This article was downloaded by: [Dr Jaílson Santos de Novais] On: 15 November 2013, At: 08:43 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Palynology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tpal20 P alynological examination of the pollen pots of native stingless bees from the Lower Amazon region in Pará, Brazil Jaílson Santos de Novais a b & Maria Lúcia Absy b a Centro de Formação Interdisciplinar and Laboratório de Botânica Taxonômica , Universidade Federal do Oeste do Pará , Rua Vera Paz, s/n, Salé, 68035-110 , Santarém , Pará , Brazil b Laboratório de Palinologia, Coordenação de Biodiversidade , Instituto Nacional de Pesquisas da Amazônia , Av. André Araújo, 2.936, Petrópolis, 69067-375 , Manaus , Amazonas , Brazil Accepted author version posted online: 20 Mar 2013.Published online: 01 Nov 2013. To cite this article:Jaílson Santos de Novais & Maria Lúcia Absy (2013) Palynological examinat ion of the pollen pots of native stingless bees from the Lower Amazon region in Pará, Brazil, Palynology, 37:2, 218-230, DOI: 10.1080/01916122.2013.787127 To link to this article: http://dx.doi.org/10.1080/01916122.2013.787127 PLEASE SCROLL DOWN FOR ARTICLE T aylor & Francis makes every effort to ensure the accuracy of all the information (the “ Content”) contained in the publications on our platform. However , T aylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy , completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by T aylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Franc is shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use ofthe Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. T erms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
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8/12/2019 Palynological Examination of Pollen Loads
This article was downloaded by: [Dr Jaílson Santos de Novais]On: 15 November 2013, At: 08:43Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House37-41 Mortimer Street, London W1T 3JH, UK
PalynologyPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/tpal20
Palynological examination of the pollen pots of native
stingless bees from the Lower Amazon region in Pará,
BrazilJaílson Santos de Novais
a b & Maria Lúcia Absy
b
a Centro de Formação Interdisciplinar and Laboratório de Botânica Taxonômica ,
Universidade Federal do Oeste do Pará , Rua Vera Paz, s/n, Salé, 68035-110 , Santarém ,Pará , Brazilb Laboratório de Palinologia, Coordenação de Biodiversidade , Instituto Nacional de
Pesquisas da Amazônia , Av. André Araújo, 2.936, Petrópolis, 69067-375 , Manaus ,
Amazonas , BrazilAccepted author version posted online: 20 Mar 2013.Published online: 01 Nov 2013.
To cite this article: Jaílson Santos de Novais & Maria Lúcia Absy (2013) Palynological examination of the pollen pots of natistingless bees from the Lower Amazon region in Pará, Brazil, Palynology, 37:2, 218-230, DOI: 10.1080/01916122.2013.78712
To link to this article: http://dx.doi.org/10.1080/01916122.2013.787127
PLEASE SCROLL DOWN FOR ARTICLE
Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained
in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make norepresentations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of tContent. Any opinions and views expressed in this publication are the opinions and views of the authors, andare not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon ashould be independently verified with primary sources of information. Taylor and Francis shall not be liable forany losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoeveor howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in anyform to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions
Palynological examination of the pollen pots of native stingless bees from
the Lower Amazon region in Para, Brazil
Jaılson Santos de Novaisa,b* and Maria Lucia Absyb
aCentro de Formac~ao Interdisciplinar and Laboratorio de Botanica Taxonomica, Universidade Federal do Oeste do Para, Rua VeraPaz, s/n, Sal e, 68035-110, Santarem, Para, Brazil; bLaboratorio de Palinologia, Coordenac~ao de Biodiversidade, Instituto Nacional
de Pesquisas da Amazonia, Av. Andre Araujo, 2.936, Petropolis, 69067-375, Manaus, Amazonas, Brazil
This is the first palynological study using pollen stored by Tetragonisca angustula (Apidae: Meliponini) in the LowerAmazon region, Para, Brazil. The samples were directly collected from the pollen pots of T. angustula in apiarieslocated in Belterra and Santarem. The samples were dried, weighed, diluted in warm water and ethanol, centrifugedand then processed using the acetolysis method. After mounting the samples on slides, we identified and countedat least 500 pollen grains per sample. The results indicate that the main pollen combinations in the pollen pots of T. angustula in Belterra include pollen from Byrsonima, Cecropia and Eriope, and the combinations from Santareminclude pollen from Byrsonima, Cecropia, Clidemia hirta, Davilla kunthii , Myrcia and Vismia guianensis. Most pollentypes came from the families Fabaceae and Asteraceae. The pollen diversity (H0) ranged from 0.03 to 1.95, and the
evenness (J0) ranged from 0.04 to 0.79, with the average trend indicating heterogeneity in the collection pattern.Temporary specialisation events typified five of the samples that we studied, directly detecting pollen from Byrsonima,Cecropia and Clidemia hirta. Such events appear to be unrelated to the direct processes of effective pollination. Thepollen spectra obtained corroborate the pollen types that have previously been described in palynological analysesinvolving Tetragonisca angustula in other areas of Brazil.
typically endured by regional ecosystems. This pressure
is primarily in the form of the advance of deforestation
resulting from the rapid expansion of the agricultural
frontier toward the interior of the Brazilian Amazon.
2. Materials and methods
2.1. Study area
The study was conducted in two areas of the Brazilian
Amazon, in the districts of Santarem and Belterra,
Lower Amazon mesoregion of Para, Brazil (Figure 1).
In Belterra [023800700S, 5455053.200W, 126 m above
sea level (a.s.l.)], samples were collected monthly
from the food pots of colonies of T. angustula
(locally known as ‘jataı’ or ‘mosquito-amarela’) in the
apiary owned by the chairman of the Beekeepers
Association of the District of Belterra (Associac~ao de
Meliponicultores do Municıpio de Belterra, AMEM-
BEL) (Plate 1, figure 1). Samples from Santarem were
also collected from the food pots of T. angustula in the
apiary of the Forest School (Escola da Floresta)
(0230049.300S, 5456007.700W, 72 m a.s.l.), an institu-
tion supported by the Borough Education Council
(Secretaria Municipal de Educac~ao, SEMED) (Plate 1,
figures 2 and 3).
The Lower Amazon encompasses one of six geo-
graphical mesoregions in Para, with an average annual
rainfall of approximately 1900 mm and an average
temperature of 25 C. The regional climate is hot and
humid (Am) (Albuquerque et al. 2010; EMBRAPA
2012). The stingless bees apiary (meliponary) in
Belterra is located in an urban area, mainly surrounded
Figure 1. (A) A map showing where Brazil (shaded in light grey) is located within South America, and (B) a map showing thestates of Brazil, and the location of the two sites studied (Belterra and Santarem). The states of Brazil that are considered thenorthern region are labelled.
Palynology 219
8/12/2019 Palynological Examination of Pollen Loads
Figure 2. Seasonal distribution in the number of pollen types, Shannon-Weaver diversity (H0) and Pielou’s evenness (J0) indexesamong pollen samples obtained from pollen pots of Tetragonisca angustula in Belterra, Lower Amazon region, Para State, Brazil.
Plate 1. Areas studied in the Lower Amazon region, Para State (PA), Brazil. Figure 1. Meliponary (stingless bee apiary) sited inthe urban zone of Belterra. Figure 2. Hive of Tetragonisca angustula located at the Forest School, Santarem, PA. Figure 3. Viewfrom the Forest School in Santarem.
Figure 3. Seasonal distribution in the number of pollen types, Shannon-Weaver diversity (H0) and Pielou’s evenness (J0) indexesamong pollen samples harvested from pollen pots of Tetragonisca angustula in Santarem, Lower Amazon region, Para State,Brazil.
220 J.S. de Novais and M.L. Absy
8/12/2019 Palynological Examination of Pollen Loads
q u e n c y ( % ) o f p o l l e n t y p e s i n e a c h p o l l e n m o n t h l y s a m p l e c o l l e c t e d , S h a n n o n - W e a v e r D i v e r s i t y I n d e x ( H 0 ) , P i e l o u ’ s E v e n n e s s I n d e x ( J 0
) , t h e
o v e r a l l t o t a l s , a n d t h e t a x o n ’ s
h a b i t o f t h e p o l l e n s t o r e d b y T e t r a g o n i s c a a n g u s t u l a ( L a t r e i l l e ) f r o m S a n t a r e m , L o w e r A m a z o n r e g i o n , P a r a S t a t e , B r a z
i l . P . O . : p e r c e n t a g e o f
o c c u r r e n c e ( % ) o f e a c h p o l l e n t y p e c o n s i d e r i n g a l l t h e s a m p l e s a n a l y s e d
( p r e s e n c e / a b s e n c e ) . C . O . : c l a s s e s o f o c c u r r e n c e ( R : r a r e . I : i n f r e q u e n t . F : f r e q u e n
t . V F : v e r y f r e q u e n t . ) .
2 0 1 0
2 0 1 1
P l a n t F a m i l y ,
P o l l e n T y p e
O
c t
N o v
D e c
J a
n
F e b
M a r
A p r
M a y
P . O .
( % )
C . O .
H a b i t
A c a n t h a c e a e ,
J u s t i c i a
0
, 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 5 7
0 , 0 0
1 3
I
s h r u b
A m a r a n t h a c e a e ,
A m a r a n t h u s v i r i d i s
0
, 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
1 , 1 4
0 , 0 0
1 3
I
h e r b
A n a c a r d i a c e a e ,
T a p i r i r a g u i a n e n s i s
0
, 0 0
0 , 9 4
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
1 3
I
t r e e
A s t e r a c e a e ,
E m i l i a f o s b e r g i i
0
, 0 0
0 , 3 7
0 , 3 9
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
1 1 , 8 7
3 8
F
h e r b
A s t e r a c e a e ,
E u p a t o r i u m
1
, 7 9
0 , 0 0
0 , 0 0
0 , 0 0
0 , 1 5
0 , 1 9
0 , 0 0
0 , 0 0
3 8
F
h e r b / s u b - s h r u b
B u r s e r a c e a e ,
P r o t i u m
0
, 0 0
0 , 0 0
1 , 5 7
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
1 3
I
s h r u b / t r e e
D i l l e n i a c e a e ,
D a v i l l a k u n t h i i
0
, 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
8 3 , 1
1
1 , 1 7
2 5
F
s h r u b / l i a n a
E u p h o r b i a c e a e ,
A c a l y p h a
0
, 0 0
0 , 0 0
0 , 0 0
1 1
, 5 5
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
1 3
I
h e r b / s u b - s h r u b
F a b a c e a e ,
M a c h a e r i u m
0
, 0 0
0 , 0 0
1 0 , 0 4
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
1 3
I
s h r u b / t r e e
F a b a c e a e ,
M a c r o l o b i u m
0
, 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
2 , 6 8
1 3
I
t r e e
F a b a c e a e , S e n n a
0
, 0 0
0 , 0 0
1 0 , 6 3
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
1 3
I
t r e e
F a b a c e a e ,
P i p t a d e n i a
0
, 0 0
0 , 0 0
0 , 9 8
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
1 3
I
s h r u b / t r e e / l i a n a
F a b a c e a e ,
S t r y p h n o d e n d r o n
p u l c h e r r i m u m
1
, 0 7
0 , 0 0
0 , 0 0
0 , 1 8
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
2 5
F
s h r u b / t r e e
H y p e r i c a c e a e ,
V i s m i a
g u i a n e n s i s
3
3 , 2 1
0 , 0 0
7 2 , 4 4
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
2 5
F
t r e e
M a l p i g h i a c e a e ,
B y r s o n i m a
0
, 0 0
0 , 0 0
0 , 0 0
0 , 0 0
9 2 , 1 0
0 , 1 9
0 , 0 0
0 , 0 0
2 5
F
s h r u b / t r e e
M a l v a c e a e ,
B o m b a c o i d e a e
0
, 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 1 9
0 , 0 0
2 , 0 1
2 5
F
t r e e
M e l a s t o m a t a c e a e ,
C l i d e m a h i r t a
0
, 0 0
9 8 , 3 1
0 , 0 0
0 , 0 0
0 , 0 0
9 0 , 6 5
0 , 0 0
7 4 , 4 1
3 8
F
s h r u b
M y r t a c e a e ,
M y r c i a
0
, 0 0
0 , 0 0
0 , 0 0
8 8
, 2 7
1 , 9 8
0 , 0 0
0 , 0 0
0 , 0 0
2 5
F
s h r u b
P h y t o l a c c a c e a e ,
M i c r o t e a
0
, 5 4
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
0 , 0 0
3 , 0 4
6 , 1 9
3 8
F
h e r b
( c o n t i n u e d )
Palynology 225
8/12/2019 Palynological Examination of Pollen Loads
Tetragonisca angustula used plant species common to
the areas studied as pollen sources and even displayed
a pattern that can be characterised, among other fac-
tors, by temporary specialisation events, which appear
to be unrelated to effective pollination processes. Eco-
logical indices indicate a small range of pollen niche,which corroborates some previously published data in
the literature. In addition, such indices also indicate a
heterogeneous pattern of resource collection by
Tetragonisca angustula.
Acknowledgements
We express our sincere thanks to: Mr Geancarlo V. Gouveia,chairman of AMEMBEL (Stingless Beekeepers Associationof the District of Belterra), for authorising the collection of pollen samples at his private apiary; to the board of theForest School (Escola da Floresta) and to SEMED (BoroughEducation Council) for allowing the collection of samples at
the institution’s apiary; to Dr Claudia Elena Carneiro of
UEFS (Bahia State University at Feira de Santana), ChienoSuemitsu and Dr Lenise Vargas Flores, both of UFOPA(Western Para Federal University), who are supervisors of the laboratories used for processing and analysing the paly-nological samples; to Dr Favızia Freitas de Oliveira of UFBA (Bahia Federal University) for identifying the sting-less bee species; to the research fellows Alcides Froes DiasJr., Angelo Marcio Barbosa Bastos Jr. and Bruno HenriqueAndrade-Silva for helping with laboratory activities; toM.Sc. Leilton Santos Damascena, for helping with the maps;to the National Council for Scientific and Technological Devel-opment (Conselho Nacional de Desenvolvimento Cientıfico eTecnologico, CNPq) for funding the project (Processes575747/2008-0, 143084/2009-7 and 477127/2011-8), and to
the anonymous referees for helping us with valuable commentson this manuscript.
Author biographies
JAILSON SANTOS DE NOVAIS is anAssistant Professor at the Centre forInterdisciplinary Education at WesternPara Federal University (UFOPA),Santarem, Brazil. He received his Bach-elor’s degree in Biological Sciences in2007 from Bahia State University atFeira de Santana (UEFS), Feira de San-tana, Brazil, and his Masters in Botany
in 2009 from the same institution. Ja
ılson is currently finish-ing his Ph.D. thesis in Botany at the National Institute forAmazon Research (INPA), Manaus, Brazil. His currentresearch is on honey and pollen harvested by native stinglessbee species from Brazilian Amazon and caatinga vegetation(semi-arid zone in northeast Brazil). Novais’s research inter-ests centre on melissopalynology, stingless bees floral prefer-ences and palynology applied to meliponiculture.
MARIA L UCIA ABSY is a research palynologist for theNational Institute for Amazon Research (INPA), Manaus,Brazil. She received her Bachelor’s degree in Natural Historyin 1968 from the Catholic University of Parana, Curitiba,
Parana, her Masters in Botany in 1972 from the Universityof S~ao Paulo (USP), S~ao Paulo, and her Ph.D. in Mathemat-ics and Natural Sciences in 1979 from the University of Amsterdam, The Netherlands. Absy’s research for INPAcentres on pollen to determine foraging resources of nativestingless Amazon bees. She also analyses the pollen in honeyto determine the food sources of honey bees, and the types of honey. Another aspect of her research in palynology rests is
the study of fossil pollen with emphasis on the Quaternary.She has written several journal articles, chapters and books.
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