers and indigenous communities agents of transformation for
subsistence and environmental conservation (Rodrigues 2005; Sá and Prato 2007). Honey
production in the Amazon region has been gaining prominence, with native beekeeping being
managed by traditional and indigenous communities (Costa et al. 2012).
Agriculture is the main activity of Sateré Mawé indigenous communities, and 97% of
its production is for personal consumption, whereas the remaining is marketed (Teixeira 2005).
Stingless beekeeping has therefore been gaining relevance, generating economic benefits and
especially in food supplementation for these communities (Belém et al. 2011; Marinho et al.
2013).
The meliponiculture can present a sustainable strategy, since besides the production of
food can also be seen as an alternative to stop deforestation and ensure the maintenance of
floristic diversity (Smith et al. 1998). Knowledge about which plants are exploited by bees in
the Amazon is essential for management programs, expansion of beekeeping activities, honey
botanical characterization, and determination of honey origin. Using this knowledge,
beekeepers can promote the maintenance of groups of plants essential to honey production and
the conservation of bee colonies (Absy et al. 2013; Ferreira and Absy 2013, 2015, 2017a,
2017b).
Palynological studies are essential because they may help clarify interactions between
pollinators and native plant species (Novais et al. 2012; Vossler et al. 2014). In the Amazon,
the use of bee resources depends on food availability (pollen and nectar), reinforcing the
importance of plant conservation for bee maintenance (Absy et al. 1980; Absy et al. 1984;
15
Oliveira et al. 2009; Novais and Absy 2013, Absy et al. 2013; Ferreira and Absy 2013, 2015,
2017a, 2017b).
The aim of the present study was to identify the pollen types in honey samples from
colonies of Melipona and Scaptotrigona species, collected in three Sateré Mawé indigenous
communities. This is the first study to report important pollen types (bee pastures) for stingless
beekeeping in these indigenous communities.
Materials and Methods
Study site and honey sample collection
The study was performed in apiaries from three different Sateré Mawé communities,
located along the edges of the Marau River in the municipality of Maués, state of Amazonas,
Brazil (3°39'45.00"S, 57°20'17.99''W): Ilha Michiles (IM), Nova Esperança (NE), and Monte
Horeb (MH) (Figure 1). The vegetation in the study area is characterized as floodplain forest;
Amazonian floodplain forests are considered the most species-rich floodplain forests
worldwide (Wittmann et al. 2006).
Figure 1: General location of the study area, encompassing three indigenous communities (Ilha Michiles, Nova
Esperança, and Monte Horeb), located along the edges of the Marau River in the municipality of Maués, state of
Amazonas, Brazil (Source: Qgis).
16
Collections were performed as part of the project “Native Bees of the Sateré Mawé
Indigenous Area: Mapping of Pollination and Characterization of Stingless Bee Products”,
coordinated by Dr. Helyde Albuquerque Marinho. Honey samples were collected from different
colonies. Honey samples from Melipona seminigra merrillae (Ms) were collected in the Nova
Esperança (n=6) and Monte Horeb (n=8) communities, from Scaptotrigona sp. (S), that was
not identified at the species level, in the Nova Esperança (n=9) community, and from
Scaptotrigona nigrohirta (Sn) in the Ilha Michiles (n=4) community. Honey samples were
directly collected from the pots in the colony using a syringe, separated, placed in hermetically
sealed sterile containers, and sent to the Laboratory of Palynology at the National Institute for
Amazonian Research (INPA).
Honey chemical processing and pollen identification
Samples were prepared for pollen analysis using a method adapted from and
recommended by the International Commission for Bee Botany (Louveaux et al. 1978),
consisting of the following stages: dilution of 10 mL of honey in 20 mL of distilled water +
alcohol (1:1) and slight heating at 40 °C, followed by centrifugation (10 min, 3500 rpm) for
pollen separation. The samples were then subjected to acetolysis (Erdtman 1960), and pollen
grains were mounted in glycerinated gelatin in sets of three slides sealed with paraffin (Kisser
1935).
The pollen type was identified by comparison with the pollen collection of the
Laboratory of Palynology of INPA and by consultation of specialized literature (Roubik and
Moreno 1991; Carreira et al. 1996). A total of 58 species of local vegetation distributed in 29
families were collected and deposited in the INPA´s Herbarium to help identification.
Taxonomic characterization of the pollen grains was performed using the “pollen type” system
proposed by Joosten and de Klerk (2002) and de Klerk and Joosten (2007), which groups pollen
based on shared morphological features between one or more plant species. Pollen grain
measurements and photomicrographs were obtained using a Zeiss Primo Star microscope
coupled to a Canon Power Shot A650IS camera and an ocular micrometer.
Honey quantitative analysis, statistical indices, and trophic relations
For quantitative analysis, 600 pollen grains were counted for each sample (Vergeron
1964). Frequency classes were defined using the classification proposed by Louveaux et al.
17
(1978) and Novais et al. (2009) as predominant pollen (>45%), secondary pollen (≤45% to
>15%), important minor pollen (≤15% to ≥3%), and minor pollen (<3%).
Diversity index (H') by Shannon-Weaver (1949), was calculated using the following
equation: H'= ∑ (pi.lnpi), where H' is the diversity index, (pi) is the proportion of each pollen
type found in the sample, and (ln) is the natural logarithm. J' index of Pielou (1977) was used
to evaluate the homogeneity of the honey samples among the different communities, using the
following equation: J' = H'/H'max, where H' is the diversity index, and H'max is the natural
logarithm for the total number of pollen types present in the samples. Differences between
different samples and communities were tested using Student’s t-test in the R software.
Niche overlap index by Pianka (1973) was calculated for the two bee species (Melipona
seminigra and Scaptotrigona sp.) for the Nova Esperança community, using the following
equation: Oik = ∑ pij pik / √pij2 ∑ pik2, where pij is the proportion of pollen types in the sample
for one bee species, and pik is the corresponding value for the other bee species. Niche overlap
varies between 0 and 1 and is considered biologically significant when it is equal to or higher
than 0.6 (Zaret and Rand 1971; Wallace 1981).
Interactions between the studied stingless bees and collected resources were represented
as bipartite graphs, generated using the R software (package: bipartite). Cluster analysis of the
similarity of the resources collected by the bees from the different studied communities was
performed using Biostat 5.0 software.
Results
Indigenous community - Ilha Michiles
Scaptotrigona nigrohirta
For the Ilha Michiles community, 29 pollen types belonging to 13 plant families were
identified in honey samples collected from four pots. The most frequent pollen types, per pot,
were Eschweilera tenuifolia, Tapirira guianensis, and Bredemeyera floribunda. These pollen
types presented frequencies between 15 and 45%, and they were classified as secondary pollen.
Pollen types Alchornea triplinervia, Croton lanjouwensis, Amanoa guianensis, Casearia
javintensis, Spondias mombin, Miconia type, Alchornea type, and Mabea type presented
frequencies between 3 and 15% and were classified as important minor pollen. The remaining
pollen types were classified as minor pollen (Table 1).
18
Table 1: Frequency of pollen types present in honey from Scaptotrigona nigrohirta bees from the Ilha Michiles
community, located along the edges of the Marau River in the municipality of Maués, state of Amazonas, Brazil.
P (Pot).
Family/Pollen types P1 P2 P3 P4
ANACARDIACEAE
Spondias mombin 6.17 0.33 0.83 10.67
Tapirira guianensis 22.50 31.83 24.67 16.00
CHRYSOBALANACEAE
Couepia type 0.83 0.33 0.67 0.17
EUPHORBIACEAE
Alchornea triplinervia 14.00 11.00 6.83 4.83
Alchornea type 1.83 4.00 3.67 1.33
Amanoa guianensis 2.33 10.67 5.00 12.00
Croton lanjouwensis 1.50 12.67 8.67 12.83
Mabea type 3.50 1.33 0.83
Sebastiania brasiliensis 0.17
FABACEAE/CAESALPINIOIDEAE
Bauhinia purpúrea 1.00 0.17 0.17
Sclerolobium hypoleucum 0.67 0.17 0.33
FABACEAE/MIMOSOIDEAE
Mimosa guilandinae 0.83 1.00 0.33
Mimosa spruceana 0.17 0.17 0.33
LECYTHIDACEAE
Eschweilera tenuifolia 23.67 19.67 43.83 15.17
MELASTOMATACEAE
Miconia type 9.50 2.00 1.67 0.67
MYRTACEAE
Eugenia type 0.67 0.33 0.00 1.00
Syzygium type 0.17 0.17 0.17
POACEAEA
Type 1 0.17
Type 2 0.17
Type 3 1.33
POLYGALACEAE
Bredemeyera floribunda 0.33 1.67 2.00 22.00
RUBIACEAE
Borreria capitata 0.33 1.00
Borreria latifólia 0.33
SALICACEAE
Casearia grandiflora 0.17 0.17
Casearia javitensis 11.67 0.00
SAPINDACEAE
Talisia type 0.17
INDETERMINATE
Type 1 0.17
Type 2 0.17
Type 3 0.17
Total % 100 100 100 100
Number of pollen types 21 19 16 19
Diversity H' 2.271 2.049 1.755 2.209
Evenness J' 0.75 0.70 0.63 0.75
19
Indigenous community - Nova Esperança
Scaptotrigona sp.
For Scaptotrigona sp., 43 pollen types belonging to 22 plant families are identified in
two beehives (A and B). For beehive A, the most frequent pollen types, per pot, were Tapirira
guianensis, Alchornea triplinervia, and Amanoa guianensis, with frequencies between 15 and
45%, and they were classified as secondary pollen. Spondias mombin, Couepia type, Tapura
lanceolata, Alchornea type, Croton lanjouwensis, Sebastiania brasiliensis, Bauhinia purpurea,
Cynometra type, Sclerolobium hypoleucum, Inga type 1, Mimosa guilandinae, Mimosa
spruceana, Swatzia type, Eschweilera tenuifolia, Miconia type, and Eugenia type presented
frequencies between 3 and 15%, and these were classified as important minor pollen. For
beehive B, Sclerolobium hypoleucum, Tapirira guianensis, Eugenia type, and Alchornea type,
presented frequencies between 15 and 45%, and they were classified as secondary pollen.
Spondias mombin, Protium heptaphyllum, Doliocarpus type, Alchornea triplinervia, Amanoa
guianensis, Croton lanjouwensis, Mimosa spruceana, and Miconia type presented frequencies
between 3 and 15% and were classified as important minor pollen. The remaining pollen types
were classified as minor pollen (Table 2).
Table 2: Frequency of pollen types present in honey from Scaptotrigona sp. bees from the Nova Esperança
communitycy, located along the edges of the Marau River in the municipality of Maués, state of Amazonas, Brazil.
P (pot).
Beehives A Beehives B
Family/Pollen types P1 P2 P3 P4 P1 P2 P3 P4 P5
ANACARDIACEAE
Mangifera indica 0.17
Spondias mombin 3.33 2.50 3.00 4.67 0.33 5.50 3.33 6.17 1.50
Tapirira guianensis 12.33 30.33 43.00 12.17 1.17 15.33 8.17 16.83 16.83
ARECACEAE
Maximiliana maripa 0.17 0.17 0.17 0.33 0.17 0.67
ARALIACEAE
Schefflera morototoni 0.17
ASTERACEAE
Vernonia scabra 0.33
BIGNONIACEAE
Type 1 2.17 0.67
BURSERACEAE
Protium heptaphyllum 0.33 0.50 0.17 0.50 6.67 0.33 1.67
CHRYSOBALANACEAE
Couepia type 0.33 6.83 9.17 1.17 0.17 0.17 1.00 2.17 0.17
DICHAPETALACEAE
Tapura lanceolata 4.33 3.67 2.33 6.50 0.17 0.33 1.67 0.33 0.17
DILLENIACEAE
Doliocarpus type 10.17 3.17 5.67 7.67 4.00
20
Continuation
ERICACEAE
Type 1 0.50
EUPHORBIACEAE
Alchornea triplinervia 12.00 9.67 5.00 23.50 2.17 8.67 12.67 11.67 8.33
Alchornea type 12.67 15.50 8.17 8.33 6.50 13.33 14.83 22.83
Amanoa guianensis 19.00 8.00 0.33 7.67 12.00 4.00 6.50 4.17 11.67
Croton lanjouwensis 1.67 0.67 0.17 7.50 15.17 4.67 2.67 7.00 6.00
Sapium type 0.17
Sebastiania brasiliensis 1.67 2.67 4.83 1.83
Bauhinia purpurea 3.50 0.33
Cassia type 1 0.50 0.17
Cynometra type 0.17 3.67 0.17
Macrolobium type 0.17
Sclerolobium hypoleucum 4.00 3.33 1.17 10.50 40.67 11.50 17.00 13.33 13.50
Inga type 1 0.83 5.33 10.17 0.17 2.17 0.50 1.33 0.83
Mimosa guilandinae 6.50 1.50 0.17 0.17
Mimosa spruceana 0.50 3.83 6.17 1.17 4.33 4.33 2.50 2.67
FABACEAE/PAPILIONOIDEAE
Swartzia type 3.67 0.33 1.00
HYPERICACEAE
Vismia macrophylla 0.33
LECYTHIDACEAE
MELASTOMATACEAE
Miconia type 3.00 1.00 3.17 1.67 0.17 2.00 7.50 0.67 0.67
MYRTACEAE
Eugenia type 5.00 2.67 5.17 5.17 3.83 24.67 6.50 3.00 5.50
Syzygium type 0.50 0.50 0.33 0.67
POACEAE
Type 0.67
POLYGALACEAE
Bredemeyera floribunda 2.00
RUBIACEAE
Borreria capitate 0.17 2.67 1.00 1.00 2.50 1.33
Warscewiczia coccinea 1.50 0.50
SALICACEAE
Casearia grandiflora 0.33 0.33 0.50 0.83 2.00 0.33 0.83 1.17
Casearia javitensis 0.33 0.33
Homalium racemosum 0.67 2.50 0.50 0.17
INDETERMINATE
Type 1 0.17
Type 2 0.17
Type 3 0.17
Type 4 0.50
Total % 100 100 100 100 100 100 100 100 100
Number of pollen types 20 27 23 20 18 22 21 24 20
Diversity H' 2.680 2.583 2.219 2.556 1.958 2.547 2.679 2.717 2.444
Evenness J' 0.89 0.78 0.71 0.85 0.68 0.82 0.88 0.86 0.82
21
Melipona seminigra
For M. seminigra, 39 pollen types belonging to 18 plant families were identified in four
pots. The most frequent pollen types per pot were the Miconia type and Protium heptaphyllum,
with frequencies >45 %, and these were classified as predominant pollen. Tapirira guianensis,
Maximiliana maripa, Couepia type, Tapura lanceolata, Sebastiania brasiliensis and Eugenia
type presented frequencies between 3 and 15 % and were classified as important minor pollen.
The remaining pollen types were classified as minor pollen (Table 3).
Table 3: Frequency of pollen types present in honey from Melipona seminigra from the Nova Esperança
P (Pot).
Family/Pollen types P1 P2 P3 P4 P5 P6
ANACARDIACEAE
Anacardium type 0.17
Mangifera indica 0.83 1.33 0.17 0.50
Spondias mombin 0.17 0.17 0.17 0.33 1.67 2.00
Tapirira guianensis 5.33 5.00 3.50 5.33 5.33
ARECACEAE
ASTERACEAE
Mikania congesta 0.17
BURSERACEAE
Protium heptaphyllum 2.00 40.67 9.67 69.17 10.00 10.67
CHRYSOBALANACEAE
Couepia type 0.17 0.67 7.83 0.50 1.17
DICHAPETALACEAE
Tapura lanceolate 4.67 2.83 5.33 1.00 3.67 3.00
Type 1 0.17
EUPHORBIACEAE
Alchornea triplinervia 0.17 1.33 0.17 0.17
Croton lanjouwensis 0.17
Sapium type 0.50 0.17 0.33
Sebastiania brasiliensis 2.50 1.67 0.17 0.50 7.50 8.50
Cassia type 1 0.17 0.50 0.17
Inga type 0.17
Mimosa guilandinae 0.17 0.17
Mimosa pigra 0.17 0.17
Mimosa pudica 0.17 0.17 0.17
Mimosa spruceana 0.33 0.17
HYPERICACEAE
Vismia macrophylla 0.33 0.50
LECYTHIDACEAE
MALPIGHIACAEAE
Byrsonima type 0.50
MELASTOMATACEAE
22
Continuation
Bellucia imperialis 0.83
Clidemia type 0.17
Miconia type 77.00 42.33 63.33 22.00 58.83 60.67
Type 0.17 0.17 0.83
MYRTACEAE
Eugenia type 3.33 2.17 4.00 3.17 5.17 3.33
Syzygium type 0.17 0.17 0.17 0.33 0.50 0.50
PROTEACEAE
Euplassa inaequalis 0.83 0.17
Grevillea type 0.17
RUBIACEAE
Borreria capitate 0.17
Warscewiczia coccinea 0.33
RUTACEAE
Citrus type 0.17 0.17
SALICACEAE
Casearia grandiflora 0.17 0.17 0.17 0.17
SAPINDACEAE
Matayba type 0.17
Paulinia cupania 0.17
Serjania type 0.17
Total % 100 100 100 100 100 100
Number of pollen types 16 17 19 18 24 21
Diversity H' 1.002 1.424 1.457 1.001 1.679 1.549
Evenness J' 0.36 0.50 0.49 0.35 0.53 0.51
Indigenous community - Monte Horeb
Melipona seminigra
For the M. seminigra from the Monte Horeb community, 34 pollen types belonging to
19 plant families were identified in two beehives (A and B). For beehive A, the most frequent
pollen types, per pot, were Diplotropis purpurea and Miconia with frequencies >45 %, and
these were classified as predominant pollen. Doliocarpus type and Eugenia type presented
frequencies between 15 and 45 % and were classified as secondary pollen. Maximiliana maripa,
Couepia type, Alchornea triplinervia, and Sclerolobium hypoleucum presented frequencies
between 3 and 15 % and were classified as important minor pollen. For beehives B, only the
Miconia type presented a frequency >45 % and this type was classified as a predominant pollen.
Tapura lanceolata and the Eugenia type presented frequencies between 15 and 45 % and were
classified as secondary pollen. Spondias mombin, Maximiliana maripa, Protium heptaphyllum,
Alchornea triplinervia, Sclerolobium hypoleucum, Diplotropis purpurea, and Eschweilera
tenuifolia presented frequencies between 3 and 15 % and were classified as important minor
23
pollen. The remaining pollen types presented frequencies <3 % and were classified as minor
pollen (Table 4).
Table 4: Frequency of pollen types present in honey from Melipona seminigra bees from the Monte Horeb
P (Pot)
Beehives A Beehives B
Family/Pollen types P1 P2 P3 P4 P5 P1 P2 P3
ANACARDIACEAE
Mangifera indica 0.17 0.17 0.33 0.17
Spondias mombin 0.17 1.33 0.17 6.33 1.83 0.50
ARECACEAE
Maximiliana maripa 1.83 2.83 1.67 1.67 3.50 2.00 3.50 3.00
BURSERACEAE
Protium heptaphyllum 0.33 0.33 2.50 1.33 1.50 4.00 3.67 1.50
CALOPHYLLACEAE
Caraipa grandifolia 0.33 1.33
CHRYSOBALANACEAE
Couepia type 5.00 0.50 1.50 0.67 0.17
DICHAPETALACEAE
Tapura lanceolate 0.33 1.83 15.50 13.67
DILLENIACEAE
EUPHORBIACEAE
Alchornea triplinervia 0.67 1.17 7.33 3.17 3.17 0.33 3.83
Croton lanjouwensis 0.17
Sapium type 0.33 1.00 2.00 0.50
Sebastiania brasiliensis
Cassia type 1 0.17 0.17 0.33
Cassia latifolia 0.17 0.33 2.00
Sclerolobium hypoleucum 3.83 0.17 0.67 1.00 0.17 3.83
FABACEAE/PAPILIONOIDEAE
Diplotropis purpurea 18.67 61.17 0.83 8.00 21.83 3.00 1.33
Cynometra type 0.50
Mimosa guilandinae 0.50
Mimosa spruceana 0.33 0.17 0.17
HYPERYCACEAE
Vismia type 1.17
LECYTHIDACEAE
Eschweilera tenuifolia 1.83 0.83 1.67 1.50 1.17 2.17 4.67 4.33
MALPIGHIACAEAE
Byrsonima chrysophila 0.33 0.33 0.33
MELASTOMATACEAE
Miconia type 38.67 20.50 57.00 34.67 48.00 67.83 48.33 42.33
Type 0.33
MYRTACEAE
Eugenia type 4.67 5.67 1.67 29.50 3.33 3.17 12.67 22.67
Syzygium type 0.33
POACEAE
Type 1 2.83 0.50

24
Continuation
RUBIACEAE
Borreria capitate 2.00 0.50 0.33 0.83 1.33 0.50 1.33 0.50
Warscewiczia coccinea 0.17 0.17 1.17 0.50 0.17 0.17
SALICACEAE
SAPINDACEAE
Paullinia cupania 0.67 0.17 0.17
SOLANACEAE
Solanum type 0.17 0.50
INDETERMINATE
Type 1 0.17
Total % 100 100 100 100 100 100 100 100
Number of pollen types 21 15 18 16 17 18 19 17
Diversity H' 1.908 1.290 1.457 1.795 1.686 1.454 1.867 1.813
Evenness J' 0.63 0.48 0.50 0.65 0.58 0.51 0.63 0.64
Ecological indices and trophic interaction network
The diversity (H') per pot varied between 1.271 and 1.755 for S. nigrohirta from Ilha
Michiles (Table 1), between 1.958 and 2.717 for Scaptotrigona sp. from Nova Esperança (Table
2), and between 1.001 and 1.679 for M. seminigra (Table 3) and 1.290 and 1.908 for M.
seminigra (Table 4) from Monte Horeb. Significant differences were observed among the pots
within each community. For Nova Esperança, the niche overlap (Oi) between M. seminigra and
Scaptotrigona sp. was 0.148.
Trophic interaction networks were represented as bipartite graphs, showing the relations
of each bee species with the plants collected for each community, and those shared by all studied
communities. From the 65 pollen types identified in pots, five types were exclusive for
Scaptotrigona sp. (NE), five for M. seminigra (MH), six for Scaptotrigona nigrohirta (IM), and
13 for M. seminigra (NE) (Plate 1,2; Figure 2). Of the 22 main pollen types with the highest
proportions, Miconia was the only type shared among the bees from the four bee colonies
(Figure 3). The pollen types present in three bee colonies were Spondias mombin (NE-S, NH-
Ms, and IM-Ss), Tapirira guianensis (NE-S, NE-Ms, and IM-Sn), Protium heptaphyllum (NE-
S, NE-Ms, and MH-Ms), Tapura lanceolata (NE-S, NE-Ms, and MH-Ms), Alchornea
triplinervia (NE-S, MH-Ms, and IM-Sn), and Eugenia type (NE-S, NE-Ms, and MH-Ms). The
pollen types present in two bee colonies were Maximiliana maripa (NE-Ms and MH-Ms),
Couepia type (NE-S and Ne-Ms), Doliocarpus type (NE-S and MH-Ms), Alchornea type (NE-
S and IM-Sn), Amanoa guianensis (NE-S and IM-Sn), Croton lanjouwensis (NE-S and IM-Sn),
Sebastiania brasiliensis (NE-S and NE-Ms), and Eschweilera tenuifolia (MH-Ms and IM-Sn).
Sclerolobium hypoleucum, Inga type, and Mimosa spruceana were present in the highest
25
proportions in Nova Esperança (Scaptotrigona sp.); the Mabea type, Bredemeyera floribunda,
and Casearia javitensis were present in the highest proportions in Ilha Michiles (S. nigrohirta).
The Diplotropis purpurea type was present in highest proportion only in Monte Horeb (M.
seminigra) (Figure 3).
The cluster analysis generated two different groups based on the similarity of collected
pollen types. The first group was formed by S. nigrohirta (IM) and Scaptotrigona sp. (NE); the
second group was formed by M. seminigra (NE and MH) (Figure 4).
26
Plate 1: Photomicrographs of predominant pollen types found in honey samples of Melipona seminigra,
Scaptotrigona sp., and Scaptotrigona nigrohirta from three communities (Ilha Michiles, Nova Esperança, and
Monte Horeb). Alchornea type (1, 2); Alchornea triplinervia (3, 4); Amanoa guianensis (5, 6); Bredemeyera
floribunda (7, 8); Diplotropis purpurea (9, 10); Doliocarpus type (11, 12); Eschweilera tenuifolia (13, 14);
Eugenia type (15, 16). Scale bars: 10 µm.
27
Plate 2: Photomicrographs of predominant pollen types found in honey samples of Melipona seminigra,
Scaptotrigona sp., and Scaptotrigona nigrohirta from three communities (Ilha Michiles, Nova Esperança, and
Monte Horeb). Miconia type (1, 2); Protium heptaphyllum (3, 4); Sclerolobium hypoleucum (5, 6); Tapirira
guianensis (7, 8). Scale bars: 10 µm.
28
Figure 2: Bipartite graph showing the presence or absence of trophic interactions between four bee colonies from
three indigenous communities and the pollen types present in the honey samples. NE-S (Nova Esperança-
Scaptotrigona sp.), NE-Ms (Nova Esperança-Melipona seminigra), MH-Ms (Monte Horeb–Melipona seminigra),
IM-Sn (Ilha Michiles-Scaptotrigona nigrohirta).
29
Figure 3: Bipartite graph showing the proportion of trophic interactions between four bee colonies from three
indigenous communities, and the main pollen types present in honey samples. NE-S (Nova Esperança-
Scaptotrigona sp.), NE-Ms (Nova Esperança-Melipona seminigra), MH-Ms (Monte Horeb–Melipona seminigra),
IM-Sn (Ilha Michiles-Scaptotrigona nigrohirta).
30
Figure 4: Cluster analysis of bee species per community, according to pollen type similarity, based on Euclidian
distances. Legend: NE-S (Nova Esperança-Scaptotrigona sp.), NE-Ms (Nova Esperança-Melipona seminigra),
MH (Monte Horeb–Melipona seminigra), IM-Sn (Ilha Michiles-Scaptotrigona nigrohirta).
Discussion
Among the bees reared in stingless bee apiaries in the Amazon, several palynological
studies have been performed on the two studied genera Melipona and Scaptotrigona (Absy and
Kerr 1977; Absy et al. 1980; Absy et al. 1984; Marques-Souza et al. 2002; Marques-Souza et
al. 2007; Oliveira et al. 2009; Ferreira and Absy 2013, 2015, 2017a, 2017b).
The number of different pollen types collected was higher for Scaptotrigona sp. from
Nova Esperança than for the remaining bee species and communities and was lower for S.
nigrohirta from Ilha Michiles. The latter result was likely because four pots were analyzed for
this community, whereas six to nine pots were analyzed for the remaining communities. Bees
from genus Scaptotrigona present more individuals per colony (approximately 10,000) than
bees from the genus Melipona (approximately 1500), and have thinner bodies (Peralta 1999).
The number of bees from genus Scaptotrigona collecting nectar and pollen is therefore
considerably larger than the number of Melipona species, and this may be one of the reasons
for the different number of pollen types observed for the two studied species (Peralta et al.
1999). This finding is in accordance with that of Marques-Souza et al. (2007), who identified
31
97 pollen types in pollen collected from the pollen basket of Scaptotrigona fulvicutis Moure
bees in a 1-year period in the Central Brazilian Amazon. Also, Ferreira and Absy (2017b)
identified 28 pollen types for Melipona interrupta Latreille in terra firme forests in the Central
Brazilian Amazon in a 1-year period. However, higher numbers of different pollen types have
been observed for bees from the same genus in flooded areas (Ferreira and Absy 2015, 2017a).
For S. nigrohirta and Scaptotrigona sp. from Ilha Michiles and Nova Esperança, no
predominant pollen types were observed, and most pollen types presented low frequency. For
these species, in both communities (Ilha Michiles and Nova Esperança), Eschweilera tenuifolia,
Tapirira guianensis, Sclerolobium hypoleucum, Alchornea type, Eugenia type, Bredemeyera
floribunda, Alchornea triplinervia, and Amanoa guianensis were the most frequent pollen
types, with Tapirira guianensis being the most common. Melissopalynological studies in the
Amazon have found Tapirira guianensis to be the best represented pollen type in corbicular
pollen (Marques-Souza et al. 2007, Ferreira and Absy 2015, 2017b) and in honey samples
(Ferreira and Absy 2017a).
Absy (1980) studied two native bees from the Amazon for a year and observed the
presence of Tapirira guianensis in four samples for M. seminigra and in eight samples for
Melipona rufiventris. Similarly, Absy et al. (1984) found Tapirira guianensis for nine bee
species in the middle Amazon region. Ramalho (1990) identified a total of 92 pollen types in
pollen collected by three Scaptotrigona species, with only six types being intensely exploited
and classified as predominant and secondary pollens. Marques-Souza (2007) identified 97
pollen types, of which only six showed high abundance, with Tapirira guianensis being one of
the predominant types. Rech and Absy (2011a) evaluated the pollen concentration per pot for
Ptilotrigona lurida and Scaptotrigona sp. along the Negro River and also found Tapirira
guianensis to be highly represented.
Similar results were observed for honey samples from Scaptotrigona sp. from three
Sateré Mawé communities (Nova União, Vila Nova, and Simão), with Tapirira guianensis
being the most used pollen type for the three communities (Belém et al. 2011).
For the bee M. seminigra, from both Nova Esperança and Ilha Michiles, three pollen
types were found to be more frequent in the honey pots (Miconia type, Protium heptaphyllum,
and Diplotropis purpurea), with the Miconia type showing the highest proportions. Miconia-
type pollen was also reported to be dominant in M. seminigra honey samples collected in the
city of Manaus, located in the Amazon region (Ferreira and Absy 2017a). Other studies of
pollen collected by Melipona bees in the Amazon showed strong relations between these bees
and the family Melastomataceae, especially the Miconia type (Absy and Kerr 1977; Absy et al.
1980; Ferreira and Absy 2013, 2015, 2017 a, 2017b). The strong presence of Miconia type in
32
honey samples may be related mainly to contamination through the vibration collection
behaviors of the wing musculature.
Unlike other bees belonging to the tribe Meliponini, bees from the genus Melipona
Illiger, 1806, collect pollen by vibrating their wing muscles (Buzz-Pollination). This is an
effective mechanism developed during plant-pollinator evolution, through which abundant
pollen is collected (Buchmann 1983). Approximately 98% of the family Melastomataceae
provide pollen as the sole resource for pollinators. These plants have poricidal anthers, and their
pollen grains are more easily removed by wing-muscle vibration (Renner 1983).
Although pollen types with a frequency lower than 15% were classified as being of
minor importance, they can indicate that these resources contribute with nectar supply for honey
production to bees and help maintain bee colonies during periods with variations in resource
availability, due to low flowering or environmental factors (Ramalho et al. 1985; Marques-
Souza 1999; Ferreira and Absy 2015).
Variations in pollen types were observed among the different pots and were sometimes
significant. This collection and storing behavior indicates that bees try to collect the maximum
possible amount of an attractive resource, even if it is ephemeral. However, some similarities
between pots were observed, showing that a given resource, when long lasting, can be collected
for several months and stored in several pots. Reck and Absy (2011b) analyzed the pollen
content of 104 pots for Partamona, Scaura, and Trigona bees and also observed no pollen
collection pattern, a result suggested to be related to the nest location and the sharing of different
pollen type resources. Also, different pollen collection patterns were observed in the present
study on M. seminigra and Scaptotrigona sp. bees from Nova Esperança, as indicated by the
low trophic niche overlap. However, Ferreira and Absy (2015, 2017a) compared collection
patterns for Melipona bees in central Amazon and observed high trophic niche overlap between
Melipona bees reared in the same location. In the present study, although the different
communities were separated by distances of more than 2 km, they presented high similarity of
pollen types. Specifically, this similarity was observed for the Miconia type pollen, which
presented high proportions for M. seminigra bees from two communities but was also shared
with Scaptotrigona from two communities, although in lower proportions. The high proportions
of some pollen types observed for the four bee studied shows that although the bees used
different niches, some pollen types can be considered key for the maintenance of their colonies.
This preference for the same resources in different environments is in agreement with other
studies performed in the Amazon (Ferreira and Absy 2015, 2017b). This similarity was also
observed in the cluster analysis, which resulted in two groups, one composed by the two
33
Scaptotrigona species and one by M. seminigra, showing that although the two genera share
some resources, they have different food preferences.
The present study showed that some groups of plants (Alchornea type, Alchornea
triplinervia, Amanoa guianensis, Bredemeyera floribunda, Diplotropis purpurea, Doliocarpus
type, Eschweilera tenuifolia, Eugenia type, Miconia type, Protium heptaphyllum, Sclerolobium
hypoleucum, and Tapirira guianensis) are important for the maintenance of the studied bee
colonies and likely benefit from pollination services. Significant differences may or may not
exist in stored pollen resources between different pots, showing that bees work according to the
available resources and the duration and attractiveness of these resources.
The studied bees and collected resources indicate a similar vegetation in the different
communities, which provides environments with high resource similarity, allowing the rearing
of these stingless bees and the development of local stingless beekeeping.
Resource demand was higher for Scaptotrigona species than for Melipona species, due
to their colonies having a higher number of individuals, thus requiring these bees to expand
their trophic niches. Conversely, Melipona species restrict their niche, using only a few essential
(key) sources to maintain their colonies. Another detail was that groups of plants strongly
represented in the sample of Melipona in this study, present in their majority anthers poricidal
and, therefore, more related to bees that use the buzz polination.
The development of stingless beekeeping requires improved knowledge of the trophic
resources used by the reared bees. Thus, this study provides essential data on which plants are
important for the bee pasture and how the bees of different genera behave in relation to available
resources. Considering the interest and consequently the development of beekeeping in the
indigenous communities Sateré Mawé, the data of the present work provide relevant
information for future pasture management programs related to native bee rearing.
Acknowledgements
The authors wish to thank the Amazon Research Foundation (FAPEAM) for the Research
Productivity Scholarship (002/2016) granted to the first author and for the scholarship and
financial support (062.01180/2015) granted to the third author, the Bionorte/FAPEAM
Graduate Program for the scholarship granted to the first author, the Bionorte Program for the
support, and the Laboratory of Palynology (COBIO) of the National Institute for Amazonian
Research (INPA) for the facilities provided.
34
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39
CAPÍTULO II
REZENDE, A.C.C; ABSY, M.L.; FERREIRA, M.G;

MARINHO, H.M. Honey botanical origin of stingless bees
(apidae meliponini) in the nova américa community of the sateré
mawé indigenous tribe, Amazon, Brazil
In: GRANA (no prelo)/doi: 10.1080/00173134.2020.1724323
40
Honey Botanical Origin Of Stingless Bees (Apidae Meliponini) In The Nova América
Community of The Sateré Mawé Indigenous Tribe, Amazon, Brazil
Abstract: This study analyzed the pollen present in honey samples collected from colonies of
stingless bees (Meliponini) from the meliponary of the Nova América community of the Sateré
Mawé tribe, located on the Marau River, Maués municipality, Amazonas state, Brazil
(3°39'45.00" S, 57°20'17.99” W). Collections were made directly from honey storage pots. A
total of 47 pollen types were identified, belonging to 22 plant families. Bees with the largest
number of polen types were Melipona seminigra (31 collected pollen types), followed by
Melipona sp. (27 pollen types), Scaptotrigona sp. (25 pollen types), and Melipona dubia (19
pollen types). Plant families most commonly collected were: Anacardiaceae, Arecaceae,
Burseraceae, Chrysobalanaceae, Dichapetalaceae, Dilleniaceae, Euphorbiaceae, Fabaceae,
Lecythidaceae, Melastomataceae, Myrtaceae, Rhamnaceae and Salicaceae. Scaptotrigona sp.
had the highest pollen types diversity (H' = 2.32) and, consequently, greatest between-collection
uniformity. Trophic niche overlap was significant between the following pairs of bees: M.
seminigra and M. dubia (Oi= 0.93); M. seminigra and Scaptotrigona sp. (Oi= 0.79) and M.
dubia and Scaptotrigona sp. (Oi= 0.69). These data demonstrate the importance of these shared
groups of plants for the maintenance of these bees and, consequently, for the development of
meliponiculture in Brazilian Amazonia.
Keywords: Native bees, Pollen analysis, Meliponiculture, Brazilian Amazon

41
Introduction
Meliponini bees form a very diverse group of social bees and exhibit great niche
plasticity, and extensive behavioral diversity (Michener 2007; Rasmussem & Cameron 2007).
Additionally, unlike honeybees exploited in beekeeping, the stinging apparatus is atrophied in
these bees, so they cannot be used as a defensive mechanism (Lopes et al. 2005). Most feed on
nectar and pollen, thereby establishing a mutually beneficial relationship of supply and demand
for resources between themselves and the plants they visit (Absy et al. 2018; Rezende et al.
2018).
Bees play a prominent part in animal-plant interactions, not only because of their great
ecological relevance, via their role in angiosperm pollination, but also because of their key
economic role in the pollination of cultivated plants (Roubik 1989; Kevan & Imperatriz-
Fonseca 2002; Imperatriz-Fonseca et al. 2012). Ecologically speaking, bees are key to
sustaining biodiversity, efficiently ensuring the pollination of up to 90% of the angiosperms in
any one biome in which they are found (Kerr 1996).
Honey from stingless bees is a product that is appreciated not only for its exotic flavor,
and role as a nutritious food, but also for its medicinal qualities (Souza et al. 2004; Cunha et al.
2016, 2017). The composition and quality of stingless bee honey depends essentially on the
characteristics of the plants that have been visited during its making (Barth 2004; Luz et al.
2010). Consequently, understanding the collection behavior, as well as knowing the flora
visited by the bees (meliponiculture pasture) is essential for ensuring high productivity and for
quality certification of generated products (Luz et al. 2011; Luz & Barth 2012).
Thus, identification of resource supply plants is of great importance for meliponiculture
because this identifies sources of nectar and pollen, and so allows the maximum utilization of
available trophic resources and identification of physical-chemical and nutritional
characteristics. Since each plant has specific nectar and pollen characteristics, natural
vegetation is a highly heterogenous mix of nectar and pollen types (Almeida-Muradian et al.
2005; Melo et al. 2009; Carpes et al. 2009). A knowledge of the mellithophilous plants of a
region, together with laboratory-based analyses of pollen grains, allows calendars of
nectariferous and polleniferous flowers to be made for individual locations (Ramalho et al.
1989, 1990; Ramalho 2004; Luz et al. 2007). Such information is essential as it assists both
stingless beekeeping and beekeepers in choosing the best location for their beehives, as well as
for identifying the periods when nectar and pollen availability is low (off-season or "non-
flowering"), and allowing the botanical and phytogeographical origin of the products to be
verified, so that they may be certified (Modro 2006; Modro et al. 2007, 2011).
42
In recent years, the rearing of stingless bees in traditional communities of Central

Amazonia has received attention both as a subsistence activity and for its sustainability potential
(Brito et al. 2013; Absy et al. 2018). Thus, the keeping of stingless bees is an ecologically-
appropriate activity, which has low initial investment and good prospects of financial return,
and so is likely to be an excellent means for generating alternative income (Magalhães &
Venturieri 2010).
A number of factors contribute to the viability of meliponiculture in the Amazon region.
These include the model of agricultural occupation (small properties) and the immense potential
of manageable native bee species (Venturieri et al. 2012). Combined, this means there is a
strong future for domestication and rational use of native stingless bee species in the production
of honey, wax, geopropolis and also in the pollination of crops (Cortopassi-Laurino et al. 2006;
Slaa et al. 2006).
Consequently, the objective of this study was to identify the botanical origin and to
quantitatively analyze the pollen contained in samples of honey from four species of stingless
bees reared in meliponary in the Nova América community of the indigenous Sateré Mawé
tribe in Amazonian Brazil.
Material and Methods
Study location and sample collection
The study was carried out in the meliponary from an indigenous Sateré Mawé
community, located on the Marau River, Maués municipality, Amazonas state, Brazil
(3°39'45.00" S, 57°20'17.99” W: Figure 1).
43
Figure 1: Nova América indigenous community, located on the lands of the indigenous Sateré Mawé people, on
the banks of the Marau River, Maués municipality, Amazonas state, Brazil (Qgis).
The vegetation around the area has characteristics of várzea forest. Of all Amazonian
floodplain environments, this vegetation is considered to have the richest variety of plant
species (Wittmann et al. 2010). For the high várzea, the most well-represented families are
Euphorbiaceae, Moraceae, Arecaceae, Annonaceae, Meliaceae and Myristicaceae and, for the
low várzea, Fabaceae, Malvaceae, Salicaceae, Urticaceae and Brassicaceae (Wittmann et al.
2006; Wittmann et al. 2010).
The climate of Central Amazonia is predominantly tropical, humid with seasonal
rainfall between May or June and August or September and torrential rains between September
or October to April or May (Weischet 1996).
The collections made for the current study were part of the project "Native Bees of the
Sateré Mawé Indigenous Area: Mapping of Pollination and Characterization of Meliponic
Products" coordinated by Dr. Helyde Albuquerque Marinho. The honey samples were collected
directly from the storage pots in beehives of Melipona (Michmelia) seminigra Cockerell, 1919
(five pots from a beehive); Melipona (Michmelia) dubia Moure & Kerr, 1950 (four pots from
a beehive); Melipona sp. Illiger, 1806 (six pots from a beehive) and Scaptotrigona sp. Moure,
1942 (four pots from beehive A and three pots from beehive B). Subsequently, the honey
samples were individually separated by pots, and were then placed in sterile-resealed bottles
and sent to the Palynology Laboratory of the National Institute of Amazonian Research (INPA),
Manaus, AM.
44
Chemical processing of honey and pollen identification
Sample preparation followed a methodology adapted from that recommended by the

International Commission for Bee Botany (Louveaux et al. 1978) in which 10 ml of each honey
sample was diluted in 20 ml of distilled water + alcohol solution (1: 1), slightly warmed to 40°
C, then centrifuged (10 min at 3500 rpm) to separate the pollen. Samples were then submitted
to the acetolysis, following the method of Erdtman (1960), and pollen grains mounted in
glycerinated gelatin on sets of three slides sealed with paraffin (Kisser 1935). Pollen type
identifications were made using the Laboratory of Palynology of the National Institute of
Amazonian Research (INPA) pollen reference collection, and by consulting the specialist
literature (Roubik & Moreno 1991; Carreira et al. 1996; Punt et al. 2007). When taxonomically
characterizing pollen grains, the concept of "pollen type" adopted followed Joosten & De Klerk
(2002) and De Klerk & Joosten (2007). The measurements and photomicrographs were
obtained through a microscope (Zeiss - PrimoStar), and with the AxioCamICc1 image capture
program.
Quantitative analysis of honey, statistical indices and trophic relationships
For the quantitative analysis, 600 grains of pollen were counted, using the method
proposed by Vergeron (1964). Frequency class definitions followed the adaption by Novais et
al. (2012) of the method of Louveaux et al. (1978): predominant pollen (>45%); secondary
pollen (≤45%–>15%); important minor pollen (≤15% – ≥3%); and minor pollen (<3%).
To determine trophic niche width, we calculated the Shannon-Weaver diversity index
(Shannon 1949) using H’= ∑(pi.lnpi), where H’ is the level of diversity, (pi) the proportion of
each pollen type found in the samples and (ln) the natural logarithm. The Pielou Index (Pielou
1977) was used to assay bee collection uniformity. This was calculated by the formula J' = H' /
H'max, H' being the diversity index and H'max the natural logarithm of the total number of pollen
types present in the samples. These indices were calculated using the Past program
(Paleontological statistic) version 3.0.
In addition, resource use overlap between bees studied was calculated from the formula
proposed by Pianka (1973) in which Oik= ∑pijpik/ √pij2 ∑ pik2, where pij is the proportion of
pollen types in the sample for one species and pik is the value derived from the other bee species.
The overlap index varies from 0 to 1, and may be considered biologically significant for
values greater than or equal to 0.6 (Zaret & Rand 1971; Wallace 1981).
45
Using the R platform, it was possible to determine the similarity and frequency of pollen
types in honey samples for the four bees studied, using cluster analysis (average method)
associated with a pollen diagram (package: vegan and rioja). The set of interactions between
the stingless bees studied were represented by bipartite graphs generated from binary and
quantitative matrices, applying the bipartite package.
Results
Pollen resources
A total of 47 pollen types from 22 botanical families were identified in the samples.
Bees with the highest number of pollen types in the samples were Melipona seminigra with 31
types in 18 botanical families, followed by Melipona sp. with 27 pollen types in 15 families,
Scaptotrigona sp. with 25 pollen types in 18 families, and Melipona dubia with 19 pollen types
in 13 families. (Tables I, II, III and IV). The most commonly encountered families were
Anacardiaceae, Arecaceae, Burseraceae, Chrysobalanaceae, Dichapetalaceae, Dilleniaceae,
Euphorbiaceae, Fabaceae, Lecythidaceae, Melastomataceae, Myrtaceae, Rhamnaceae and
Salicaceae.
For M. seminigra, Miconia was the most frequent pollen type, being classified as a
dominant pollen; Doliocarpus type and Dicorynia paraensis were classified as secondary
pollen and Maximiliana maripa, Tapura lanceolata, Alchornea type, Dialium type, Diplotropis
type, Bellucia imperialis and Eugenia type, as pollen of minor importance. The 21 other pollen
types in the sample were classified as rare pollen (Table I; Figures 2 and 3).
Table I: Frequency of pollen types present in honey from Melipona seminigra bees from the Nova América
P (Pot).
Family/Pollen types P1 P2 P3 P4 P5
ARALIACEAE
Schefflera morototoni 0.17 0.50
ANACARDIACEAE
Tapirira guianensis 0.50 0.17 0.17
Type 1.33
ARECACEAE
Euterpe type 1.00 0.50
Maximiliana maripa 1.33 4.67 1.00 2.00 1.17
BURSERACEAE
Protium heptaphyllum 0.50 0.17 0.33
Type 0.17 2.00 1.17 0.50
DICHAPETALACEAE
Tapura lanceolata 3.17 2.17 0.83 4.33
46
Continuation
DILLENIACEAE
Doliocarpus type 13.33 14.17 19.17 7.83
EUPHORBIACEAE
Alchornea type 1.33 8.50 0.50 2.33 2.00
Mabea type 0.17
Cassia type 0.17 0.17 0.17
Croton type 0.17
Dialium type 0.50 6.83 0.17
Dicorynia paraenses 29.67 8.17 2.00
Mimosa pudica 0.17 0.17
FABACEAE/FABOIDEAE
Andira inermis 0.67 0.33
Diplotropis type 0.17 2.83 8.17 1.67
MALPIGHIACEAE
Byrsonima type 0.83
MELASTOMATACEAE
Bellucia imperialis 6.67 0.33 0.17
Miconia type 52.17 54.50 77.00 46.67 73.83
MYRTACEAE
Eugenia type 1.83 5.00 1.50 7.33 1.83
Syzygium type 0.17 0.17
POACEAE
Type 0.33
POLYGALACEAE
POLYGONACEAE
Triplaris type 0.17 0.17
SALICACEAE
Casearia grandiflora 1.50 0.50 0.17 0.50 0.17
SOLANACEAEA
Solanum type 0.83 0.67 0.50
SAPINDACEAE
Paullinia cupana 0.17
URTICACEAE
Cecropia type 0.17 0.17 0.17
Total % 100 100 100 100 100
Number of pollen types 16 13 15 23 20
47
Figure 2: Photomicrographs of predominant pollen types found in honey samples of Melipona seminigra, Melipona
dubia, Melipona sp. and Scaptotrigona sp. from Nova América community. Alchornea type (A,B); Alchornea
triplinervia (C,D); Croton type (E,F); Dicorynia paraenses (G,H); Doliocarpus type (I,J); Eugenia type (K,L). Scale
bars: 10 µm.
48
Figure 3: Photomicrographs of predominant pollen types found in honey samples of Melipona seminigra,
Melipona dubia, Melipona sp. and Scaptotrigona sp. from Nova América community. Gouania blanchetiana
(A,B); Miconia type (C,D); Protium heptaphyllum (E,F); Stryphnodendron guianense (G,H); Tapirira guianensis
(I,J); Tapura lanceolata (K,L). Scale bars: 10 µm.
For M. dubia, the pollen types from Protium heptaphyllum, Doliocarpus type, Miconia
type, Eugenia type and Gouania blanchetiana were classified as secondary pollen; while
Maximiliana maripa, Tapura lanceolata, Stryphnodendron guianense Casearia grandiflora
were in the pollen class of minor importance. Nine other pollen types were classified as rare
pollen (Table II; Figures 2 and 3).
49
Table II: Frequency of pollen types present in honey from Melipona dubia bees from the Nova América
P (Pot).
Family/Pollen types P1 P2 P3 P4
ANACARDIACEAE
Spondias mombin 0.50 0.33 0.50
Tapirira guianensis 1.50 2.83 0.50 2.67
ARECACEAE
Maximiliana maripa 0.17 5.33 6.33 1.83
BURSERACEAE
Protium heptaphyllum 43.00 4.83 16.50 26.17
DICHAPETALACEAE
Tapura lanceolata 4.67 0.83 2.83 0.67
DILLENIACEAE
Dillenia type 0.67 1.67 0.83
Doliocarpus type 5.00 18.67 13.67 17.50
EUPHORBIACEAE
Alchornea type 2.67 3.00 0.83 2.83
Amanoa guinensis 2.00 0.33
Sapium type 0.17 0.33 0.33
Stryphnodendron guianensis 0.17 1.00 6.33 4.83
Mimosa type 0.17
MALPIGHIACEAE
Byrsonima type 0.33 0.17
MELASTOMATACEAE
Bellucia imperialis 0.17 0.17
Miconia type 8.50 26.17 40.33 34.33
MYRTACEAE
Eugenia type 1.33 25.83 4.17 1.50
POLYGONACEAE
Triplaris type 0.17 0.17
RHAMNACEAE
Gouania blanchetiana 31.17 2.67 4.50 2.17
SALICACEAE
Total % 100 100 100 100
Number of pollen types 15 15 14 18
For Melipona sp., Tapirira guianensis, Alchornea type and Eugenia type pollen were
classified as dominant, while Croton type and Stryphnodendron guianense were classified as
secondary pollen. Doliocarpus type, Diplotropis purpurea and Gouania blanchetiana were in
the pollen class of minor importance. Another 18 pollen types were classified as rare (Table III;
Figures 2 and 3).
50
Table III: Frequency of pollen types present in honey from Melipona sp. bees from the Nova América community,
located along the edges of the Marau River in the municipality of Maués, state of Amazonas, Brazil. P (Pot).
Family/Pollen types P1 P2 P3 P4 P5 P6
ANACARDIACEAE
Spondias mombin 0.17 0.33 0.83 0.17 0.83
Tapirira guianensis 68.67 24.00 17.67 2.50 31.67 1.17
ARECACEAE
Euterpe type 0.17
Maximiliana maripa 0.17 1.17 0.67 0.17
Type 1.67 1.17 0.83 0.50
BURSERACEAE
Protium heptaphyllum 0.17 0.17
CHRYSOBALANACEAE
Couepia type 1.17 1.33 1.50
DICHAPETALACEAE
Tapura lanceolata 1.33 2.33 0.83 0.17 2.17
DILLENIACEAE
Doliocarpus type 8.33 7.67 4.17 0.50 2.00 0.33
EUPHORBIACEAE
Alchornea type 1.50 30.00 33.33 49.50 12.83 20.00
Amanoa guinensis 0.67 0.33 1.17 0.33 0.33

Croton type 1.17 0.67 3.17 15.83 4.67
Cassia type 0.33
Sclerolobium hypoleucum 3.50 2.00 0.33 0.67 3.00 0.67
FABACEAE/FABOIDEAE
Andira inermis 0.17
Aeschynomene type 0.33
Diplotropis purpúrea 4.67 2.17
Inga type 0.33 0.83 0.17 0.17
Stryphnodendron guianense 6.83 16.67 28.00 37.17 19.67 8.17
LECYTHIDACEAE
Eschweilera tenuifolia 0.67 0.83 0.17 1.83 0.17
MELASTOMATACEAE
Miconia type 2.83 2.17 0.33 0.67 0.17
MYRTACEAE
Eugenia type 1.33 4.00 4.00 1.83 2.50 63.17
POLYGONACEAE
Triplaris type 0.17 0.17 0.50 0.17 0.17
RHAMNACEAE
Gouania blanchetiana 3.00 3.50 0.17 3.33
SALICACEAE
Casearia grandiflora 0.17 0.33 0.50 0.33 0.17 0.17
Casearia javitensis 0.33
SAPINDACEAE
51
Continuation
Total % 100 100 100 100 100 100
Number of pollen types 14 19 20 18 20 15
Scaptotrigona sp. bees collected large amounts of Miconia type and Stryphnodendron
guianense pollen, which were classified as dominant; Tapirira guianensis, Tapura lanceolata,
Doliocarpus type, Alchornea type and Alchornea triplinervia, were classified as secondary
pollen, while the pollen types Couepia type, Dillenia type, Amanoa guinensis, Croton type,
Derris type and Eugenia type were classified as pollen of minor importance. Twelve other
pollen types were classified as rare (Table IV; Figures 2 and 3).
Table IV: Frequency of pollen types present in honey from Scaptotrigona sp. bees from the Nova América
P (Pot).
Beehive A Beehive B
Family/Pollen types P1 P2 P3 P4 P1 P2 P3
ANACARDIACEAE
Tapirira guianensis 17.67 11.50 22.17 1.17 0.50 2.00
ARECACEAE
BURSERACEAE
Protium heptaphyllum 1.33 4.67 2.17
CHRYSOBALANACEAE
Couepia type 4.50 1.83 4.00 1.67 0.67 0.33 0.50
DICHAPETALACEAE
Tapura lanceolata 12.67 2.00 17.17 3.17 1.00 0.50
DILLENIACEAE
Dillenia type 6.00 1.50 6.17 0.50 4.17 2.17
EUPHORBIACEAE
Alchornea type 9.50 9.17 1.00 16.33 0.17 1.50 0.67
Alchornea triplinervia 15.83 1.00 5.50
Amanoa guinensis 0.83 1.00 0.33 14.50
Croton type 13.83 4.33 0.17 1.33 1.33
Sapium type 0.17 0.17 0.33
Cassia type 0.17 0.33
Sclerolobium hypoleucum 0.50 1.00 2.67 0.17 0.83
FABACEAE/FABOIDEAE
Derris type 0.83 5.33 5.67 1.33 0.33 0.17
Stryphnodendron guianense 25.33 41.67 20.83 45.83 0.17 0.33
HYPERICACEAE
Vismia guianensis 0.33 0.17 0.67
52
Continuation
LECYTHIDACEAE
Eschweileta tenuifolia 9.50
MELASTOMATACEAE
Miconia type 0.50 0.67 4.50 3.83 71.00 64.67 57.50
MYRTACEAE
Eugenia type 6.67 3.67 2.50 2.33 2.17 1.83 2.17
RHAMNACEAE
Gouania blanchetiana 0.17
POACEAE
Type 0.17
SALICACEAE
Casearia grandiflora 0.33 0.17 0.17 0.17 0.50 0.83
Casearia javitensis 0.50 0.17 0.33 0.33
SAPINDACEAE
Total % 100 100 100 100 100 100 100
Number of pollen types 15 16 16 15 17 16 16
Statistical analysis and interaction network
Based on diversity (H') and equitability (J') indices of the studied bees, Scaptotrigona
sp. had the highest diversity and consequently the greatest between-sample uniformity (H' =
2.32 and J' = 0.72); followed by M. dubia (H' = 2.09 and J' = 0.71); Melipona sp. (H' = 2.05 and
J' = 0.62) and M. seminigra H' = 1.59 and J' = 0.46) (Figure 4A). The overlap index was
significant for bees M. seminigra and M. dubia (Oi = 0.93), M. seminigra and Scaptotrigona sp.
(Oi = 0.79) and M. dubia and Scaptotrigona sp. (Oi = 0.69) (Figure 4B).
Figure 4: A) Values of diversity (H’) and evenness (J’) of the four species of bees; B) Overlapping values for the four
bee species. Captions: Scaptotrigona sp. (S), Melipona dubia (Md), Melipona sp. (M) and Melipona seminigra (Ms).
53
Collection similarity between studied bees was tested through cluster analysis, using the
main families collected. Three groups resulted. One, formed by M. seminigra, separated out
due to the dominance of Melastomataceae pollen in the sample. Another group was formed by
Melipona dubia, due to the prominence of Melastomataceae and Ramnaceae pollen. The
grouping of Melipona sp. and Scaptotrigona was mainly due to the families Anacardiaceae,
Euphorbiaceae and Fabaceae/Mimosoideae (Figure 5).
Figure 5: Pollen diagram showing the frequencies of pollen types for each bee. Ms: Melipona seminigra; Md: Melipona
dubia; M: Melipona sp.; S: Scaptotrigona sp.
The interaction network, as represented by the bipartite graph, showed the relation of
the four bees to the collected plants. Of the 47 pollen types, seven were exclusive to M.
seminigra, four exclusive to Melipona sp., and two collected only by Scaptotrigona sp.
Melipona dubia did not have any exclusive pollen types. Of those types shared by the four bees,
Melipona seminigra had 17, Melipona dubia 17, Scaptotrigona 21 and Melipona sp. 23 types.
Among the four species of bees studied, 9 pollen types were used by all species (from Tapirira
54
guianensis, Maximiliana maripa, Protium heptaphyllum, Tapura lanceolata, Doliocarpus,

Alchornea, Miconia, Eugenia and Casearia grandiflora) (Figure 6).
Figure 6: Bipartite graph showing the presence or absence of trophic interactions between four stingless bee species
at the Nova América indigenous community and the pollen types present in the honey samples.
Discussion
The pollen types identified in this study agree with the study of Rezende et al. (2018) in
which other communities of the same indigenous people (Sateré Mawé) were studied. Thus,
indicating a common preference by these bees for pollen types that provide nectar for honey
production, as well as pollen types from polliniferous plants. These often well-represented and
provide a source of natural contamination in honey samples. As noted by Ferreira & Absy
(2017a), bees of the genus Melipona tend to use a large number of polliniferous plants with
poricidal anthers, such as those found in the families: Melastomataceae, Solanaceae and many
species of Fabaceae. In many cases these were well-represented in samples of honey in the
current study. This fact may be related to the evolutionary mechanism of buzz pollination, in
which bees of this genus generally vibrate their wing musculature to liberate pollen from
poricidal anthers (Buchmann 1983; Renner 1983).
The data show that Melipona bees tend to diversify their niche within related botanical
groups, whereas bees of the genus Scaptotrigona diversify their niche across different botanical
families. Nevertheless, Scaptotrigona bees, although being smaller in body size, tend to be
55
generalists as a result of the greater number of individuals in the colony and, consequently, the
greater demand for both pollen and nectar (Rezende et al. 2018).
Considered highly polliniferous, the Melastomataceae is undoubtedly the plant family
that most contributes to the maintenance of bees of the genus Melipona: its importance has been
highlighted in several studies in the Amazon, of pollen collected and transported to the colonies,
and of samples of honey (Absy & Kerr 1977; Absy et al. 1980,1984; Ferreira and Absy 2013,
2015, 2017a, 2017 b; Rezende et al. 2018). In support, studies by Ferreira & Absy (2017b) and
Rezende et al. (2018) found high frequencies of Miconia pollen in M. seminigra honey samples.
As the study site is based in várzea, it becomes pertinent to understand the importance
of this vegetation type for the practice of meliponiculture in indigenous communities. The key
role of várzea is indicated by presence of pollen types known to be good suppliers of nectar,
such as representatives of the families: Myrtaceae, Burseraceae, Anacardiaceae among others
that, even at low frequencies, are considered mellitophilous plants. In addition, Ferreira (2014),
studying annual variability of corbicular pollen and honey samples from the genus Melipona,
noted that even though members of the the families Sapindaceae, and Polygonaceae were rare,
they were always present in honey sample. This was also true for some Fabaceae, and
highlighted the importance of these families, especially for honey production. The same author
highlights the importance of Triplaris (Polygonaceae) pollen, a genus considered endemic to
várzea environments (Wittmann et al. 2010). In addition, Triplaris type pollen has already been
identified in samples of post-emergence residue of Melipona interrupta (Ferreira & Absy
2013). In this same context, Ferreira & Absy (2017b), studying the trophic niche of Melipona
interrupta, note that honey samples contained pollen samples from the terra firme environment
that were considerably lower in diversity and with a smaller equitability index than those from
the várzea environment, despite the former having a higher tree species diversity. This shows
the close relationship that the bees of the genus maintain with Amazonian seasonally-flooded
habitats. Indeed, as far back as 1950, Moure & Kerr had suggested that stingless bees had a
very close relationship with Amazonian várzea areas. Indeed, most species of the genus
Melipona occur in this habitat, resulting in the high bee species diversity of these areas.
Since Scaptotrigona bees do not conduct buzz pollination, they tend, evolutionarily, to
be linked to a wide range of plants that provide pollen resources via both poricidal and non-
poricidal anthers. For this group of bees, the question of food is of key importance, both for the
maintenance of the offspring and for the formation of queens (Camargo 1972; Nogueira-Neto
1997). Probably as a direct result of high colony resource demand, Scaptotrigona had the
highest diversity and equitability index in this study. This concurs with Rezende et al. (2018),
where the genus Scaptotrigona also showed the higher rates of diversity and equitability than
56
bees of the genus Melipona. The great diversity of pollen types collected by Scaptotrigona bees
has also been shown by Ramalho et al. (1990) and Marques-Souza et al. (2007).
Based on this, an appropriate hypothesis for low richness of pollen types collected by
Melipona bees, when compared to those of the genus Scaptotrigona, may relate to the number
of individuals present in the colony. This is lower in Melipona colonies thus producing a lower
demand for pollen resources, in contrast, a greater pollen demand by Scaptotrigona bees, where
colonies are larger. Likewise, Kajobe (2006) suggests that the number of foraging workers may
be related to the size of the colony, which implies a greater demand and higher pollen variability
in their diet. In this context, Ramalho et al. (2007) have emphasized that the generalist foraging
is likely to be standard among eusocial bees with large perennial colonies and high rates of
offspring production, since these require large volumes of food to sustain them throughout the
year.
Despite the differences in collection mechanisms and numbers of individuals in the
colonies for the bee species studied, the resources identified in Melipona sp. and Scaptotrigona
sp honey samples being sufficiently similarity that the species grouped together. This contrasts
with the results of Rezende et al. (2018). This may be related to the vegetation characteristics
of the flooded areas (várzea) that has a lower species diversity than adjacent terra firme. (ter
Steege et al. 2000; Wittmann et al. 2010), forcing bees of different species and with different
collection mechanisms to exploit the same resources.
Moreover, for bees from the same community, the data revealed extensive similarities
in floral resource preferences, resulting in a significant overlap index between some species.
Thus, colonies of species with broader niche dimensions are more likely to meet their energetic
demands, but those resources collected by several species of bees may become limited, and this
may be detrimental to those bee species that tend to collect fewer resources (Biesmeijer et al.
1999; Ferreira & Absy 2013), thus increasing competition between different species of bees
that collect the same resource (Ferreira & Absy 2015). Accordingly, in honey samples, one
should not ignore pollinic types with low frequencies. They have often been considered as
contaminants, but such plants may be good suppliers of nectar for honey production, and
ecologically represent the unique resource axis of the bee species involved.
In the current study, M. dubia did not have a dominant pollen type. However, some
types classified as secondary pollen (e.g. Protium heptaphyllum, Doliocarpus, Miconia,
Eugenia and Gouania blanchetiana) are types found at high frequencies by other authors
studying Melipona bees (Ferreira and Absy 2015; 2017 a,b). Even the pollinic types of minor
importance (i.e. percentages lower than 10%), form important complementing resources during
57
periods of low resource availability, so keeping the colony operative during such lean periods
(Ramalho et al. 1985).
We verified that the bees Melipona seminigra, Melipona sp. and Scaptotrigona sp. are
generalists, with niches that are broad in relation to available resources. In contrast, Melipona
dubia, although also considered a generalist, had its niche restricted to a specific group of plants.
Plant groups, such as Miconia sp., which provide little or no nectar for honey production, were
strongly represented in the samples. However, their importance to the composition of the honey
is based on their function to increment the protein levels of the final product (Ferreira & Absy
2017a). This may be widespread in this family since, as Renner (1989) points out, in
approximately 98% of Melastomataceae species, pollen is the only resource offered.
Of the families that most attractive and important plants for bees reared in local
meliponiculture, those such as the Anacardiaceae, Arecaceae, Burseraceae, Chrysobalanaceae,
Dichapetalaceae, Dilleniaceae, Euphorbiaceae, Fabaceae, Lecythidaceae, Melastomataceae,
Myrtaceae, Rhamnaceae and Salicaceae that, besides participating in the common preference
of the studied bees, are also strongly linked to the várzea areas in the Central Amazon.
Conclusion
Studies of the pollen types collected by native Amazonian bees are fundamental for the
development of local meliponiculture. These plants determine the production of honey and
consequently the support of the colony, moreover, promote the conservation of the flora and
native bees as well as providing a sustainable way of subsistence for the traditional communities
of the Amazon.
Acknowledgements
The authors wish to thank the Amazon Research Foundation (FAPEAM) for the
scholarship (002/2016) granted to the first author and for the scholarship and financial support
(062.01180/2015) granted to the third author, and the Conselho Nacional de Desenvolvimento
Científico e Tecnológico (CNPq) for the scholarship granted to the second author
(Proc.308425/2016-2), the BIONORTE Program for the support, and the Laboratory of
Palynology of the National Institute for Amazonian Research (INPA) for the facilities provided.
Adrian Barnett helped with the English.
58
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CAPÍTULO III
REZENDE, A.C.C; ABSY, M.L.; FERREIRA, M.G. Pollen

niche of Melipona dubia Moure & Kerr, 1950, Melipona
seminigra Cockerell, 1919 and Scaptotrigona sp. Moure, 1942
(Apidae:Meliponini) kept in indigenous communities of the
Sateré Mawé tribe, Amazonas, Brazil
In: Journal of Apicultural Research (Submetido)
66
Pollen niche of Melipona dubia Moure & Kerr, 1950, Melipona seminigra Cockerell, 1919
and Scaptotrigona sp. Moure, 1942 (Apidae:Meliponini) kept in indigenous communities
of the Sateré Mawé tribe, Amazonas, Brazil
Abstract: Pollen samples collected by Melipona dubia, Melipona seminigra and Scaptotrigona
sp. bees from communities of the Sateré Mawé tribe were analyzed and 61 pollen types were
identified. The most representative botanical families in the samples were: Anacardiaceae,
Arecaceae, Burseraceae, Euphorbiaceae, Dilleniaceae, Fabaceae, Melastomataceae and
Myrtaceae. Among these families, pollen of Miconia type (Melastomataceae) collected by
Melipona dubia and Melipona seminigra and Croton cajucara (Euphorbiaceae) and Eugenia
type (Myrtaceae) collected by Scaptotrigona sp. presented temporary specialization (>90%) in
some samples. On the other hand, Scaptotrigona sp. showed higher richness in their collections
(H' =1.66 and J’= 0.45), followed by Melipona seminigra (H' = 1.43 and J’= 0.39) and Melipona
dubia with (H' = 0.45 and J’= 0.14). The connectance of interactions between bees and plants
in the study locations was 19.37 %, which is considered high for palynological data. The other
network metrics, both for presence and absence (NODF= 54.07) and for quantitative matrix
(WNODF= 34.03) were found to be significant (p<0.001) and highly nested. Cluster analysis
from the collected resources presented two distinct groups, a group formed by the genus
Melipona and another by Scaptotrigona. The results show that even though they have their
peculiarities in the collections, these groups of bees share many resources, presenting
themselves as both generalists and temporary specialists, according to the colony’s needs.
Keywords: palynology, interaction network, stingless bees, biodiversity, Amazon.

67
Introduction
Bees play a fundamental role in pollination and are considered the most important group
due to their high visitation rates to flowers (Kerr et al., 1996; Thorp 2000). Many eucotyledons
have been strongly dependent on bee pollination since the Cretaceous, confirming the origin of
the bee and the increased abundance and geographic expansion of these plants approximately
123 Ma (millions of years) (Cardinal & Danforth, 2013).
About 80% of all cultivated plants in the world are pollinated by wild bees, while
stingless bees pollinate about 50% of cultivated plants in tropical America, with Brazil holding
the highest richness of these bees (Kerr et al., 1999). Therefore, bees have a fundamental
ecological role, since feeding on nectar and pollen intensifies a mutualistic and beneficial
relationship of supply and demand for resources, thus acting in maintaining diversity (Kerr et
al., 1996; Absy et al., 2018).
The Meliponini tribe comprises about 60 genera with approximately 600 species, which
are distributed throughout the planet's wide tropical and subtropical range, with emphasis on
the Amazonian forest (Roubik, 1992; Camargo, 1994; Michener, 2007; Rasmussen & Cameron,
2010). These bees are popularly known as stingless bees because they have an atrophied stinger
and, unlike the melliferous bees exploited in beekeeping, they are a diverse group of social bees
with high diversity of niches and behaviors (Michener, 2007; Rasmussem & Cameron, 2007).
In the Amazon, traditional communities domesticate some of these bee species, mainly
those from the genus Melipona, making meliponiculture (beekeeping with stingless bees) a
profitable subsistence activity (Magalhães & Venturieri, 2010; Villas-Bôas, 2012; Brito et al.,
2013). Following the principles of agro-ecology, it is possible to develop meliponiculture that
incorporates the economic, social, ecological, political, cultural and ethical dimensions of
sustainability (Teixeira, 2005; Absy et al., 2018).
Understanding the trophic niche and relationships of these bees with plants is
fundamental, since each species dynamically contributes to maintain the ecosystem (Ebeling et
al., 2008). In this context, palynological analyses have practically and indirectly contributed to
knowledge about the flora used by bees (Absy et al., 2018). Samples obtained from pollen and
honey pots generate information that was previously only obtained through direct observations
in the field and provide significantly more information about pollinator/plant interactions
(Vianna et al., 2014; Ferreira & Absy, 2015).
Thus, information about plant species through pollen and nectar sources has helped
characterize and determine the origin of the resource used, providing a better understanding
68
about these pollination mechanisms, as well as the attractive flora for bees (meliponiculture
pasture) (Luz et al., 2010; Luz et al., 2011; Serra et al., 2012; Luz & Barth, 2012).
In order to determine the pollen niche and trophic relationships between three stingless
bee species kept in meliponaries of the Vila Nova II, Nova América and Nova Esperança
communities belonging to the Sateré Mawé indigenous tribe, the aim of this study was to
identify and quantify the botanical origins of pollen samples, to understand how these bees
behave in the same floristic scenario using interaction networks.
Material and methods
Study site
This study was conducted in three communities belonging to the Sateré Mawé tribe:
Nova América (NA), Nova Esperança (NE) and Vila Nova II (VN), located on the banks of the
Marau River in the municipality of Maués, Amazonas, Brazil at the coordinates 3°39'45.00" S
and 57°20'17.99” W (Figure 1).
Figure 1: Collection site with the three communities: Nova América, Nova Esperança and Vila Nova II, located
on the banks of the Marau River in the municipality of Maués, Amazonas State, Brazil (Source: Qgis).
69
This collection area has vegetation that is characteristic of floodplain forest, a type of
flooded forest presenting seasonal rains from May/June to August/September and torrential
rains from September/October to April/May, predominantly tropical humid (Weischet, 1996;
Wittmann et al., 2010).
The floodplain forest can be classified into two types: low floodplain situated at a higher
water level and high floodland situated at a lower water level. For the low floodplain, the most
representative plant families are: Fabaceae, Malvaceae, Salicaceae, Urticaceae and
Brassicaceae, and for the high floodplain the most representative families are: Euphorbiaceae,
Moraceae, Arecaceae, Annonaceae, Meliaceae and Myristicaceae (Wittmann et al., 2006;
Wittmann et al., 2010).
Collections, chemical processing and pollen identifications
Collections for this work were part of the project "Native Bees of the Sateré Mawé
Indigenous Area: Mapping of Pollination and Characterization of Meliponiculture products"
coordinated by Dra. Helyde Albuquerque Marinho.
A total of 51 pollen samples were collected, with eight samples collected for Melipona
dubia Moure & Kerr, 1950 (Community:Vila Nova II), 21 samples for Melipona seminigra
Cockerell, 1919 (Community: Nova Esperança) and 22 samples for Scaptotrigona sp. Moure,
1942 (Community: Nova América). Each sample was collected from a pollen pot inside the
hive using disposable plastic straws where several insertions were made. Soon after, the
samples were separated and individually placed in Falcon 15 mL tubes, which were
hermetically sealed and sent to the Palynology Laboratory at the Amazonas National Research
Institute (INPA). At the same time, the plant species surrounding the meliponaries were
surveyed to facilitate pollen identification, and the material was deposited in the herbarium at
the Amazonas National Research Institute (INPA).
To prepare the pollen samples, 5 ml of acetic acid was added to each tube (for at least
24 hours), and then subjected to the acetolysis method (Erdtman, 1960). Finally, a set of three
slides were assembled for each sample in glycerin gelatin and sealed with paraffin (Kisser,
1935).
Pollen was identified by comparing the slides with the Pollen Library of the Palynology
Laboratory at the Amazonas National Research Institute (INPA), as well as with specialized
bibliography (Roubik & Moreno, 1991; Carreira et al., 1996; Punt et al., 2007). The pollen
grains were classified according to the "pollen type" concept proposed by Joosten & De Klerk
(2002) and De Klerk & Joosten (2007). Measurements and photomicrographs of pollen types
70
were obtained using a microscope (Zeiss - PrimoStar) and the AxioCam ICc 1image capture
program.
Ecological indices and network of interactions
For each sample, 600 pollen grains were counted according to the counting classes
proposed by Vergeron (1964). Pollen frequencies followed two percentage categories, where
10% represented the minimum amount for the plant to be considered attractive to the bee and
90% was the minimum percentage for "temporary specialization" events (Ramalho et al., 1985).
The amplitude of the trophic niche was calculated using the Shannon-Weaver index
(1949) with the formula H’= ∑(pi.lnpi), where H' is the diversity index, (pi) the proportion of
each pollen type found in the samples and (ln) a natural logarithm. To verify the uniformity in
plant collections by bees, equitability was calculated using the formula J' = H' / H'max, with H'
being the diversity index and H' max a natural logarithm of the total number of pollen types
present in the samples. The indices were calculated using the Past program (Paleontological
statistic) version 3.0.
In order to determine the similarity and frequency of pollen types from the pollen
samples, a cluster analysis (phylogenetic signal) was performed along with a pollen diagram
for the most representative botanical families in the samples. The set of mutual interactions
between plant and pollinator was represented through a bipartite graph, generated from the
binary matrix (absence and presence) of the pollen types collected. The R program was used to
create ecological indices and interaction networks (packages: vegan, rioja and bipartite).
Network metrics were verified from the connectance and degree of nestedness.
Connectance was calculated using the formula C = E/AP, where C is the ratio between the
number of interactions observed, E is the pollen types identified and AP the universe of possible
interactions (A= number of bee species involved and P= amount of plants with melliferous
potential in the area). Nestedness, on the other hand, was determined from the NODF
(Nestedness Metric Based On Overlap And Decreasing Fill), using the CC null model (cored
rows, cored columns), inspired by its theoretical consistency (Guimarães & Guimarães, 2006).
WNODF was also used with the RCTA null model (Row and Column Totals Average) based
on the quantitative matrix of the data (Almeida-Neto & Ulrich, 2011). For both metrics,
FALCON software was used (a software package for analyzing nestedness in bipartite
networks) loaded through the R platform (Beckett et al., 2014).
71
Results
A total of 61 pollen types were identified for the three bees (Melipona dubia, Melipona
seminigra and Scaptotrigona sp.), which are distributed in 24 botanical families. Only two
pollen types were unidentifiable. In general, the most representative botanical families in this
study were: Melastomataceae, Anacardiaceae, Euphorbiaceae, Dilleniaceae, Myrtaceae and
Fabaceae (Mimosoideae and Caesalpinioideae). In this scenario, the Meslatomataceae family
proved to be particularly important for bees in the genus Melipona, presenting high percentages,
while the Euphorbiaceae families, along with Fabaceae and Myrtaceae were preferred by
Scaptotrigona sp. bee.
Melipona dubia –Vila Nova II Community
For this bee, the storage pots (n=8) presented between nine and 16 distinct pollen types,
with the most representative being Miconia type found in seven pots and presenting frequencies
above 90%, characterized as a "temporary specialization". Additionally, only one pot (P=6)
presented a percentage above 10% and was therefore attractive to the bee. The other pollen
types presented frequencies below 10% and were not considered attractive for this bee (Table
1 and Figure 2).
Table 1: Frequency of pollen types in pollen pots collected by Melipona dubia in the Vila Nova II indigenous Community,
located between the Marau river in the municipality of Maués, Amazonas, Brazil. P (Pots).
Family/Pollen types P1 P2 P3 P4 P5 P6 P7 P8
ANACARDIACEAE
Spondias mombin 0.17 0.17
ARECACEAE
Euterpe 0.17 0.17 0.17 0.17
Maximiliana maripa 0.17 0.17 1.33 2.83 3.00 9.33 0.17 0.50
Type 0.50 0.17 0.17
BURSERACEAE
Protium heptaphyllum 0.17 0.17 0.67 0.33 2.33 0.33 0.17 1.33
CHRYSOBALANACEAE
Couepia longipendula 0.17
CYPERACEAE
Type 0.17 0.17 0.17
DICHAPETALACEAE
Tapura lanceolata 0.17 0.17 0.17 0.67 0.17 1.67 0.17 0.17
DILLENIACEAE
Doliocarpus 0.50 1.00 1.83 0.67 2.00 4.00 0.17 3.83
72
Continuation
EUPHORBIACEAE
Alchornea 2.17 0.67 4.67 0.17
Aparisthimium 0.50 0.17 0.17
Micandra 0.17 0.17
Sebastiana brasiliensis 0.17 0.17 0.17 0.17 0.17 0.17 0.17
Schizolobium amazonicum 0.17
Sclerolobium hypoleucum 0.17 0.17
FABACEAE/FABOIDEAE
Desmodium 2.17
HYPERICACEAE
Vismia 0.17
MELASTOMATACEAE
Miconia 97.67 97.33 92.67 91.67 90.17 76.83 98.17 92.50
Type 0.17
MYRTACEAE
Eugenia 0.17 0.17 0.17 0.17
SALICACEAE
Lindackeria 0.17 0.33 0.17 0.17
SAPINDACEAE
Paullinia cupana 0.17 0.50 0.17 0.17 0.17 1.50 0.17 0.17
TOTAL 100 100 100 100 100 100 100 100
Number of pollen types 13 9 11 13 11 16 12 15
73
Figure 2: Photomicrographs of predominant pollen types found in pollen samples from Melipona dubia, Melipona
seminigra and Scaptotrigona sp. in the Nova América, Nova Esperança and Vila Nova II indigenous communities.
Alchornea type (A,B); Amanoa guianensis (C,D); Cassia type (E,F); Croton cajucara (G,H); Doliocarpus type (I,J);
Eugenia type (K,L); Maximiliana maripa (M,N); Miconia type (O,P). Scale bars: 10 µm.
74
Figure 3: Photomicrographs of predominant pollen types found in pollen samples of Melipona dubia, Melipona
seminigra and Scaptotrigona sp. in the Nova América, Nova Esperança and Vila Nova II indigenous communities.
Mimosa pudica (A,B); Protium heptaphyllum (C,D); Sclerolobium hypoleucum (E,F); Sebastiana brasiliensis (G,H);
Spondias mombin (I,J); Stryphnodendron guianense (K,L). Scale bars: 10 µm.
75
Melipona seminigra –Nova Esperança Community
The richness presented by this bee in 21 storage pots ranged from two to 22 pollen types,
with Miconia type (nine pots) presenting frequencies above 90%, characterizing a "temporary
specialization". The pollen types considered attractive (10%) were: Spondias mombin,
Maximiliana maripa, Protium heptaphyllum, Doliocarpus type, Sebastiana brasiliensis,
Mimosa pudica, Miconia type and Eugenia type. All other pollen types presented frequencies
below 10%, and therefore were not considered attractive (Table II and Figure 2 and 3).
76
Table 2: Frequency of pollen types in pollen pots collected by Melipona seminigra in the Nova Esperança indigenous community, located between the Marau river in the municipality of Maués,
Amazonas, Brazil. P (Pots).
Family/Pollen types P1 P2 P3 P4 P5 P6 P7 P8 P9 P10 P11 P12 P13 P14 P15 P16 P17 P18 P19 P20 P21
ANACARDIACEAE
Spondias mombin 0.17 0.50 0.33 40.17 0.17 1.17 0.33 0.17 20.83 0.17 0.17 4.17 0.33 0.17 0.17 0.17
Tapirira guianensis 6.67 0.17 2.00 0.17 1.33 0.17 0.33 0.17 0.17
Type 0.67 0.17 0.17
ARECACEAE
Elaeis 0.17 0.17
Euterpe 0.17 2.67 0.17 0.17 3.67 0.17 0.17 0.17
Maximiliana maripa 2.00 0.17 0.17 23.50 1.50 2.00 2.00 0.17 0.17 1.67 0.33 3.00 0.33 0.33 0.83
Type 0.17 0.17
BURSERACEAE
Protium heptaphyllum 2.33 0.17 0.50 0.17 0.17 1.00 0.17 12.67 0.17 0.17 0.33 1.17 1.33 0.17 0.17 0.17 0.67
CHRYSOBALANACEAE
Couepia 0.17
CYPERACEAE
Type 0.50 0.17
DICHAPETALACEAE
Tapura lanceolata 0.17 1.33
DILLENIACEAE
Doliocarpus 0.17 0.17 0.17 0.00 0.67 0.17 69.50 0.50 0.50 0.17 0.50 13.33 1.83 0.17 13.83 0.17
EUPHORBIACEAE
Alchornea 0.17 0.17
Micandra 0.17 1.67 0.33 0.67 0.17
Sebastiana brasiliensis 1.67 51.67 0.17 0.17 2.17 33.50 0.50 1.50 0.33 63.00 0.17 7.67 23.50 58.50 0.17 30.67 72.67
FABACEAE/FABOIDEAE
Swartzia 0.17 0.17 0.17 0.17 0.33
Type 0.33 0.17 0.17 0.17
77
Continuation
Bauhinia 0.17 0.33
Cynometra 0.83 0.17
Sclerolobium hypoleucum 0.17 0.33 0.17 0.17
Mimosa spruceana 0.67 0.17 0.17 0.83 0.17 0.17 0.33 0.17
Mimosa pigra 1.00
Mimosa pudica 0.17 59.17 35.17 1.50 0.17
HYPERICACEAE
Vismia 0.17 0.17 0.17 0.17 0.17 0.17 0.17
LECYTHIDACEAE
Eschweilera tenuifolia 0.17 0.17
MALPIGHIACEAE
Byrsonima 6.83 0.83 3.17 0.17 0.17
MELASTOMATACEAE
Bellucia 0.50
Miconia 94.67 39.33 91.17 96.00 99.83 28.33 35.50 94.00 15.17 98.33 24.17 6.17 72.83 26.67 99.33 17.33 80.17 57.17 98.83 6.83 99.17
Type 0.33 0.17 0.50 2.00 0.17 0.17
MYRTACEAE
Eugenia 1.00 4.67 0.17 1.00 0.17 0.67 16.83 0.33 0.50 0.17 11.67 0.33 15.00 9.17 0.17 11.00 0.33 7.50 0.17 2.33 0.17
Syzygium 0.17 0.33 0.17 1.00 0.17 0.17 0.33 0.33 0.67 0.17 0.33 0.17 0.50
POLYGALACEAE
Bredemeyra floribunda 0.17
RUBIACEAE
Isertia 1.00 0.67 0.17 0.33 1.33 0.17 0.17
Palicourea 0.17
Warszewiczia 0.17
SALICACEAE
78
Continuation
Casearia grandiflora
0.17 0.17
SAPINDACEAE
Paullinia cupana 0.17 0.17
Matayba 0.17 0.67
INDETERMINATE
Type 0.17 0.17
Total % 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100
Number of pollen types 6 13 11 16 2 10 22 11 18 10 10 13 12 11 5 16 14 15 8 13 6
79
Scaptotrigona sp. –Nova América Community
For Scaptotrigona sp., the samples from 22 storage pots showed a richness ranging
from 10 to 20 pollen types, presenting Croton cajucara (P=1, P=8 and P=18) and Eugenia
type (P=6) with frequencies greater than 90%, which was considered "temporary
specialization". Pollen types characterized as attractive for this bee (10%) were: Doliocarpus
type, Alchornea type, Amanoa guianensis, Croton cajucara, Cassia type, Sclerolobium
hypoleucum, Stryphnodendron guianense and Eugenia type. The other pollen types
presented frequencies below 10% (Table III and Figure 2 and 3).
80
Table 3: Frequency of pollen types in pollen pots collected by Scaptotrigona sp. in the Nova América indigenous, located between the Marau river in the municipality of Maués, Amazonas, Brazil. P (Pots).
Family/Pollen types P1 P2 P3 P4 P5 P6 P7 P8 P9 P10 P11 P12 P13 P14 P15 P16 P17 P18 P19 P20 P21 P22
ANACARDIACEAE
Spondias mombin 0.17 1.00 0.17 0.17 0.17 0.17 0.17 4.00 2.33 0.50 0.17 0.67 0.17 0.33 0.17 0.83
Tapirira guianensis 0.17 0.17 0.17 0.50 0.17 0.17 0.33 0.17 0.33 0.17 0.17 0.17 0.33
ARECACEAE
Elaeis 0.17
Euterpe 0.17 0.17 0.17 0.17
Maximiliana maripa 0.17 0.17 0.17 0.17 0.17
ASTERACEAE
Artemisia 0.17 0.17 0.17
Type 0.33 0.17
BIGNONIACEAE
Martinella 0.17 0.83 0.17 0.17 0.83 0.17 0.17 1.33 0.17 0.17 0.17
CHRYSOBALANACEAE
Couepia 0.17 0.17
CYPERACEAE
Type 0.33 0.17 0.17 0.33 0.50 0.17 0.50 0.17 0.33 0.17 0.17 0.17 0.17 0.17 0.17
DICHAPETALACEAE
Tapura lanceolata 0.17 0.17 0.17 0.17 0.17 0.17
DILLENIACEAE
Doliocarpus 0.33 0.33 0.83 0.67 0.17 0.17 0.17 27.17 17.33 16.83 13.00 0.17 0.17 31.50
EUPHORBIACEAE
Alchornea 0.50 8.50 2.67 1.67 2.33 0.67 41.00 0.33 0.17 2.17 12.50 4.00 10.17 0.50 14.17 8.17 22.50 0.17 2.33 5.17 26.83 5.67
Amanoa guianensis 0.17 0.67 0.17 0.17 0.17 0.17 0.17 0.17 0.17 5.17 0.17 5.00 4.83 3.33 0.17 19.50 21.33 1.83
Aparisthimium cordatum 0.17 1.67 0.17 0.17 0.17 1.00 0.17 0.17
Croton cajucara 94.50 71.00 89.67 83.00 48.83 0.83 42.17 91.33 74.50 77.17 22.50 5.00 46.67 20.00 29.83 64.83 49.00 97.50 43.50 23.83 15.17 40.83
Sapium 0.17
81
Continuation
Sebastiana brasiliensis 0.17 0.33 0.17 0.17 0.17 0.17 0.17 0.17 0.17
Andina 0.33 0.33 0.33 0.33
Cassia quinguangulata 0.17
Cassia 0.17 5.33 0.17 4.00 0.17 4.33 0.50 0.17 0.33 23.17 21.50 0.33 0.17 0.17 0.17 3.00 0.17 0.33 8.00
Sclerolobium hypoleucum 1.17 9.83 3.17 3.50 37.17 3.00 5.33 4.67 1.33 15.83 20.17 59.67 4.50 0.17 25.17 0.67 5.33 1.00 9.50 46.67 1.33 34.00
FABACEAE/FABOIDEAE
Crotalaria 0.17
Type 0.50 0.17 1.00 0.17 0.17 0.17 0.17
Stryphnodendron guianense 0.33 3.17 1.00 0.67 1.17 0.17 2.00 0.17 0.17 0.50 15.33 4.67 3.50 0.17 3.00 2.00 3.50 2.33 1.00 2.00 4.67
HYPERICACEAE
Vismia 0.17 0.33 0.17
LECYTHIDACEAE
Eschweilera tenuifolia 0.33 0.17
MALPIGHIACEAE
Byrsonima 0.17 0.17 0.17 0.17 0.17 0.17 0.17 0.17 0.17
MELASTOMATACEAE
Miconia 0.50 0.17 0.33 0.17 3.50 0.17 0.17 0.17 0.17 0.17 0.33 0.17 0.17 0.17 0.33 0.33 0.33 0.17 0.17 0.33 0.50
MORACEAE
Type 0.17
MYRTACEAE
Eugenia 1.00 0.17 1.67 9.50 0.83 94.17 0.17 1.00 21.67 1.83 0.50 0.17 0.67 77.67 1.17 0.17 0.33 0.33 38.17 1.83 0.50 2.67
POACEAE
Type 1 0.17 0.17 0.17
Type 2 0.17 0.17 0.17 0.17 0.17 0.17
POLYGALACEAE
82
Continuation
RHAMNACEAE
Gouania 0.17 0.17
SALICACEAE
Casearia javitensis 0.17
SAPINDACEAE
URTICACEAE
Cecropia 0.17 0.17 0.17 0.17 0.17
INDETERMINATE
Type 0.17
TOTAL 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100
Number of pollen types 16 12 13 11 16 12 17 14 18 17 16 14 16 14 17 19 20 10 12 17 13 15
83
Ecological indices and trophic interaction
Scaptotrigona sp. presented higher diversity and, consequently, higher uniformity in its
pollen collections (H' = 1.66 and J’= 0.45), followed by Melipona seminigra (H' = 1.43 and J’=
0.39) and Melipona dubia with (H' = 0.45 and J’= 0.14) (Figure 4).
Figure 4: Diversity (H') and similarity (J') values for the three bee species: Melipona dubia, Melipona seminigra
and Scaptotrigona sp.
The set of interactions of bee species based on the identified pollen types was
represented by the bipartite graph, in which four of the 61 pollen types were unique for
Melipona dubia, 13 types for Melipona seminigra and 16 pollen types for Scaptotrigona sp.
The bee Melipona dubia shared 21 types, Scaptotrigona sp. shared 24 types and Melipona
seminigra shared 26 types. Among the three bees, 15 pollen types were shared, with the
Miconia, Croton cajucara and Eugenia types presenting high frequencies (Figure 5A).
84
Figure 5: A) Bipartite graph showing the presence and absence of trophic interaction between the three bee species in
three indigenous communities (Nova América, Nova Esperança and Vila Nova II). B) NODF graph based on the presence
and absence matrix of pollen samples from the three bee species in three indigenous communities. C) WNODF graph based
on quantitative matrix of pollen samples from three bee species in three indigenous communities.
85
For the three bee species studied in the three communities, the metrics showed a
connectance of 19.37%, with the degree of nestedness for both the presence and absence of
pollen types (NODF = 54.07) and quantitative data (WNODF=34.03) being significant
(p<0.01), and high nestedness of the interaction network between the bees studied and the plants
used as trophic resources (Figure 5B and C).
The pollen diagram shows the most representative families collected by the bees, with
emphasis on: Anacardiaceae, Dilleniaceae, Euphorbiaceae, Fabaceae, Melastomataceae and
Myrtaceae. These families indicate a similarity of the pollen types collected among the bees
studied, which was highlighted by the high collection frequencies, leading to the formation of
two groups: one with Melipona dubia and Melipona seminigra in which the Melastomataceae
family contributed the most to this grouping with Miconia type; group two was only formed by
Scaptotrigona sp. due to the strong presence of pollen types of families Euphorbiaceae,
Fabaceae, Myrtaceae and Dilleniaceae (Figure 6).
Figure 6: Pollen and cluster diagram showing the frequency of pollen types and the formation of each bee group.
Key: Md: Melipona dubia; Ms: Melipona seminigra; S: Scaptotrigona sp.
86
Discussion
The data presented here corroborates recent studies about pollen contained in honey
samples from the Sateré Mawé indigenous communities, presenting a richness of pollen types
compatible with the present study (Rezende et al., 2018).
Melipona seminigra, Melipona dubia and Scaptotrigona sp. acquire floral resources
from a large number of plant species belonging to several botanical families, and these bees are
considered generalists (Ramalho et al., 2007). However, when comparing the resources
collected by Melipona bees with Scaptotrigona bees, their different body sizes and demands
for different resources should be considered. Thus, the constant need for resources can
determine the degree of generalization of a colony (Kajobe 2006, 2007; Ramalho et al., 2007),
and depending on the availability of food, these bees can behave as generalists or specialists
(Roubik & Moreno, 2000). Furthermore, Swihart et al. (2003) suggest that generalist species
are more likely to meet their demands and needs in different habitats. In contrast, more
specialized species rely on fewer sources to meet their energetic demands, ensuring their
survival in a restricted number of habitats (Quinn et al., 1998).
Regarding body size, we show that it has little influence on the richness of pollen types
collected, as several studies with trophic resources in the Brazilian Amazon have revealed that
stingless bee species with smaller sizes and high offspring rates, such as Tetragonisca angustula
(Novais et al., 2013); Scaptotrigona filvicutis (Marques-Souza et al., 2007) and Frieseomellita
varia (Marques- Souza, 2010), present a substantially larger diversity of resources compared to
studies with larger Melipona bees whose offspring rates are relatively lower, such as M.
seminigra merrillae and M. interrupta (Ferreira & Absy, 2015, 2017a, 2017b). This subtlety
can be seen in Ferreira & Absy (2015), in which the authors studied two Melipona bee species
and found that even though M. interrupta was considered a larger bee, its niche was lower than
M. seminigra merrillae, which has a greater number of individuals in its hive (Peralta, 1999)
and consequently, more workers on flowers. This relationship corroborates data found by
Rezende et al. (2018) for Scaptotrigona sp., which presents a smaller body size and collected
43 pollen types, and M. seminigra, which collected 34 pollen types and presents a larger body
size. Thus, both among stingless bee species of the same genus (Ferreira & Absy, 2015, 2017a)
and species of different genera (Rezende et al., 2018), we found that the factor that may have
the greatest influence on the trophic niche is the maintenance of offspring, that is, the more
individuals in the hive the higher the demand (need) for trophic resources is.
For M. dubia and M. seminigra, polliniferous plants, mainly Myconia type, represented
the main resources collected. Such data corroborates previous studies with stingless bees, which
87
showed the strong relationship between Melipona bees and the Melastomataceae family (Absy
& Kerr, 1977; Marques-Souza et al., 2002; Ferreira & Absy, 2015, 2017b). Most often, they
present percentages above 90 %, causing these bees to present temporary specialization for this
trophic resource (Ferreira & Absy, 2015, 2017b).
The strong relationship of plants with poricidal anthers and Melipona bees could be
partially explained by the coevolutionary aspect, in which bees of this genus are able to extract
the powdery pulverulent pollen from poricidal anther through the vibration of the flight
musculature, known as "buzz pollination” (Buchmann, 1983; Renner, 1983).
The number of pollen types collected by Melipona dubia was lower compared to
Melipona seminigra. Therefore, we have to consider whether the number of pots analyzed in
Melipona seminigra (n=21) was higher than Melipona dubia (n=8), as it could have influenced
this difference in the number of pollen types for bees of the same genus.
Although most pollen types are attractive to the bees studied (>10%), we highlight the
importance of Myrtaceae and Melastomataceae families, as well as species of the
Anacardiaceae, Arecaceae, Burseraceae, Dilleniaceae and Fabaceae families. Such botanical
groups have also been reported with high percentages in other studies about the pollen of these
bees (Absy & Kerr, 1977; Absy et al., 1980,1984; Ferreira & Absy, 2015, 2017a,2017b).
For Scaptotrigona sp., the Myrtaceae and Euphorbiaceae families were particularly
important, as they presented temporary specialization (>90%). While studying pollen from
Scaptotrigona fulvicutis, Marques-Souza et al. (2007) also verified the importance of these
families with Myrcia amazonica and Croton matourensis in the analyzed samples, which were
also significant in the collections herein. The same was verified by Ferreira et al. (2010) when
analyzing the pollen collected by Scaptotrigona depilis, highlighting the clear preference for
Myrtaceae pollen types.
The pollen types that presented frequency below 10% (less attractive) for the three bee
species studied here are considered additional resources that help maintain colonies, as they act
as key resources in relation to seasonal variations (Ramalho et al., 1985).
Highlighting the importance of adding palynological data to network analyses (Ferreira
& Absy, 2015), the data from the present study showed a universe of only 315 possible
interactions, 61 of which were carried out by confirming the presence of pollen, which
generated 19.37 % connectance. Although they presented few bee species when compared to
other studies (Pigozzo & Vianna, 2010), the connectance of the interaction network found here
was similar to that presented by Biesmeijer et al. (2005), who worked with a higher number of
social bees in several localities in Brazil and recorded 19% connectance. Using only
palynological data, Ferreira & Absy (2015) analyzed the interaction of only two bee species
88
(Melipona seminigra and Melipona interrupta) in the Amazon, resulting in high connectance
(28%). The same authors support that including palynological data significantly increases the
number of interactions compared to only observation data in the field (Bosch et al., 2009;
Olesen et al., 2010; Absy et al., 2018). Such fact can be observed in most studies with
connectance (Viana & Kleinert, 2006; Rodarte et al., 2008; Biesmeijer et al., 2005) in which a
universe of possible interactions that is much larger than those actually carried out is presented.
This can be seen in Pigozzo & Vianna (2010), who presented a universe of 2,800 possible
interactions, of which only 296 were observed, presenting a connectance of 10.6 %.
Optional mutual interactions with a set of specialized species interacting with
generalists (plants and pollinators), as seen here, tend to have a nested network structure
(Bascompte et al., 2003; Guimarães Jr., 2009). However, nestedness for bee species that share
many resources can be strongly linked to the degree of local fragmentation and decrease in
established interactions, that is, the loss of generalist species would consequently decrease the
degree of nestedness (Guimarães Jr., 2009). In addition to the bipartite representation model for
mutual species (Figure 5A), herein we explored the nestedness metrics (NODF and WNODF)
used for both binary and quantitative matrices, generated by the set of interactions between the
bees and the identified and quantified pollen types. Considering the generalist pattern of the
species involved in these interactions, both the number of overlap and abundance of shared
pollen types highlight a high degree of nestedness that is significant for both verified metrics.
However, nestedness was higher for the binary matrix represented by NODF (Figure 5B), which
can be explained by the fact that these social bees have large populations and present high
pollen resource demands. On the other hand, few shared pollen types showed large proportions,
which indicates lower nestedness for the quantitative matrix, since WNODF (Figure 5C)
presents a greater weight for pollen types with high proportions, thus generating "strong"
interactions and highlighting the presence of specializations (Bascompte et al., 2006; Vázquez
et al., 2007). In this case, the WNODF may represent the uniqueness of each bee species, for
example: pollen types such as Miconia (Melastomataceae) proved to be strongly related to
Melipona bees, presenting high proportions, whereas Croton cajucara (Euphorbiaceae) and
Eugenia (Myrtaceae) pollen types were most frequent for the Scaptotrigona bee (Table 1, 2 and
3). Significant nestedness in mutualistic networks (plant-pollinator), as well as connectance,
was also verified by Bosch et al. (2009), both for field observations, pollen only, and in both
approaches. Although the field and pollen observations were not significant, Absy et al. (2018)
found that they were significant when the data sets were combined (field observations + pollen).
Few studies using these nestedness metrics have been conducted on mutualistic networks of
plants and bees, however, it is clear that the addition of palynologic data significantly increases
89
the links that field observations alone may not detect (Bosch et al., 2009; Ferreira & Absy,
2015; Absy et al., 2018).
The preference (presence and proportion) for pollen resources identified here allowed
us to verify the phylogenetic signal of these bees from the Cluster analysis, resulting in two
distinct groups: one composed of Melipona dubia and Melipona seminigra and the other formed
by Scaptotrigona sp.. This formation indicates evolutionary aspects strongly related to
preference for trophic resources, as the same was verified in honey samples for the same bees
in similar localities (Rezende et al., 2018). Bees of the genus Melipona tend to have similar
niches, especially in the same location, showing high overlap rates (Ferreira & Absy, 2015,
2017a). In this study, as mentioned above, the grouping between Melipona species was
conditioned by "strong" interactions, mainly due to the high frequencies of collections
(specializations) of the Miconia type (Meslatomataceae). On the other hand, the group formed
by the Scaptotrigona sp. bee was conditioned by the broader preference, highlighted by the high
rates of diversity, equitability and the high percentages of certain pollen types, such as: Croton
cajucara (Euphorbiaceae) and Eugenia (Myrtaceae).
Based on these results, we can verify the importance of a large number of plants that
provide trophic resources for bees kept in the same location, some of which are considered here
as key species for maintaining these bees and in the composition of meliponiculture pasture:
(Spondias mombin, Maximiliana maripa, Protium heptaphyllum, Doliocarpus type, Sebastiana
brasiliensis, Mimosa pudica, Miconia type, Eugenia type, Alchornea type, Amanoa guianensis,
Croton cajucara, Cassia type , Sclerolobium hypoleucum, Stryphnodendron guianense).
However, we emphasize that bees of the genus Melipona (sympatric species) with the
same collection characteristics have some peculiarities, leading to temporary specialization
events and the distinction of Melipona species in a single group.
Even so, both the high network connectance and the high degree of nestedness reveal
that, although they present preferences for certain resources, perennial social bees with a large
number of individuals in their colonies tend to behave as generalists, sharing a large number of
trophic resources.
Acknowledgements
The authors thank the Amazon Research Foundation (FAPEAM) for the scholarship
(002/2016) granted to the first author and for the scholarship and financial support
(062.01180/2015) granted to the third author, the Conselho Nacional de Desenvolvimento
Científico and Tecnológico (CNPq) for the scholarship granted to the second author
90
(Proc.308425/2016-2), the BIONORTE Program for the support, and the Laboratory of
Palynology at the National Institute for Amazonian Research (INPA) for the facilities provided.
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96
4 CONCLUSÃO
A partir dos dados desse estudo foi possível observar a importância das plantas presentes
em área de várzea para a manutenção de espécies de abelhas sem ferrão criadas em comunidades
indígenas. A maioria dessas comunidades se localiza na calha de grandes rios na Amazônia, o
que favorece a criação e manutenção de abelha nativas, tendo em vista que muitas dessas
abelhas também ocorrem naturalmente nessas áreas.
Áreas de várzea na Amazônia, como destacado em diversos estudos supracitados, possui
características peculiares (água abundante e substratos de nidificação) que favorecem a
manutenção dessas abelhas. Além disso, por se tratar de um ecossistema aberto, o regime de
chuvas favorece a rápida recomposição florística e consequentemente o suprimento trófico para
uma grande diversidade de abelhas.
Em suma, essas abelhas estudadas diferenciam sutilmente seu nicho, sendo o gênero
Melipona, que mesmo considerada generalista, teve seu nicho fortemente vinculado a poucos
grupos botânicos (Melastomataceae e Fabaceae), as quais muitas delas caracterizam-se por
apresentarem anteras poricidas dificultando a extração de pólen. No entanto, abelhas desse
gênero são caraterizadas por vibrar a musculatura do tórax na extração de pólen de anteras
poricidas e também não poricidas.
Em contrapartida o gênero Scaptotrigona, com abelhas que apresentam menores
dimensões corporais, teve seu nicho mais amplo nesse estudo, justificado pela alta demanda de
recursos tróficos, já que possui um maior número de indivíduos na colônia. Essa relação foi
constatada em todo estudo quando se compara os nichos de espécies dos dois gêneros em
questão.
Mesmo apresentando particularidades em seus nichos (Melipona e Scaptotrigona),
quando alocadas em uma mesma comunidade revelaram semelhanças na atratividade por
muitos tipos polínicos, o que conferiu uma alta sobreposição de recursos. Tal fato pode estar
relacionado com a presença de plantas melíferas endêmicas de várzea com maior abundância e
grandes inflorescências, diluindo o efeito da competitividade por recursos coletados em
comum. Corroborando essa assertiva, as métricas de rede interações mostraram alto
aninhamento para as abelhas estudadas, além de um alto grau de generalização (porcentagem
de conectância) observado.
Esses dados enfatizam a importância da vegetação de áreas de várzea da Amazônia, pois
mesmo antropizadas, devido a sua rápida recomposição florística, favorecem a criação
(manutenção) de espécies de abelhas nativas, assim como inferências na produtividade de mel.
97
Ainda assim, esses resultados aqui levantados podem contribuir para futuros programas
de manejo e desenvolvimento da meliponicultura em comunidades indígenas da Amazônia,
subsidiando aspectos legais da prática da criação e rotulação dos produtos meliponícolas.
98
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106
6 ANEXOS
___________________________________________________________________________
Submission Confirmation for Pollen niche of Melipona dubia Moure & Kerr, 1950, Melipona seminigra
Cockerell, 1919 and Scaptotrigona sp. Moure, 1942 (Apidae:Meliponini) kept in indigenous
communities of the Sateré Mawé tribe, Amazonas, Brazil.
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INSTITUTO NACIONAL DE PESQUISAS DA

CARACTERIZAÇÃO DAS FONTES DE RECURSOS TRÓFICOS PARA

ALINNE COSTA CAVALCANTE REZENDE

CARACTERIZAÇÃO DAS FONTES DE RECURSOS TRÓFICOS PARA

Tese de doutorado apresentada ao Programa de Pós-

Orientadora: Dra. Maria Lúcia Absy

R467c Rezende, Alinne Costa Cavalcante

Tese (Doutorado - Programa de Pós Graduação em

1. Palinologia. 2. Melissopalinologia. 3. Rede

A Deus, meus pais Daniel e Marlene Cavalcante, meu

Em primeiro lugar eu agradeço a Deus em quem eu acredito e que me ajudou em toda

Então disse Deus: "Cubra-se a terra de vegetação:

importância dessas plantas para a manutenção dessas abelhas e para o desenvolvimento da

Figura 1: Mapa das comunidades Sateré Mawé localizadas no município de Maués,

Plate 1- Photomicrographs of predominant pollen types found in honey samples of

Plate 2- Photomicrographs of predominant pollen types found in honey samples of

Figure 2- Photomicrographs of predominant pollen types found in honey samples of

Figure 3- Photomicrographs of predominant pollen types found in honey samples of

Figure 2: Photomicrographs of predominant pollen types found in pollen samples from

Table 1- Table 1: Frequency of pollen types present in honey from Scaptotrigona

ABSTRACT ..................................................................................................................... viii

LISTA DE TABELAS ..................................................................................................... xii

3 REVISÃO BIBLIOGRÁFICA .................................................................................... 3

Capítulo I. Pollen of honey from Melipona seminigra merrillae Cockerell, 1919,

6 ANEXOS ....................................................................................................................... 106

pólen). Dessa forma, através do conhecimento botânico, o meliponicultor poderá adquirir

3.1 Abelhas sem ferrão

De uma forma geral, as abelhas possuem comportamento solitário ou social, em que

3.2 Déficit de polinizadores

A análise do pólen auxilia no entendimento sobre mecanismo de polinização, recursos

3.4 Tribo indígena Sateré Mawé

4.1 Área de estudo

O Amazonas abrange uma região com 11.458,5km2 de extensão (Saraiva et al.,2009).

4.2 Espécies de abelhas

4.3 Coleta e preparação das amostras de pólen e mel

Um total de 52 amostras de pólen e 48 de mel das cinco comunidades foram estudadas.

4.4 Processamento químico e identificação polínica

As amostras de pólen foram acondicionadas em tubos falcon de 15mL contendo 5mL

4.5 Análise estatística

potencial melíferas do local). Já o aninhamento foi determinado a partir do NODF (Nestedness

REZENDE, A.C.C; ABSY, M.L.; FERREIRA, M.G;

Pollen of honey from Melipona seminigra merrillae Cockerell, 1919; Scaptotrigona

Keywords: Amazon, meliponiculture, pot honey, trophic resources, stingless bee.

Materials and Methods

Study site and honey sample collection

Honey chemical processing and pollen identification

Honey quantitative analysis, statistical indices, and trophic relations

Indigenous community - Ilha Michiles

Indigenous community - Nova Esperança

Indigenous community - Monte Horeb

Type 1 2.83 0.50

Ecological indices and trophic interaction network

Joosten H, de Klerk P. 2002. What’s in a name? Some thoughts on pollen classification,

Louveaux J, Maurizio A, Vorwohl G. 1978. Methods of melissopalynology. Bee World. 59(4):

Marques-Souza AC. 1996. Fontes de pólen exploradas por Melipona compressipes

Ramalho M. 1990. Foraging by Stingless Bees of the Genus, Scaptotrigona (Apidae,

Ramalho M, Imperatriz-Fonseca VL, Kleinert-Giovannini A. 1985. Exploitation of floral

Sá NP, Prato M. 2007. Conhecendo as abelhas: Um projeto de ensino. Bioscience Journal.

Smith N, Dubois J, Current D, Lutz E, Clement C. 1998. Experiências Agro-florestais na

Teixeira P. 2005. Sateré-Mawé: retrato de um povo indígena. Manaus (AM): UNICEF/FNUAP.

Wallace H. 1981. An assessment of diet overlap indexes. Transactions of the American

REZENDE, A.C.C; ABSY, M.L.; FERREIRA, M.G;

Keywords: Native bees, Pollen analysis, Meliponiculture, Brazilian Amazon

In recent years, the rearing of stingless bees in traditional communities of Central