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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

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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.

Keywords: melissopalynology; entomopalynology; meliponiculture; ‘jataı’ stingless bee; Tetragonisca angustula;Meliponini

1. Introduction

Palynology provides data that help to understand the

trophic, ecological and evolutionary links between bees

and plant groups. Over the past few decades, studies of

this type have been infrequent in the Amazon region, avast area encompassing the planet’s largest tropical

biodiversity. Palynological analyses of honey (Oliveira

et al. 1998; Silva & Reboucas 1998; Silva & Absy 2000;

Marques et al. 2011; Martins et al. 2011), nectar from

the honey stomach (Absy et al. 1980), corbicular pollen

(Marques-Souza 1996, 2010; Marques-Souza et al.

1993, 1995, 1996, 2002, 2007; Oliveira et al. 2009) and

food pots (Absy et al. 1984; Kerr et al. 1986–1987;

Rech & Absy 2011a, 2011b) have identified the main

floral rewards collected by bees in the Amazon region.

Silveira et al. (2002) estimated that the species rich-

ness of native bees found in the Amazon rainforest

exceeds 100 and that this plays a key role in the mainte-

nance of regional ecosystems through pollination

mechanisms. Among native bees, Tetragonisca angus-

tula (Latreille, 1811) (Hymenoptera: Apidae: Melipo-

nini) is one of the most well known, and is distributed

virtually throughout Brazil (Silveira et al. 2002;

Camargo & Pedro 2012). Since the 1970s, studies have

been published on the pollen and nectar sources sought

by this species in Brazil (Iwama & Melhem 1979;

Imperatriz-Fonseca et al. 1984; Novais et al. 2006;

Morgado et al. 2011; Braga et al. 2012). However, sys-

tematic data on the floral preferences of T. angustula inthe Amazon are not available, except for two studies.

Rech and Absy (2011a) palynologically analysed two

food pots of T. angustula at the Rio Negro channel

region and Novais and Absy (2013) analysed the honey

of T. angustula from the same localities where the pres-

ent study was conducted.

The lack of knowledge on the relationship between

T. angustula and the regional Amazonian flora makes

it difficult to propose actions to maintain the native

vegetation that is significant for beekeeping. Therefore,

we conducted a palynological study of pollen samples

that were periodically collected directly from the food

pots of T. angustula in two areas of the Lower Amazonregion. The goal of this study was to evaluate the main

pollen sources by analysing the pollen spectrum and to

assess the pollen combinations that typify the pollen

analysed. The impact of this study is the additional

knowledge regarding T. angustula’s foraging activities,

and to provide the beekeeping industry in the interior

*Corresponding author. Email: [email protected]

2013 AASP – The Palynological Society

Palynology, 2013

Vol. 37, No. 2, 218–230, http://dx.doi.org/10.1080/01916122.2013.787127

mailto:[email protected]

http://dx.doi.org/10.1080/01916122.2013.787127

http://dx.doi.org/10.1080/01916122.2013.787127

mailto:[email protected]



of the Lower Amazon with information to develop

a strategy that alleviates the constant pressure

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



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



by ruderal and ornamental vegetation, including native

fruit trees, namely ‘muruci’ (craboo) (Byrsonima spp.,

Malpighiaceae). The meliponary of the Forest School

(Escola da Floresta) is intended for environmental edu-

cation activities and occupies an area of mostly second-

ary forest, with remnants of primary forest, in addition

to some ornamental plants.

2.2. Sample collection and laboratory processing

In Belterra, 15 pollen samples were collected between

September 2010 and January 2012 (except February

and March 2011) and in Santarem 8, samples were

obtained from October 2010 to May 2011. From each

site one sample was harvested monthly from the same

hive of Tetragonisca angustula.

A total of 23 pollen samples were collected using

sections (approximately 4 cm) of disposable plastic

straws that were pressed against what appeared to be

the most recent pollen pots of T. angustula, and a profilewas obtained for subsequent processing. After collec-

tion, the pollen was placed into plastic vials, properly

identified and refrigerated until laboratory preparation.

The following steps were used to process the pollen

samples collected from T. angustula pollen pots. These

steps are based on a previous protocol (Novais et al.

2009) for processing pollen collected by Africanised

honeybees (Apis mellifera L., 1758) with some modifica-

tions and the usual protocols for the pollen analysis of

honey (Louveaux et al. 1978; Iwama & Melhem 1979):

(1) Dry the samples in an oven at approximately

40 C for 48 hours or until weight stabilisationoccurs (Alvarado & Delgado 1985);

(2) Dissolve 2 to 5 g of stingless bee pollen in a

beaker with 5 ml of warm water and mix with

a glass rod;

(3) Add 5 ml of research grade ethanol (ETOH)

(95%) into the beaker and stir the solution.

ETOH minimises the loss of pollen grains

when removing the supernatant after centrifu-

gation, given the low specific gravity of alcohol

compared to water (Jones & Bryant 2004). If

necessary, let the solution stand for approxi-

mately 3 hours to ensure complete dissolution

of the pollen loads;(4) After homogenising the solution using a glass

rod, centrifuge (1048 g for 10 minutes) and

discard the supernatant liquid;

(5) Add 3 to 5 ml of anhydrous acetic acid to each

sample. Let the mixture stand for at least 3 hours

to promote the dehydration of the pollen residue.

Centrifuge and discard the supernatant;

(6) Add 3 to 5 ml of acetolysis mixture (Erdtman

1960) to each sample. Place the tubes in a

100C water bath for 3 minutes. Centrifuge

and discard the supernatant;

(7) Add 3 to 5 ml of distilled water to the test tube

containing the pollen residue and stir suffi-

ciently to remove the excess acetolysis mixture.

Add a few drops of ETOH to the tube and then

centrifuge it and discard the supernatant;

(8) Add 3 ml of 50% glycerine to each tube and let

stand between 1 and 24 hours. Centrifuge the

tube and discard the supernatant and leave the

test tube upside down until no more water is

left;

(9) Mount the pollen residue in glycerinated gela-

tine between a glass slide and a cover slip;

(10) Analyse the slides under a microscope, identify

the pollen types and count at least 500 pollen

grains per sample. In the pollen spectrum, the

percentages represent the frequency of each

pollen type, based on the total amount of pol-

len grains counted (at least 500) in one sample.These values show the contribution of each

pollen type to the analysed sample.

2.3. Identification, categorisation and analysis

The botanical identification of pollen types found in

the samples was based on pollen catalogues (Roubik &

Moreno 1991; Carreira et al. 1996) and comparison

with palinotheca reference samples from the Palynol-

ogy Laboratory of the National Institute of Amazon

Research (Instituto Nacional de Pesquisas da

Amazonia, INPA). We adopted the definitions of pol-

len type according to Joosten and de Klerk (2002) andde Klerk and Joosten (2007), understanding that the

concept of pollen type, as a morphological entity, may

include more than one species or taxonomic entity.

Thus, the author of a species is indicated only when

referring to a distinct plant species. However, this is

not necessary when only the pollen type is mentioned,

as in Tables 1 and 2.

We adopted the classes proposed by Jones and

Bryant (1996), rare (<10%), infrequent (10 to 20%),

frequent (21 to 50%) or very frequent (>50%), based

on the percentage of occurrence of each pollen type in

the sample set (regarding only its presence or absence

in the samples instead of its frequency). This value mayrepresent ‘long-term’ pollen and nectar resource

through the year, for example. The range of pollen

types based on the Shannon-Weaver diversity index

(H0) was calculated, and a pollen diversity index was

developed for each sample (Ludwig & Reynolds 1988).

Complementing H0, Pielou’s evenness index (J0), rang-

ing from 0 to 1, was calculated and indicated a trend

towards heterogeneity (0) or homogeneity (1) in the

bee’s use of resources in each area studied (Pielou

Palynology 221



1977). The analyses were performed using the PAST

(PAlaeontological STatistics, version 2.16) software

(Hammer et al. 2001).

3. Results

Thirty-two morphologically distinct pollen types were

found in the pollen spectrum of samples taken from

Tetragonisca angustula in Belterra. These types have

botanical affinity with 22 plant families found in the

area studied. The families with the highest number of

pollen types were Fabaceae (four types), Asteraceae

(three), Euphorbiaceae (three), Myrtaceae (three) and

Amaranthaceae (two). The remaining families (17)

were represented by only one pollen type each

(Table 1).

Analysis of the pollen samples collected from the

colonies of T. angustula in Santarem distinguished 24

pollen types from 19 families. The Fabaceae and the

Asteraceae families had the highest number of pollentypes (five and two, respectively). The remaining plant

families (17) were represented by only one pollen type

each (Table 2).

We recorded the presence of six pollen types that

are considered very frequent in the pollen samples

from Belterra, occurring in over 50% of the samples:

Alternanthera (Amaranthaceae), Borreria verticillata

(Rubiaceae, Plate 2, figure 1), Cecropia (Urticaceae,

Plate 2, figure 2), Eupatorium (Asteraceae), Schefflera

morototoni (Araliaceae, Plate 2, figure 3) and Tabebuia

(Bignoniaceae, Plate 2, figure 4). The remaining types

were frequent (seven), infrequent (11) or rare (eight) in

the samples (Table 1). Conversely, there were neithervery frequent nor rare pollen types from Santarem.

However, 15 frequent (between 21% and 50% of the

samples) and nine infrequent types were found

(Table 2).

Pollen types such as Alternanthera (Amarantha-

ceae), Borreria verticillata (Rubiaceae), Byrsonima

(Malpighiaceae), Emilia fosbergii (Asteraceae), Schef-

flera morototoni (Araliaceae), Tabebuia (Bignoniaceae)

and Tapirira guianensis (Anacardiaceae) occurred for

at least four consecutive months in the samples from

Belterra (Table 1). Borreria verticillata stood out

among these types with consecutive occurrence from

June 2011 through January 2012 (Table 1). InSantarem only Serjania (Sapindaceae) occurred for

three consecutive months, from October through

December 2010 (Table 2). Meanwhile, the remaining

pollen types occurred for one or two consecutive

months (Table 2).

In Belterra, three pollen types had a high fre-

quency (>45%) in one or more of the samples: Byrso-

nima (Malpighiaceae, 49.06% – October 2011; 82.68%

– November 2011; 55.56% – December 2011; 73.96%

– January 2012, Plate 2, figures 1, 2, 5 and 6), Cecro-

pia (Urticaceae, 82.02% – November 2010; 99.6% –

January 2011; 58% – April 2011; 97.03% – May 2011;

49.08% – August 2011; 76.78% – September 2011)

and Eriope (Lamiaceae, 74.07% – July 2011, Plate 2,

figure 6) (Table 1, Figure 2). Thus, the data suggest

that these three types were the most relevant pollen

combinations in the pollen pots of Tetragonisca

angustula from this region.

In Santarem, the highest frequencies were associ-

ated with six pollen types: Byrsonima (Malpighiaceae,

92.1% – February 2011), Cecropia (Urticaceae, 60.71%

– October 2010), Clidemia hirta (Melastomataceae,

98.31% – November 2010; 90.65% – March 2011;

74.41% – May 2011, Plate 2, figure 7), Davilla kunthii

(Dilleniaceae, 83.11% – April 2011, Plate 2, figure 8),

Myrcia (Myrtaceae, 88.27% – January 2011, Plate 2,

figure 9) and Vismia guianensis (Hypericaceae, 72.44%

– December 2010) (Table 2, Figure 2). These, therefore,

represent the pollen combinations that were mostexploited by Tetragonisca angustula in Santarem.

The data indicate that in Belterra, the pollen

types with the highest frequency have a botanical

affinity to species that typically have herbaceous

or arboreal habits (Table 1). Conversely, the pollen

pots from Santarem consisted of pollen types that are

predominantly linked to tree and shrub species

(Table 2).

In Belterra, the lowest richness of pollen types per

sample (six types on average) was found between

December and May, which corresponds to the rainy

season in most parts of the Lower Amazon (Albuquer-

que et al., 2010). On average, 11 different pollen typescomprised each sample from this area between June

and November, which is the driest period in the region

(Table 1). The small number of samples studied from

Santarem compared to Belterra prevents making con-

clusive statements for this region.

The Shannon-Weaver diversity index (H0) ranged

from 0.03 to 1.95 [1.04 s.d. 0.62 (n ¼ 15)] in the

pollen samples collected in Belterra, and from 0.10 to

1.00 [0.59 s.d. 0.34 (n ¼ 8)] in the samples from

Santarem. Complementing H0, the evenness (J0)

ranged from 0.04 to 0.79 [0.46 s.d. 0.21 (n ¼ 15)] in

Belterra, and from 0.07 to 0.46 [0.32 s.d. 0.15 (n ¼

8)] in Santarem (Tables 1 and 2, Figures 2 and 3). Atthe beginning of the study in Belterra, H0 was decreas-

ing each month from September through November

2010 (Figure 2). January 2011 had the lowest H0 of

any month, and December 2010 had the highest one

(Figure 2). In Santarem, November 2010 showed the

lowest H0, whereas the highest one was found in

December 2010 (Figure 3). J0 matched H0 for the sam-

ples in Belterra but not in Santarem. There was a

slight difference in them from January through March




T a b l e 1 . P o l l e n s p e c t r u m , f r e

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 B e l t e r r a , 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

2 0 1 2

P l a n t F a m i l y ,

P o l l e n T y p e

S e p

O c t

N o v

D e c

J a n

A p r

M a y

J u n

J u l

A u g

S e p

O c t

N o v

D e c

J a n

P . O . ( % )

C . O .

H a b i t

A c h a r i a c e a e ,

L i n d a c k e r i a

p a l u d o s a

0 , 0 0

0 , 0 0

0 , 0 0

1 6 , 2 5

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

7

R

t r e e

A m a r a n t h a c e a e ,

A l t e r n a n t h e r a

2 , 7 4

2 2 , 6 6

0 , 0 0

0 , 0 0

0 , 0 0

0 , 5 3

1 , 5 8

3 , 5 8

0 , 1 8

1 , 1 1

0 , 1 7

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

5 3

V F

h e r b /

s u b - s h r u b


A m a r a n t h u s

v i r i d i s

3 , 9 4

6 , 2 3

0 , 0 0

0 , 3 6

0 , 0 0

0 , 0 0

0 , 0 0

0 , 1 6

0 , 0 0

0 , 1 8

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 1 9

4 0

F

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 , 5 1

0 , 3 5

2 , 8 1

6 , 1 4

0 , 0 0

0 , 0 0

0 , 0 0

1 , 3 0

0 , 0 0

0 , 0 0

1 , 8 2

1 6 , 7 4

0 , 0 0

0 , 0 0

0 , 0 0

4 7

F

t r e e

A r a l i a c e a e ,

S c h e f fl e r a

m o r o t o t o n i

3 7 , 1 6

4 1 , 8 7

0 , 0 0

2 , 5 3

0 , 0 0

0 , 0 0

0 , 0 0

0 , 4 9

0 , 0 0

0 , 0 0

0 , 0 0

6 , 2 0

0 , 9 8

1 8 , 9 5

2 , 2 6

5 3

V F

t r e e

A r e c a c e a e ,

A s t r o c a r y u m

a c u l e a t u m

0 , 0 0

0 , 1 7

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 1 7

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

2 , 0 5

1 , 3 8

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

1 , 4 6

1 , 5 9

0 , 1 8

0 , 1 7

0 , 1 4

0 , 0 0

0 , 0 0

0 , 0 0

4 7

F

h e r b


E u p a t o r i u m

2 , 5 7

2 , 2 5

0 , 0 0

2 , 5 3

0 , 0 0

0 , 3 5

0 , 0 0

1 , 7 9

0 , 8 8

1 , 4 8

0 , 0 0

0 , 2 9

0 , 4 9

0 , 3 3

0 , 0 0

6 7

V F

h e r b / s u b -

s h r u b


V e r n o n i a

0 , 3 4

0 , 1 7

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

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

B i g n o n i a c e a e ,

T a b e b u i a

1 3 , 1 8

4 , 5 0

0 , 1 9

5 , 0 5

0 , 0 0

0 , 8 8

0 , 0 0

2 3 , 9 0

0 , 0 0

2 0 , 8 5

0 , 6 6

0 , 1 4

0 , 0 0

0 , 0 0

0 , 0 0

6 0

V F

t r e e

B u r s e r a c e a e ,

P r o t i u m

0 , 0 0

0 , 0 0

5 , 9 9

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

7

R

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

0 , 0 0

0 , 3 3

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

7

R

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

0 , 0 0

0 , 4 0

3 7 , 7 9

1 , 3 9

0 , 0 0

0 , 1 8

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

2 7

F

h e r b / s u b -

s h r u b


A p a r i s t h m i u m

c o r d a t u m

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

2 , 0 2

0 , 0 0

0 , 0 0

0 , 0 0

7

R

t r e e


C r o t o n

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 3 3

0 , 1 6

0 , 3 8

2 0

I

s h r u b / t r e e

F a b a c e a e ,

S e n n a / C a s s i a

0 , 0 0

1 , 5 6

0 , 1 9

1 , 4 4

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

2 0

I

t r e e

F a b a c e a e ,

M i m o s a

p u d i c a

3 , 4 2

1 , 0 4

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

1 3

I

h e r b

( c o n t i n u e d )

Palynology 223



T a b l e 1 . ( C o n t i n u e d ) .

2 0 1 0

2 0 1 1

2 0 1 2


P o l l e n T y p e

S e p

O c t

N o v

D e c

J a n

A p r

M a y

J u n

J u l

A u g

S e p

O c t

N o v

D e c

J a n

P . O . ( % )

C . O .

H a b i t

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

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 6 6

1 , 0 1

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 ,

P h a s e o l u s

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 2 9

0 , 0 0

0 , 0 0

0 , 5 7

1 3

I

h e r b

G o u p i a c e a e ,

G o u p i a g l a b r a

2 , 2 3

3 , 2 9

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

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

L a m i a c e a e , E r i o p e

3 , 4 2

0 , 5 2

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

6 , 6 7

7 4 , 0 7

0 , 5 5

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

3 3

F

h e r b

L o r a n t h a c e a e ,

P s i t t a c a n t h u s

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 1 4

0 , 0 0

0 , 0 0

0 , 0 0

7

R

h e m i p a r a s i t 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

0 , 0 0

0 , 0 0

0 , 0 0

3 3 , 5 0

0 , 0 0

2 5 , 4 6

1 9 , 0 7

4 9 , 0 6

8 2 , 6 8

5 5 , 5 6

7 3 , 9 6

4 7

F

s h r u b / 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 i a h i r t a

0 , 0 0

0 , 0 0

0 , 0 0

0 , 1 8

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

7

R

s h r u b

M o r a c e a e ,

B r o s i m u m

p a r a e n s e

0 , 0 0

0 , 0 0

0 , 0 0

3 1 , 2 3

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

7

R

t r e e

M y r t a c e a e ,

E u g e n i a

s t i p i t a t a

0 , 0 0

0 , 0 0

8 , 4 3

5 , 0 5

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

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

M y r t a c e a e ,

M y r c i a

0 , 3 4

0 , 0 0

0 , 3 7

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

1 3

I

s h r u b

M y r t a c e a e ,

P s i d i u m

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

1 , 4 4

0 , 0 0

0 , 0 0

0 , 0 0

7

R

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 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

1 , 7 9

8 , 8 2

0 , 3 7

0 , 0 0

0 , 0 0

0 , 1 6

0 , 1 6

0 , 0 0

3 3

F

h e r b

R u b i a c e a e ,

B o r r e r i a

v e r t i c i l l a t a

2 5 , 6 8

1 4 , 0 1

0 , 0 0

9 , 0 3

0 , 0 0

2 , 2 8

0 , 0 0

1 7 , 5 6

1 4 , 2 9

0 , 3 7

0 , 5 0

1 , 4 4

1 5 , 3 6

2 4 , 8 4

2 2 , 6 4

8 0

V F

h e r b / s u b -

s h r u b

S a p o t a c e a e ,

P o u t e r i a

0 , 6 8

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 3 7

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

1 3

I

t r e e

U r t i c a c e a e ,

C e c r o p i a

1 , 2 0

0 , 0 0

8 2 , 0 2

2 0 , 2 2

9 9 , 6 0

5 8 , 0 0

9 7 , 0 3

7 , 4 8

0 , 0 0

4 9 , 0 8

7 6 , 7 8

2 1 , 0 7

0 , 0 0

0 , 0 0

0 , 0 0

6 7

V F

t r e e

U n d e t e r m i n e d

0 , 5 1

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 1 8

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

–

–

–

T O T A L

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

–

–

–

T o t a l n u m b e r o f

p o l l e n t y p e s

i d e n t i fi e d

1 5

1 4

7

1 2

2

6

3

1 3

7

1 1

9

1 3

6

6

6

–

–

–

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 )

1 , 8 8

1 , 7 3

0 , 6 8

1 , 9 5

0 , 0 3

0 , 8 7

0 , 1 5

1 , 8 3

0 , 8 4

1 , 2 5

0 , 7 2

1 , 4 6

0 , 5 5

1 , 0 3

0 , 7 1

–

–

–

P i e l o u ’ s e v e n n e s s

i n d e x ( J 0

)

0 , 6 8

0 , 6 5

0 , 3 5

0 , 7 9

0 , 0 4

0 , 4 5

0 , 1 4

0 , 7 1

0 , 4 3

0 , 5 2

0 , 3 3

0 , 5 7

0 , 3 0

0 , 5 7

0 , 3 9

–

–

–




T a b l e 2 . P o l l e n s p e c t r u m , f r e

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 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 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


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


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


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



2011, showing an opposite trend in H0 and J0 values

(Figure 3).

4. Discussion

The number of pollen types recorded in our study

exceeds that found by Rech and Absy (2011a) in the

pollen pots of Tetragonisca angustula from the Upper

Rio Negro region of the Amazon Basin. The richness

of plant species shown by the pollen spectrum of a

given bee species varies according to several factors,

including the phenological aspects of the local flora,

the seasonal changes in nectar flow, the presence of sev-

eral species of bees foraging in the same area and the

protein needs of the colony (Imperatriz-Fonseca et al.

1984; Marques-Souza 2010). In both Belterra and in

Santarem, colonies of T. angustula share the apiary

area with other stingless bees, possibly sharing some

species of the surrounding vegetation. However, we

ignored the degree of overlap in floral resource use bythe species that cohabit with T. angustula in the study

areas because this is one of the first palynological stud-

ies conducted in the region.

The Fabaceae and the Asteraceae families had

the highest number of pollen types identified in both

Belterra and Santarem. Imperatriz-Fonseca et al.

(1984) also reported these families to be the most sig-

nificant in samples of pollen stored by T. angustula in

beehives at the Institute of Biosciences at the

University of S~ao Paulo (Universidade de S~ao Paulo,

USP). Other studies have found a strong contribution

from these families in the diet of T. angustula, in addi-

tion to the Euphorbiaceae, Moraceae, Myrtaceae andRubiaceae families (Carvalho et al. 1999; Novais et al.

2006; Morgado et al. 2011; Rech & Absy 2011a).

Most pollen types in the samples occurred in fre-

quencies below 10%, which reflects, according to

Sosa-Najera et al. (1994), the dispersion rate of indi-

viduals from the colony and the degree of polylectism.

These authors also reported a few species with a fre-

quency above 10% (termed primary sources) in honey,

stored pollen and larval food extracted from colonies

of T. angustula in Chiapas, Mexico.

However, Imperatriz-Fonseca et al. (1984), citing

Heinrich (1976), stress that although some plant spe-

cies are prominent in the pollen spectrum in terms of their high frequencies, bees tend to continue collecting

from species that provide small amounts of food. Such

plants would become alternative sources of trophic

resources for the colony and are especially useful when

other providers of pollen and nectar are saturated by

other pollinators or are diminished. Moreover, a priori ,

those secondary sources could, over time, occupy a

central position in the food supply. Marques-Souza

(2010) also argued that although stingless bees T a b l e 2 . ( C o n t i n u e d ) .

2 0 1 0

2 0 1 1


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

P o a c e a e , T y p e 1

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0

0

1 , 8 2

0 , 9 5

0 , 0 0

0 , 1 7

3 8

F

h e r b

R u b i a c e a e ,

W a r s z e w i c z i a

c o c c i n e a

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0

0

2 , 8 9

0 , 0 0

0 , 3 8

0 , 0 0

2 5

F

s h r u b / t r e e

S a p i n d a c e a e ,

S e r j a n i a

0 , 7 1

0 , 3 7

0 , 7 9

0 , 0

0

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0 0

3 8

F

l i a n a

S a p o t a c e a e ,

P o u t e r i a

0 , 0 0

0 , 0 0

0 , 0 0

0 , 0

0

0 , 1 5

0 , 0 0

0 , 0 0

1 , 5 1

2 5

F

t r e e

U r t i c a c e a e ,

C e c r o p i a

6 0 , 7 1

0 , 0 0

1 , 3 8

0 , 0

0

0 , 4 6

7 , 8 2

0 , 0 0

0 , 0 0

5 0

F

t r e e

U n d e t e r m i n e d

1 , 9 6

0 , 0 0

1 , 7 7

0 , 0

0

0 , 4 6

0 , 0 0

1 1 , 7

6

0 , 0 0

–

–

–

T O T A L

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

1 0 0 , 0

–

–

–

T o t a l n u m b e r

o f p o l l e n

t y p e s i d e n t i fi e d

6

4

8

3

7

6

5

8

–

–

–

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 , 9 3

0 , 1 0

1 , 0 0

0 , 3

7

0 , 4 0

0 , 3 7

0 , 6 1

0 , 9 5

–

–

–

P i e l o u ’ s

e v e n n e s s

i n d e x ( J ’ )

0 , 4 8

0 , 0 7

0 , 4 6

0 , 3

4

0 , 1 9

0 , 2 1

0 , 3 4

0 , 4 6

–

–

–




tend to use a potential food source to the fullest

upon its discovery, these insects continue collecting

from less-rewarding sources. However, the bees

can develop the skills required to best use new

food sources, including the manipulation of floral

parts.

Byrsonima, Cecropia, Clidemia hirta, Davilla kun-

thii , Eriope, Myrcia and Vismia guianensis were the

most significant pollen types, as their frequency was

above 70% in some samples. Rech and Absy ( 2011a)

recorded the occurrence of ‘temporary specialisation’

events in 19 of 51 pollen pots of Amazonian stingless

Plate 2. Photomicrographs of some pollen types found in stingless bee pollen samples from Belterra and Santarem, LowerAmazon region, Para State, Brazil. Bars ¼ 10 mm. Figure 1. Bv, Borreria verticillata (Rubiaceae); By, Byrsonima (Malpighiaceae).Figure 2. By, Byrsonima (Malpighiaceae); Ce, Cecropia (Urticaceae). Figure 3. Schefflera morototoni (Araliaceae). Figure 4.

Mi , Microtea (Phytolaccaceae); Ta, Tabebuia (Bignoniaceae). Figure 5. Byrsonima (Malpighiaceae). Figure 6. Byrsonima(Malpighiaceae); By, Er: Eriope (Lamiaceae). Figure 7. Clidemia hirta (Melastomataceae). Figure 8. Davilla kunthii (Dilleniaceae). Figure 9. Myrcia (Myrtaceae).

Palynology 227



bees. They identified such an event as when a given

pollen type had an occurrence above 90% of the total

pollen grains counted. Based on this, we can infer

from our data that temporary specialisation occurred

in five samples, which included the following pollen

types: Byrsonima (February 2011, in Santarem),

Cecropia (January and May 2011, in Belterra) and

Clidemia hirta (October 2010 and March 2011, in

Santarem).

However, it is worth noting three aspects regarding

our recording of temporary specialisation in the pollen

collections of Tetragonisca angustula. Species of Byrso-

nima, as found in most genera of the Malpighiaceae,

are usually pollinated by oil-collecting bees, such as

those from the Centridini group (Teixeira & Machado

2000; Rego et al. 2006). However, pollen types linked

to Byrsonima are part of the pollen spectra generated

from studies of stingless bees in the Amazon, including

the genera Cephalotrigona, Melipona, Partamona,

Scaptotrigona, Scaura and Trigona (Absy et al. 1980,1984; Marques-Souza et al. 2007; Oliveira et al. 2009;

Rech & Absy 2011a, 2011b). Cecropia mainly com-

prises anemophilous species despite being a genus

frequently cited in studies of stingless bees (Ribeiro

et al. 2002; Rech & Absy 2011a). However, while we

can infer that Tetragonisca angustula contributes negli-

gibly to the pollination of Cecropia, we emphasise the

relevance of this genus in the composition of pollen

samples in addition to its significance in providing

clues about the vegetation surrounding the colonies

because its presence is indicative of degraded areas and

is crucial for their recovery (Ribeiro et al. 2002).

Clidemia hirta (L.) D. Don has poricidal anthers,a characteristic shared by almost all species of

Melastomataceae (Ribeiro et al. 2002). Thus, C. hirta

depends on bees that are able to vibrate these anthers

to extrude the pollen mass, thereby enabling the trans-

port of the microgametophyte enclosed within the

microspore wall to another flower and completing the

pollination process. Therefore, small bees, including

Tetragonisca angustula, gain advantages by collecting

residual pollen from the previous work performed by

larger bees that can promote pollen extrusion from the

anthers of Malpighiaceae (Imperatriz-Fonseca et al.

1984). Therefore, we conclude that the events of tempo-

rary specialisation noted in the foraging pattern of T.angustula in Belterra and Santarem appear to have no

direct link with the effective pollination of the plant spe-

cies involved, which preferably rely on other agents to

ensure such processes.

Another finding is that the pollen grains of Byrso-

nima, Cecropia and Clidemia are small or very small

(< 25 mm), which favours their detection in the paly-

nological analyses of honey and pollen (Demianowicz

1964). This factor should be considered when

estimating the actual contribution of different species

with pollen grains of markedly different sizes (Silveira

1991; Marques-Souza et al. 2002).

In general, the greater the trophic niche amplitude

is, represented here by the Shannon-Weaver diversity

index (H0), the higher the uniformity or trend of homo-

geneity (J0 ¼ 1) in the bee’s pattern of floral resource

collection, which is inferred by Pielou’s evenness index

(J0). In both Belterra and in Santarem, Tetragonisca

angustula showed low uniformity in their collection. In

their study in Piracicaba, S~ao Paulo, Brazil, Carvalho

et al. (1999) found that a colony of T. angustula

showed the lowest uniformity when compared to colo-

nies of three other species of stingless bees [Nannotri-

gona testaceicornis (Lepeletier, 1836), Partamona

helleri (Friese, 1900) and Plebeia droryana (Friese,

1900)] and Apis mellifera from the same area. These

authors also noted that Tetragonisca angustula showed

the smallest niche amplitude, similar to Nannotrigona

testaceicornis, and the lowest percentage of pollensources (25%) found above 1% in the pollen spectrum.

Morgado et al. (2011) also recorded low diversity of

pollen types (0.23 H0 0.85) while analysing the pol-

len loads of Tetragonisca angustula classified by colour-

ation, which were collected in an area of the Atlantic

Forest (Mata Atlantica) in Rio de Janeiro, Brazil.

According to Oliveira et al. (2009), pollen spectra pres-

ent higher diversity in sites covered by secondary and

primary forests than in areas with gardens and reduced

primary forests. Conversely, the opposite was observed

here. Belterra presented the highest averages for H0

and J0, although beehives were placed near gardens.

However, pollen types related to native species, such asAstrocaryum aculeatum G. Mey. and Goupia glabra

Aubl., were also registered in the samples and contrib-

uted to increasing the local trophic niche of Tetrago-

nisca angustula.

Imperatriz-Fonseca et al. (1984) argued that the

small size of T. angustula implies a relatively low energy

requirement. This may be responsible for attracting T.

angustula to a higher number of plants, and these

species would also be relevant as a food source if there

are competitors in their foraging area.

We emphasise the need for future studies investi-

gating the coexistence of T. angustula with other

native species of stingless bees in the study areasbecause several species occur together in this region.

In Belterra, for example, the meliponary houses

approximately 15 different species of stingless bees, in

some cases with more than one colony per species.

Therefore, we can hypothesise possible intra- and

interspecific pressure on the bees for food resources in

this area, given the increasing suppression of native

vegetation resulting from the expansion of urban

areas.




5. Conclusions

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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