ISSN 2236-4420
Semana Entomológica da Bahia (SINSECTA), 03 a 09 de dezembro de 2012
Flight activity of the eusocial bee Melipona quadrifasciata anthidioides
(Hymenoptera: Apidae, Meliponini)
Andreia Santos do Nascimento1; Luzimario Lima Pereira1; Carlos Alfredo Lopes de Carvalho1; Cerilene
Santiago Machado1; Melissa Oda-Souza1; Bruno de Almeida Souza1,2
1
Universidade Federal do Recôncavo da Bahia, Centro de Ciências Agrárias, Ambientais e Biológicas. Rua Rui Barbosa, 710.
CEP: 44380-000, Cruz das Almas-BA, Brasil. E-mail: [email protected].
2
Empresa Brasileira de Pesquisa Agropecuária - Meio-Norte, Núcleo de Pesquisa com Abelhas, Av. Duque de Caxias, 5650 /
Buenos Aires 64006-220 - Teresina, PI – Brasil. E-mail: [email protected].
Abstract: Many stingless bees are restricted to specific regions. Although they are adapted to the local climate and
flora, they are susceptible to modifications in the environment, which directly influence their flight activity. The
present study aimed at gathering information about the flight activity of the eusocial bee Melipona quadrifasciata
anthidioides, in order to contribute to the knowledge on this species. We assessed the flow of bees entering and
leaving the colony and identified the materials transported by them. We correlated this information with climatic
data collected simultaneously with the observations, which were carried out from May 2005 to July 2006.
Temperature strongly influenced the flight activity of this species, as it has a significant negative correlation with
bee flow. Humidity was positively correlated with bee flow. The effective flight activity of M. quadrifasciata
anthidioides began at 18.90 ºC and relative humidity of 82.37%. The peak activity was observed from 5:00 a.m. to
8:00 a.m., when the temperature varied between 18.90 ºC and 20.60 ºC, and humidity varied between 82.37% and
79.20%. The flight activity ended at 6:00 pm, at 26.10 ºC and humidity of 57.57%.
Key words: stingless bee, foraging, “mandaçaia” bee, meliponiculture.
Atividade de vôo da abelha eusocial Melipona quadrifasciata anthidioides
(Hymenoptera, Apidae, Meliponini)
Resumo: Muitas espécies de meliponíneos são específicas de suas regiões de ocorrência e mesmo sendo
adaptadas às condições locais de clima e flora, estão sujeitas às modificações do ambiente externo, influenciando
diretamente a sua atividade de voo. Este trabalho teve como objetivo obter informações sobre a atividade de voo
da abelha social Melipona quadrifasciata anthidioides, contribuindo para o conhecimento desta espécie. Foi
avaliado o fluxo de abelhas, entrando e saindo da colônia, e a identificação do tipo de material transportado. Estas
informações foram correlacionadas com dados climáticos coletados no momento das observações, realizadas
entre maio de 2002 e julho de 2006. A temperatura foi o fator de maior influência sobre a atividade de voo desta
espécie, apresentando correlação negativa significativa com a entrada e saída de abelhas da colônia. Contudo, a
umidade relativa do ar mostrou uma correlação positiva significativa com o movimento das abelhas. A atividade de
efetiva de voo de M. q. anthidioides foi iniciada à temperatura de 18,90ºC e umidade relativa de 82,37%,
apresentando pico de atividade entre 05:00-08:00 horas, quando a temperatura variou de 18,90 a 20,60ºC e a
umidade relativa do ar entre 82,37 e 79,20%. A atividade externa das abelhas foi encerrada às 18:00 hs, com
temperatura de 26,10ºC e umidade relativa de 57,57%.
Palavras chave: abelhas em ferrão, forrageamento, mandaçaia, meliponicultura.
Introduction
Bees are part of the ecosystem where they live, and stand out as important pollinators due to their
abundance, broad geographic distribution, and attraction to flowers (Kerr et al., 1996; Nogueira-Couto and Couto,
2000).
Social insects, such as stingless bees, respond to changes in external conditions by adjusting the colony’s
internal environment. These alterations directly influence internal and external activities, such as the construction of
cells and food pots, as well as foraging (Kerr et al., 1996; Biesmeijer et al., 1999; Hilário et al., 2001; Souza et al.,
2006).
Magistra, Cruz das Almas-BA, v. 24, número especial, p. 112-118, dez. 2012.
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Semana Entomológica da Bahia (SINSECTA), 03 a 09 de dezembro de 2012
External factors such as temperature, humidity, luminosity, and resource availability may influence the flight
activity of stingless bees (Inoue et al., 1985; Heard and Hendrikz, 1993; Azevedo, 1997; Hilário et al., 2001; 2007).
Internal factors, such as population size and the colony’s requirements, may also influence the flight activity of
stingless bees (Hilário et al., 2000; Pompeu, 2003). In addition, differences in body size, body color, and pilosity do
also influence the effect of ambient temperature and isolation on each species (Bruijn and Sommeijer, 1997).
Bee flight activity is associated with different types of behavior, such as hygiene and collection of food and
materials used to build the colony. Thus, the flow of worker bees, which enter the colony carrying nectar, pollen,
resin, and mud, and leave the colony carrying debris, can be easily observed (Roubik, 1989; Carvalho et al., 2006).
Several species of stingless bees coexist in tropical habitats, which results in considerable overlap of the
plant species used as food (Hubbell and Johnson, 1978; Roubik, 1989). The bees’ flight activity provides relevant
ecological information on their biology, such as interspecific competition, floral preferences, and plant phenology,
which can be used in species conservation and crop pollination plans (Ramalho et al., 1989; Hilário et al., 2001).
Many stingless bees are restricted to specific regions. Although they may be adapted to the local climate and flora,
they are susceptible to environmental changes, which directly influence their flight activity. The present study aimed
at gathering information about the flight activity of worker bees of the species Melipona quadrifasciata anthidioides,
in order to contribute to the knowledge on this species.
Material and Methods
The flight activity of bees was observed every two months, two times in each sampling month (15-day
interval), from May 2005 to July 2006, in the meliponary of the Insecta Research Group, Center for Agricultural,
Environmental and Biological Sciences, Universidade Federal do Recôncavo da Bahia, Cruz das Almas, state of
Bahia, northeastern Brazil.
We randomly picked two colonies of M. quadrifasciata anthidioides, which were installed in 15x15x15-cm
beehives (INPA model) composed of nest, upper nest, and comb frame.
During each observation event, we recorded the flow of workers entering and leaving the colony from 5:00
a.m. to 6:00 p.m. The number of bees in flight was recorded for a maximum time of 10 min/h/ colony or at the count
of 15 individuals/colony each 10 min, following a protocol adapted from Carvalho and Marchini (1999). We
collected data on temperature and relative humidity with a dry-bulb/wet-bulb thermometer, and a
maximum/minimum thermometer, installed at the meliponary.
We recorded information on the material transported by worker bees by direct observation. We identified
resin, mud, and pollen loads based on characteristics of these materials (resin = shiny mass; mud = irregular
granulated mass; pollen = opaque clearly-defined mass). We counted the number of bees carrying debris in their
mandibles out of the colony. Since it was not possible to identify nectar loads, we counted the bees entering the
colony without an apparent load (Souza et al., 2006).
We analyzed the data in the program R (R Development Core Team, 2005), and used Spearman
correlations with 5% and 1% significance levels.
Results and Discussion
The flight activity of M. quadrifasciata anthidioides varied among months (Figure 1). In March 2006 we
observed the highest flow of bees entering and leaving the colony, and in May 2005 and May 2006 we recorded
the lowest activity (Figure 1).
High flight activity and high development of the colonies in November, January, and March, during the local
flowering peak, suggest that colonies of M. quadrifasciata anthidioides have seasonal activity related to food
availability. Bee flow was negatively correlated with temperature (P < 0.05) and positively correlated with relative
humidity (P < 0.05) (Table 1).
o
The flight activity of M. quadrifasciata anthidioides began at dawn, at an average temperature of 18.90 C,
and it was more intense between 5:00 and 8:00 a.m. (Figure 2). The peak of bee activity occurred between 6:00
and 7:00 a.m. In this period the average temperature was 19.2 oC and the relative humidity was 81.8%.
The peak of workers entering the colony with pollen occurred between 5:00 and 6:00 a.m., whereas the peak
of workers with no apparent load occurred between 5:00 and 8:00 a.m. M. quadrifasciata anthidioides collected
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pollen during almost all day except for the period between 2:00 and 3:00 p.m. The peak in food collection occurred
in the morning, between 5:00 and 9:00 a.m.
The number of workers of M. quadrifasciata anthidioides leaving the colony with debris or carrying no
apparent load was higher between 5:00 and 8:00 a.m.
Most bees entering the nest were carrying either pollen or debris, or had no apparent load (P < 0.05).
The number of bees leaving the colony was strongly correlated with the number of bees entering the colony
with resin loads or with no apparent load (both P < 0.01). The number of bees leaving the colony was also
correlated with the numbers of bees entering the colony with pollen and bees leaving the colony with debris (P <
0.05).
Debris transportation was positively correlated with bee flow in and out of the colony, and with bees entering
the colony with pollen or with no apparent load (P < 0.05). An increase in food availability seems to stimulate the
queen to lay more eggs, resulting in higher colony growth, which directly influences the amount of debris produced.
Figure 1 - Variations in temperature and relative humidity, monthly flow of Melipona quadrifasciata anthidioides
workers, flight activity, and distribution of transported materials from May 2005 to July 2006 (WAL = bee
with no apparent load).
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Semana Entomológica da Bahia (SINSECTA), 03 a 09 de dezembro de 2012
Table 1 - Correlation coefficient (Spearman) between environmental conditions and flight activity of workers of
Melipona quadrifasciata anthidioides from May 2005 to July 2006.
RES
MUD
POL
WAL
DEB
ENT
EXT
RHD
MUD
0,33 ns
-
POL
0,47 ns
0,05 ns
-
WAL
0,32 ns
0,25 ns
0,77 **
-
DEB
0,62 *
0,25 ns
0,70 **
0,73 **
-
ENT
0,37 ns
0,21 ns
0,88 **
0,97 **
0,77 **
-
EXI
0,63 *
0,18 ns
0,69 **
0,64 *
0,72 **
0,67 **
-
RHD
0,61 *
0,20 ns
0,88 **
0,78 **
0,78 **
0,87 **
0,75 **
-
TEM
-0,61 **
-0,20 ns
-0,88 **
-0,78 **
-0,78 **
-0,87 **
-0,75 **
-0,99 **
*, **: significant at 5% and 1% probability, respectively, by Fisher’s “z” test; ns= non significant. RES= resin load; MUD= mud load; POL= pollen
load; WAL= entry of bees without apparent load; DEB= debris load; ENT= entry of bees in the colony; EXI= exit of bees from the colony; RHD=
relative air humidity; TEM= temperature in the environment.
Resin collection was positively correlated with debris transport, bees leaving the colony, relative air humidity
(P < 0.01), and ambient temperature (P < 0.05).
M. quadrifasciata anthidioides collects large amounts of mud to use for colony construction, but the collection
of mud was not correlated with temperature, humidity, or collection of other resources.
Pollen collection increased from September 2005 on, whereas the number of bees entering the colony with
no apparent load increased in July 2005.
The number of bees entering the colony with no apparent load was positively correlated with humidity (P <
0.05) and negatively correlated with temperature (P < 0.05). Pollen collection was also negatively correlated with
temperature (P < 0.05). The number of bees entering the colony with pollen was positively correlated with the
number of bees entering the colony with no apparent load (P < 0.05).
Our observations corroborated the influence of climatic factors on the flight activity of M. quadrifasciata
anthidioides; the activity decreased with an increase in temperature and with a decrease in relative air humidity.
Souza et al. (2006) obtained opposite results with M. asilvai. This stingless bee is smaller than M.
quadrifasciata anthidioides, and lives in areas with higher temperatures and lower relative humidity than our study
area, which may explain the differences found between these species.
Climatic factors influence the flight activity of stingless bees (Hilário et al., 2000; 2001). Temperature,
luminosity, and relative air humidity are among the factors that most affect the flight activity of Tetragonisca
angustula (Iwama, 1977).
o
The flight activity of M. quadrifasciata anthidioides began at dawn, at an average temperature of 18.90 C,
and reached a peak between 5:00 and 8:00 a.m. A similar pattern was observed in M. q. quadrifasciata and M.
bicolor (Teixeira and Campos, 2005), whereas the flight activity of M. scutellaris was higher between 6:00 and
10:00 a.m. (Ramalho et al., 2007).
The flight activity of M. q. quadrifasciata begins at 13°C, and reaches a peak between 14 and 16 °C
(Imperatriz-Fonseca et al., 1985). In M. bicolor bicolor, the flight activity begins between 11 and 16 °C, and reaches
a peak between 16 and 26°C (Hilário et al., 2000).
In M. scutellaris the flight activity peaks between 5:00 and 7:00 a.m. Over 60% of the flight activity in this
species is concentrated in the first four hours in the morning, and it decreases between 11:00 a.m. and 1:00 p.m.
Then, new peak occurs between 3:00 and 4:00 p.m. (Pierrot and Schlindwein, 2003).
The flight activity of M. mandacaia peaks between 7:00 and 10:00 a.m., when the temperature varies
o
between 21.20 and 23.30 C, and the humidity varies between 79.60% and 90.60%. This species shows a second
peak between 3:00 and 5:00 p.m. (Alves et al., 2005).
The influence of bee size on the beginning of the flight activity was investigated by Teixeira and Campos
(2005). They observed that larger bees, such as M. quadrifasciata and M. bicolor, begin their activity at lower
temperatures than smaller bees.
The flight activity of M. marginata obscurior is higher in spring and summer, and increases gradually between
6:00 and 11:00 a.m., reaching a peak between 9:00 and 11:00 a.m., when the relative humidity is between 81%
and 90% (Borges and Blochtein, 2005).
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Semana Entomológica da Bahia (SINSECTA), 03 a 09 de dezembro de 2012
M. quadrifasciata anthidioides shows a peak in the number of workers entering the colony with pollen that is
similar to M. marginata obscurior (Borges and Blochtein, 2005) and M. seminigra (Carvalho-Zilse et al., 2007).
Workers of stingless bee are stimulated to forage according to the availability and quality of the resources
present in the surrounding vegetation. The colony’s requirements, internal conditions (such as stored pollen,
honey, and resin), as well as the bees’ reproductive cycle, may define which resources will be needed and at which
amounts (Pierrot and Schlindwein, 2003).
Figure 2 - Variations in temperature and relative humidity, time of flow of Melipona quadrifasciata anthidioides
workers, flight activity, and distribution of transported materials, from May 2005 to July 2006. (WAL =
bee with no apparent load).
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According to Souza et al. (2006) temperature is the factor that most influences the flight ability of M. asilvai,
with a significant positive correlation between the number of bees entering the colony and carrying pollen. These
authors noticed that mud collection was positively correlated with humidity, and that the flight activity begins at 21.0
o
C and 84.5% humidity, peaking at 27.4 oC and 60.6% humidity.
Conclusion
The temperature strongly influence the flight activity of this M. quadrifasciata anthidioides. The humidity is
positively correlated with bee flow.
Acknowledgements
The authors thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Proc.
303237/2010-4) and Coordenação de Aperfeiçoamento de Pessoal de Nível (CAPES) for the financial support.
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