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Influence of Abiotic Factors and Floral Resource Availability on Daily Foraging

Activity of Bees: Influence of Abiotic and Biotic Factors on Bees

Article in Journal of Insect Behavior · September 2014

DOI: 10.1007/s10905-014-9452-6

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Influence of Abiotic Factors and Floral
Resource Availability on Daily Foraging
Activity of Bees

Leandro P. Polatto, José Chaud-Netto &

Valter V. Alves-Junior

Journal of Insect Behavior

ISSN 0892-7553
Volume 27
Number 5

J Insect Behav (2014) 27:593-612

DOI 10.1007/s10905-014-9452-6

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 Author's personal copy
J Insect Behav (2014) 27:593–612
DOI 10.1007/s10905-014-9452-6

Influence of Abiotic Factors and Floral Resource

Availability on Daily Foraging Activity of Bees
Influence of Abiotic and Biotic Factors on Bees

Leandro P. Polatto & José Chaud-Netto &

Valter V. Alves-Junior

Revised: 7 April 2014 / Accepted: 28 April 2014 /

Published online: 8 May 2014
# Springer Science+Business Media New York 2014

Abstract In this study, the daily and seasonal influences of abiotic factors and the amount
of floral resources on the foraging frequency of bees were determined. The experiments
were performed, during 12 consecutive months, in the main floral sources used by bees in
a secondary forest fragment. The foraging frequency of each bee species on flowers of
each plant was recorded for 20-min periods, every hour. To verify whether the foraging
activity is influenced by abiotic factors, Pearson’s correlation analysis and linear regres-
sion tests were performed for the dominant bee species. Temperature and luminosity were
the two main abiotic factors regulating foraging activities of bees. A positive correlation
was found between the foraging frequency of most bees and these two variables.
Conversely, the foraging activity was influenced neither by the relative humidity nor by
the wind speed. The activity of each species depends on a combination of factors that
include not only abiotic variables, but also the amount of floral resources available during
the day, body size, and behavior of each visitor. After a certain period of the day, the
scarcity of floral resources produced by most plants can stimulate the bees to forage in the
flowers early in subsequent days, which may occur before the period in which the abiotic
conditions are really favorable.

Keywords Apis mellifera . Climate conditions . Floral resources . Foraging . Gathering of

resources

L. P. Polatto (*) : J. Chaud-Netto

Departamento de Biologia do Instituto de Biociências de Rio Claro, Universidade Estadual Paulista
(Unesp), Rio Claro, São Paulo, Brazil
e-mail: lppolatto@gmail.com

V. V. Alves-Junior
Faculdade de Ciências Biológicas e Ambientais, Universidade Federal da Grande Dourados (UFGD),
Dourados, Mato Grosso do Sul, Brazil

Present Address:
L. P. Polatto : J. Chaud-Netto : V. V. Alves-Junior
Universidade Estadual de Mato Grosso do Sul (UEMS), Unidade Universitária de Ivinhema, Ivinhema,
Mato Grosso do Sul, Brazil
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594 J Insect Behav (2014) 27:593–612

Introduction

Since they live in a dynamic environment, bees need to adjust to numerous changes in
biotic and abiotic components. Eusocial bees can adjust to the collection of food
resources in response to variations in the colony condition (Fewell and Winston
1992, 1996; Biesmeijer et al. 1999; Hofstede and Sommeijer 2006), to the quantity
and quality of the food available in the field (Seeley 1995; Biesmeijer et al. 1999;
Hofstede and Sommeijer 2006; Grüter and Farina 2007), and to climatic conditions
(Antonini et al. 2005; Polatto et al. 2007, 2012). Intrinsic factors (memory and response
threshold) also determine the decision of the collectors of each bee species whether to
carry out the foraging flight or not (Biesmeijer and Vries 2001).
The main abiotic factors that affect the flight of bees are temperature, light intensity,
relative air humidity, and wind speed (Kleinert-Giovannini 1982; Sommeijer et al.
1983; Corbet et al. 1993; Hilário et al. 2000; Vicens and Bosch 2000; Kleinert et al.
2009). Extreme temperatures, either too hot or too cold, restrict flight activity (Hilário
et al. 2000). Flying hymenopterans dehydrate or their body temperature increases to
near lethal levels when the relative humidity is too low or under conditions of very high
temperature, respectively (Coelho and Ross 1996; Kasper et al. 2008). Light intensity
acts especially on helping visual navigation of bees, from orientation to the search of
floral resources (Hilário et al. 2000). At low ambient temperatures, the light intensity is
also important for maintaining the body heat of the bees (Kovac et al. 2009; Kovac and
Stabentheiner 2011; Hartfelder et al. 2013). Very strong winds affect the flight activity
of bees, preventing them from foraging under such conditions (Sommeijer et al. 1983).
In turn, the combined effect of environmental factors determines the insects’ operative
temperature (Kovac et al. 2010; Hartfelder et al. 2013) which is achieved from the
transfer of heat by conduction, convection and radiation between the body of the insect
and the environment (Dzialowski 2005). In an environmental temperature of 15.1 °C
and solar radiation of 684 W m−2 Kovac et al. (2010) recorded a mean thoracic
temperature of 24.4 °C in two dead honeybee workers.
Each bee species depends on specific climatic conditions, which set the boundaries
for the foraging flight (Corbet et al. 1993; Kleinert et al. 2009). Thermoregulation is
well developed, particularly in the larger species of bees, in which there is an adjust-
ment of body temperature even under a wide range of environmental conditions (Stone
and Willmer 1989b; Heinrich and Esch 1994). So, the bees with larger body size
perform foraging activities with some independence from the environmental tempera-
ture (Heinrich and Heinrich 1983; Bishop and Armbruster 1999). This peculiarity is an
advantage over the smaller species of bees (Kleinert et al. 2009). Studies carried out
with bees of the genus Bombus (Heinrich 1972, 1974; Nieh et al. 2006; Mapalad et al.
2008) and Apis mellifera L. (Heinrich 1979a; Cooper et al. 1985; Coelho 1991; Kovac
and Schmaranzer 1996; Roberts and Harrison 1999; Schmaranzer 2000; Woods-Jr et al.
2005; Kovac et al. 2010; Kovac and Stabentheiner 2011) revealed that the temperature
of their thorax (the region in which the wing muscles are located) is higher compared to
the environmental temperature. This physiological condition may represent a typical
feature of bees with large body size (Coelho 1991). Researches involving other flying
insects showed that thermoregulation is not an exclusive feature of bees and confirmed
the existence of a positive correlation between the ability of thermoregulation and body
size (Bartholomew and Heinrich 1973, Bartholomew and Heinrich 1978; Heinrich
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J Insect Behav (2014) 27:593–612 595

1984; Kovac et al. 2009). However, in insects capable of increasing their thoracic
temperature, the body temperature does not remain high during the all time (Stone and
Willmer 1989a). The thorax temperature increases through vibrations of the wing
muscles before the flights for gathering of food are initiated, and is kept high during
the flight as a byproduct of muscle activity of flight (Dudley 2000). Smaller bees have a
limited capacity for thermoregulation of the thoracic region, so they generally start
foraging later in relation to the largest bees, on days when the environmental conditions
are unfavorable or when inhabiting regions of temperate climate (Stone 1993; Stone
and Willmer 1989b; Bishop and Armbruster 1999). Thermoregulation may also be
helpful to prevent overheating. Some researches with bees showed that evaporation of
water through the mouth becomes necessary when the environmental temperature is
very high, despite the high rate of water loss by evaporation to maintain body
temperature (Heinrich 1979b, 1980; Cooper et al. 1985, Roberts and Harrison 1998).
When the environmental temperature is above 38 °C there is a reduction in the
gathering of pollen, the proportion of flights to collect nectar and/or water increases,
and the regurgitation of liquids helps to cool the body (Cooper et al. 1985).
Ramalho et al. (1998) stated that the within-nest worker size variation in stingless
bee species establishes an important relation between a minimum number of collectors
and the foraging efficiency at colony level. Those authors observed an allometric
variation of the corbiculae in workers of Melipona quadrifasciata L., a stingless bee
species. According to them, there is a reduction in the efficiency of pollen transfer with
increasing body size of workers. In ecological communities, censuses of bees in the
flowers and the comparative analysis of pollen sampled in their nests indicated that the
larger species of Melipona would avoid overlapping and antagonistic interactions with
stingless bees of small size, in the use of floral resources whose supply is being
depressed by the exploitation undertaken by many species (Nuñez 2000). On the other
hand, the workers of the smaller species, such as Tetragonisca, Plebeia and Friesella
with greater capacity to transport pollen (Ramalho et al. 1994) could continue exploring
floral sources in process of local depression of pollen, because they obtain profitable
rates of return with lower levels of offer (Kleinert et al. 2009).
According to Kleinert et al. (2009), in an evolutionary overview, species with very
small workers may be able to invest more energy and time to produce offspring because
they get higher returns from biomass by pollen foraging effort per bee. Therefore, it
would be expected to find, more often, very small bee species that could take advantage
of the opportunities for reproduction, quickly and with more flexibility, such as
fluctuations in the availability of nest sites and/or profitable floral resources.
The amount of floral resources available throughout the day is another factor that
regulates the activity of foraging by bees. Fidalgo and Kleinert (2007) mentioned that
in several studies the maximum peaks of foraging by eusocial bees were recorded in the
morning. The maximum peak of pollen collection often occurs before the peak of
nectar gathering (Roubik 1989). Unlike nectar, pollen is a limited resource and it is not
replaced from the moment of anther dehiscence. On the other hand, even though there
is nectar and oil secretion throughout anthesis, in melittophilous flowers, throughout
the day the stock of resources is exhausted and this ultimately reduces the ability of the
plant to attract bees, as time passes (Roubik 1989).
Although many studies have been developed to try to understand the models of
floral foraging by bees, patterns of foraging change according to the landscape and
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climate acting on the bee community. Thus, the main objective of this study was to
evaluate the daily and seasonal influence of abiotic factors and the amount of floral
resources on the foraging activity by bees. The goals of this research were: 1. To
determine what are the main climatic factors that shape the foraging activity of bees; 2.
To infer whether the amount of floral resources available throughout the day influences
the foraging activity of bees; 3. To evaluate whether the collection of floral resources
throughout the year oscillates due to changes in environmental conditions.

Material and Methods

Study Area and Selected Plant Species

The research was conducted in a secondary forest fragment of approximately 355-ha

(22°15′ S, 53°48′ W) located in the state of Mato Grosso do Sul, in the Midwest region
of Brazil. The forest fragment presents some patches with the physiognomy of Cerrado
(Brazilian savannah) and others of Atlantic Forest.
According to the classification of Zavattini (1992), the region presents a subtropical
climate, ranging from humid to sub-humid. The climatological normals (the averages
for the period from 1973 to 1990) for the region indicate an average annual rainfall of
1,612.5 mm, annual relative humidity of about 80.5 % and an average temperature of
22 °C, with a minimum of 17.6 °C and maximum of 29.2 °C (Instituto Nacional de
Meteorologia 2011).
For 12 consecutive months (July 2010 to June 2011), the major floral sources used
by the bees were selected, i.e., the plant species that occupied large areas of the
fragment and presented abundant flowering, besides being susceptible to foraging by
the community of bees. Parts of the structure of the plant species selected were mounted
as exsiccates and incorporated into the collection of Herbarium of the University
Campus of Rio Claro, São Paulo State University-UNESP.

Sampling of the Activity of Floral Visitors

Bees were observed at three plants of each species during the period in which the flowering
synchrony among individuals of the population was high (76 % to 100 % of flowering
plants), according to Morellato et al. (1990). For each plant, a 1 m2 area close to the ground
and with flowering branches (focal area) was selected; the number of foraging trips was
recorded during 20-min intervals for every hour, from 6:00 a.m. to 5:20 p.m. Each foraging
trip was defined by the presence of a bee in the focal area sampled, regardless of the number
of flowers visited before it left the site. Data concerning temperature, relative humidity,
light, and wind speed were recorded at the beginning of each hour.
During the observation of the bees, a distance from 0.5 to 3 m from the focal areas
chosen was kept, which was considered adequate for the morphospecific identification
of each individual; the observer stood still, thus avoiding any kind of disturbance in the
activity of the foragers. For each plant species, one to four individuals of each bee
species were caught, with the aid of an insect net. The specimens collected were
sacrificed in a chamber containing ethyl acetate and then stored in 30 mL flasks,
labeled with the code of the floral visitor, time of collection, and the plant visited.
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Later they were placed in boxes suitable for entomological collections and sent to Dra.
Silvia Regina de Menezes Pedro for identification. The bees identified were deposited
into Camargo’s Collection/USP-Ribeirão Preto, Brazil.
The strategy of recording the activity of bees through visual observations, adopted in
this study, has both positive and negative biases, as reported by Polatto and Alves-Jr
(2008) and by Cane (2001), respectively. The reasons for not using the flower scanning
method, with an insect net (Sakagami et al. 1967), adopted in most of the studies, are as
follows: 1. Reduction in the number of foraging trips throughout the day, as visitors are
collected (no possibility of recording subsequent foraging trips performed by the same
individual); 2. Quantitative subsampling of some species, especially those that are more
agile and manage to escape the throw of the insect net; 3. Intimidation of visiting species to
different degrees, due to the movement of the insect net; 4. Reduction in floral attractive-
ness throughout the day, caused by the fall of many flowers during the throw of the net.

Ecological Parameters and Statistical Analysis

In order to describe the composition and structure of the bee community in the forest
fragment studied, calculations of abundance and feeding habit were made.
The faunistic analysis of abundance was performed using the data concerning the
number of foraging trips by each visiting species (Silveira-Neto et al. 1976); the
confidence interval (CI) for the mean obtained was determined at 95 % and 99 %
probability (Kaps and Lamberson 2004). The following abundance classes were then
defined: Very Abundant = when the number of foraging trips by the same species was
higher than the upper limit of the 99 % CI; Abundant = when the number of foraging
trips recorded was between the upper limits of the CI at 95 % and 99 %; Common =
when the number of foraging trips was within the 95 % CI; Dispersed = when the
number of foraging trips remained between the lower limits of the CI at 95 % and 99 %;
Rare = in cases in which the number of foraging trips was smaller than the lower limit
of the CI at 99 %. The bee A. mellifera was excluded from the calculation of abundance
because it is an exotic species widely distributed in the study area. The species regarded
as predominant were those grouped within the class Very Abundant.
Feeding habit of the species of bees was defined in four classes, according to
Michener (2007): Polylectic = species of bees that collected floral resources from
various unrelated kinds of plants (extreme generalists); Broadly oligolectic = species
of bees that collected floral resources from a number of plant species of the superficially
similar families (generalists); Oligolectic = species of bees that specialized on a partic-
ular floral resource taxon, usually in a single plant family (specialists); Monolectic =
species of bees that collected floral resources from a single species (extreme specialists).
In order to verify whether the foraging activities of the predominant bees were
correlated with abiotic factors, Pearson correlation (r) and linear regression (r2) tests
were performed using significance levels of 5 %. The purpose of the correlation analysis
is to determine the functional dependence of each variable represented in the ordinate
axis (in this particular case, the foraging activity of each predominant bee species) upon
each independent variable represented in the abscissa axis (in this case, each of the
abiotic factors considered) (Kaps and Lamberson 2004). If the association between the
foraging activity of bees and any of the abiotic variables is significant, then the use of a
linear regression equation is recommended to explain the change in the foraging activity
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598 J Insect Behav (2014) 27:593–612

as a function of the abiotic factor, which will probably provide a useful model for
understanding the data obtained (Kaps and Lamberson 2004).
In the experimental design, it was first evaluated which abiotic factors were closely
correlated, by applying the correlation test between temperature and the other abiotic
variables (relative humidity, wind speed, light intensity, and time of foraging activities)
throughout the day, to all collections.
In a second step, the test mentioned was used to correlate the frequency of foraging
of the predominant bees with the abiotic variables throughout the day. In this case, for
each bee species, the test was applied only to the plant in which the record of foraging
trips was higher. When the result of the correlation test indicated dependence between
the foraging activity of the predominant bees and any of the variables that regulate this
activity, then a simple linear regression analysis was applied between both variables.
With regard to the multiple linear regression analysis, it was applied when the foraging
activity of any predominant bee species depended on two or more preponderantly
regulatory abiotic variables.
Concurrently, only in the case of bee species grouped within the class Polylectic, the
correlation test was applied to evaluate interactions between the frequency of foraging
trips and the abiotic variables throughout the day, in the plant of each species studied in
which the number of foraging trips was higher. The species studied were excluded from
the analyses when the number of foraging trips to the most visited plant, by each of the
species considered, was less than 10 throughout the day. The purpose of this experi-
mental design was to evaluate whether the foraging activity of a bee species depends on
abiotic conditions, equally or not, at different times of the year.
The software BioEstat 5.0 was used to determine the confidence intervals and
perform the tests of Pearson correlation and simple and multiple linear regressions
(Ayres et al. 2007).

Results

In the study area, 19 plant species were selected, belonging to the families:
Bignoniaceae (Adenocalymma bracteatum, Cuspidaria convoluta, Fridericia chica,
Fridericia florida, and Pyrostegia venusta), Malpighiaceae (Banisteriopsis cf.
campestris, Banisteriopsis laevifolia, Byrsonima intermedia, and Diplopterys
pubipetala), Asteraceae (Chromolaena maximilianii, Grazielia cf. dimorpholepis, and
Trixis antimenorrhoea), Fabaceae (Senegalia polyphylla, Senegalia sp., and Senna
obtusifolia), Sapindaceae (Matayba guianensis and Serjania caracasana), Lamiaceae
(Aegiphila integrifolia), and Rhamnaceae (Gouania cf. latifolia). The flowers of the
plant species studied were attractive from the early morning until the late afternoon of
the same day or days later, covering the entire foraging period of the bees.
A total of 4,168 foraging trips by bees were recorded in 57 days of observation in the
plant species studied, which were evenly distributed between July 2010 and June 2011.
The days of observation and recording of bees in the plants were less frequent only in
September 2010 (one day of observation) and February 2011 (two days of observation)
because the flowering synchrony between plants of the selected species was low in the
respective months. There were 42 bee species observed, but only eight species were
considered predominant, accounting for 90.95 % of the foraging trips (Table 1).
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Although the bee A. mellifera was excluded from the calculations of abundance, it was
included in the class Very Abundant because its foraging activity accounted for
73.15 % of the total. Among the predominant species, only Trigona spinipes
(Fabricius) and Lophopedia pygmaea (Schrottky) are of a small body size. Regarding
the feeding habit of the species of bees that foraged from the plants studied, 15 of them
were monolectic, 3 were included as oligolectic, 23 as broadly oligolectic, and only
A. mellifera was polylectic (Table 1).
In relation to the interrelationship between the environmental factors, temperature
was positively correlated with luminosity (r=0.507; P<0.001) and wind speed (r=
0.141; P<0.001), and negatively correlated with relative humidity (r=− 0.299;
P<0.001). There was also a positive correlation between temperature and the times
of the day (r=0.489; P<0.001).
In principle, it can be stated that the foraging activity of most of the predominant bee
species depended mainly on two abiotic factors: luminosity and temperature. For the bee
species whose foraging activity correlated significantly with luminosity [A. mellifera,
Centris varia (Erichson), and Oxaea flavescens Klug], the values obtained corresponded
to a positive association. The number of foraging trips of A. mellifera, T. spinipes, and
C. varia showed a positive correlation with temperature (Table 2).
The relative humidity and time of day apparently had little influence on the foraging
activity of the bees. The foraging of two bee species (L. pygmaea and O. flavescens)
was negatively correlated with the time of day. On the other hand, only the foraging
activity of A. mellifera was negatively correlated with relative humidity (Table 2).
The analyses of correlation between the collecting activity of bees and some abiotic
variables indicated antagonistic results to what would be expected. For instance, the
foraging of L. pygmaea correlated negatively with temperature and positively with
relative humidity. A positive correlation between the number of foraging trips of
Epicharis maculata (Smith) and O. flavescens with relative humidity was also detected.
Likewise, the absence of strong winds on the days when the collecting activities were
recorded possibly led to the detection of a positive correlation between the number of
foraging trips of four bee species (A. mellifera, T. spinipes, Centris tarsata Smith, and
C. varia) and the wind speed (Table 2).
The results obtained in the simple linear regression analysis indicate that the effect of the
two main abiotic factors (temperature and luminosity), alone, was not sufficient to explain
successfully the variation in the collecting activity of bees (Figs. 1 and 2). The frequency of
foraging trips of A. mellifera and C. varia could be determined with greater efficiency by
applying a multiple linear regression analysis because the foraging activities of both species
were dependent on temperature and luminosity. The frequency of foraging trips of
A. mellifera was adjusted as a function of temperature (x1) and luminosity (x2), using the
following equation: y=25.3162–1.0124 x1 +0.000451 x2**, r2 =0.618. The frequency of
foraging trips of C. varia could also be established as a function of temperature and
luminosity, y=2.0525–0.0507 x1 +0.000041 x2*; r2 =0.427. In summary, it can be said that
61.8 % and 42.7 % of the variations observed in the frequencies of foraging trips of
A. mellifera and C. varia, respectively, can be explained by variations in
temperature and luminosity recorded on the days of collection.
The other non-predominant bees (34 species; Table 1) exerted little pressure on the
extraction of floral resources of the plant species studied. They accounted for only
9.05 % of the foraging trips made by the community of bees in the plants observed.
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Table 1 Floral foraging trips performed by bees (Hymenoptera: Apidae) in 19 plant species located in a
secondary forest fragment in the region of Ivinhema (MS, Brazil), between July 2010 and June 2011.
Taxonomic classification based on Moure et al. (2012)

SUBFAMILY TRIBE Species Foraging Trips Classes

Number % Abundance* Feeding habit

APINAE
APINI
Apis mellifera L. 1,758 3,049 73.15 VA Polylectic
MELIPONINI
Trigona spinipes (Fabricius, 1793) 147 3.53 VA Broadly oligolectic
Tetragonisca fiebrigi (Schwarz, 1938) 11 0.26 R Broadly oligolectic
Geotrigona mombuca (Smith, 1863) 6 0.14 R Monolectic
BOMBINI
Bombus morio (Swederus, 1787) 17 0.41 C Broadly oligolectic
CENTRIDINI
Centris tarsata Smith, 1874 71 1.70 VA Broadly oligolectic
Centris analis (Fabricius, 1804) 10 0.24 R Monolectic
Centris obsoleta Lepeletier, 1841 8 0.19 R Monolectic
Centris scopipes Friese, 1899 19 0.46 C Monolectic
Centris varia (Erichson, 1848) 48 1.15 VA Broadly oligolectic
Centris nitens Lepeletier, 1841 49 1.18 VA Monolectic
Centris aenea Lepeletier, 1841 17 0.41 C Broadly oligolectic
Centris (Centris) sp. 1 3 0.07 R Monolectic
Centris (Centris) sp. 2 1 0.02 R Monolectic
Epicharis flava Friese, 1900 31 0.74 C Broadly oligolectic
Epicharis maculata (Smith, 1874) 83 1.99 VA Broadly oligolectic
EXOMALOPSINI
Exomalopsis auropilosa Spinola, 1853 21 0.50 C Broadly oligolectic
Exomalopsis fulvofasciata Smith, 1879 7 0.017 R Oligolectic
Exomalopsis tomentosa Friese, 1899 4 0.10 R Broadly oligolectic
Exomalopsis analis Spinola, 1853 8 0.19 R Broadly oligolectic
TAPINOTASPIDINI
Monoeca sp. 13 0.31 D Monolectic
Lophopedia pygmaea (Schrottky, 1902) 178 4.27 VA Oligolectic
TETRAPEDIINI
Tetrapedia diversipes Klug, 1810 17 0.41 C Broadly oligolectic
NOMADINI
Thalestria spinosa (Fabricius, 1804) 11 0.26 R Broadly oligolectic
XYLOCOPINI
Xylocopa hirsutissima Maidl, 1912 21 0.50 C Broadly oligolectic
Ceratina (Crewella) sp. 43 1.03 A Oligolectic
MEGACHILINAE
MEGACHILINI
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Table 1 (continued)

SUBFAMILY TRIBE Species Foraging Trips Classes

Number % Abundance* Feeding habit

Megachile (Dactylomegachile) sp. 6 0.14 R Broadly oligolectic

Megachile (Pseudocentron) sp. 1 0.02 R Monolectic
Coelioxys simillima Smith, 1854 1 0.02 R Monolectic
ANTHIDIINI
Anthodioctes megachiloides Holmberg, 1903 2 0.05 R Monolectic
HALICTINAE
AUGOCHORINI
Augochloropsis aurifluens (Vachal, 1903) 10 0.24 R Broadly oligolectic
Augochloropsis smithiana (Cockerell, 1900) 5 0.12 R Broadly oligolectic
Augochloropsis cupreola (Cockerell, 1900) 21 0.50 C Monolectic
Augoghlora thalia Smith, 1879 3 0.07 R Broadly oligolectic
Augochlora esox (Vachal, 1911) 16 0.38 C Broadly oligolectic
Augochlora caerulior Cockerell, 1900 2 0.05 R Monolectic
Augochlora (Augochlora) sp. 1 16 0.38 C Broadly oligolectic
Augochlora (Augochlora) sp. 2 4 0.10 R Broadly oligolectic
Thectochlora alaris (Vachal, 1904) 5 0.12 R Broadly oligolectic
Pseudaugochlora graminea (Fabricius, 1804) 14 0.34 D Monolectic
HALICTINI
Dialictus opacus (Moure, 1940) 3 0.07 R Monolectic
ANDREDINAE
OXAEINI
Oxaea flavescens Klug, 1807 166 3.98 VA Broadly oligolectic
Total 4,168 100 – –

*
VA very abundant (number of foraging trips (N) > upper limit of the CI at 99 % probability), A abundant (N
between the upper limits of the CI at 95 % and 99 % probability), C common (N within the CI at 95 %
probability), D dispersed (N between the lower limits of the CI at 95 % and 99 % probability), R rare (N <
lower limit of the CI at 99 % probability) [CI 99 %: 12.9≤μ≤44.6; CI 95 %: 15.67≤μ≤39.0]

Therefore, less attention was given to the study of these species. Approximately 73.5 %
of the non-dominant species had a medium or small body size.
At different times of the year, and for most plants studied, the foraging activity of
A. mellifera correlated positively with temperature and light intensity (Table 3).
The record of the frequency of A. mellifera in the flowers of G. dimorpholepis was
very helpful to understand the influence of the quantity of floral resources available
upon the frequency of foraging trips. The plants of this species occupied vast areas and
provided pollen and nectar in large amounts. The abundance of floral resources
available was so high that even at the end of the day one could see bees with the
whole body covered with pollen. Therefore, the floral resources were not limiting, and
hence they did not interfere with the frequency of foraging trips of the bees. It was
precisely in this plant species that the collection activity reached a peak when the
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Table 2 Relationship between abiotic variables and the frequency of foraging trips made by the predominant bees to flowers of the plants that bees had greater foraging trips

Bee Plants studied and Total number of foraging Abiotic factors – Mean value [range] and value of the Pearson correlation test
record date trips and peak activity
Time (°C) Relative humidity Luminosity Wind speed
(%) (103) (lux) (m/s)

Apis mellifera L. 1,758 Senegalia polyphylla 306 – 28.4 [25.1–29.8] 77.8 [67–90] 64.3 [13.2–93] 0.5 [0.1–1.2]
01/13/2011 12:00 r=0.016 r=0.617* r=−0.800* r=0.827** r=0.793**
Trigona spinipes (Fabricius, 1793) Serjania caracasana 86 – 20.3 [16–28] 58 [53–64] 46.3 [1.4–105] 0.5 [0–1.7]
07/24/2010 9:00 r=−0.316 r=0.623* r=−0.239 r=0.373 r=0.715**
Centris tarsata Smith, 1874 Diplopterys pubipetala 30 – 28.8 [17–37] 50 [45–58] 60.8 [0.6–115] 0.6 [0.2–1]
08/31/2010 9:00 r=−0.150 r=−0.004 r=0.073 r=0.374 r=0.589*
Centris nitens Lepeletier, 1841 Byrsonima intermedia 22 – 28.8 [20–32] 51.3 [42–59] 76.9 [4–143] 0.5 [0–1.1]
11/04/2010 14:00 r=−0.082 r=0.325 r=−0.107 r=0.392 r=0.017
Centris varia (Erichson, 1848) Byrsonima intermedia 45 – 28.8 [20–32] 51.3 [42–59] 76.9 [4–143] 0.5 [0–1.1]
11/04/2010 8:00 and 12:00 r=−0.072 r=0.572* r=−0.274 r=0.727** r=0.632*
Author's personal copy

Epicharis maculata (Smith, 1874) Banisteriopsis cf. campestris 31 – 27.7 [23.1–31.1] 74.3 [61–83] 42.5 [2–98.4] 0.4 [0–1.2]
02/04/2011 9:00 r=−0.436 r=−0.175 r=0.575* r=0.377 r=−0.187
Lophopedia pygmaea (Schrottky, 1902) Banisteriopsis cf. campestris 110 – 28.4 [22.8–32.3] 67.4 [56–80] 59.3 [12–98.2] 0.4 [0.1–0.7]
02/08/2011 7:00 r=−0.647* r=−0.583* r=0.661* r=−0.421 r=−0.141
Oxaea flavescens Klug, 1807 Fridericia chica 66 – 27.8 [22–30] 69 [64–75] 54 [12.9–133] 0.5 [0–1.6]
11/24/2010 11:00 r=−0.579* r=−0.306 r=0.569* r=0.620* r=0.263

* value significant at 5 % probability; ** value significant at 1 % probability

J Insect Behav (2014) 27:593–612
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J Insect Behav (2014) 27:593–612 603

temperature was higher (Table 4). It was also found that this intense activity occurred at
3:00 p.m., a time considered atypical.
The foraging trips performed by A. mellifera to the most visited plant of
G. dimorpholepis occurred predominantly between 10:00 a.m. and 3:00 p.m., account-
ing for 97.47 % of the total. In the time interval mentioned, the weather conditions
were: rather high temperature (≥29.9 °C), slightly lower relative humidity (≤60 %),
more intense light (≥82,200 lx), and low wind speed (≤1.5 m/s).
Although foragers of A. mellifera collect more intensely when the environmental
conditions are more favorable, this was the first species of bee which collected nectar
and/or pollen earlier in the day in eight (A. integrifolia, C. maximilianii,
G. dimorpholepis, M. guianensis, P. venusta, S. polyphylla, Senegalia sp., and
T. antimenorrhoea) of 11 species of plants that received high number of visits by that
species (Table 3). Other large-sized bee species also foraged the flowers of
A. bracteatum, B. laevifolia, B. intermedia, F. chica, S. obtusifolia and S. caracasana
before the time at which the small sized bees visited the flowers. On the other hand, any
kind of small bee visited the plants in the early hours of the day, even in the absence of
large bees.

Discussion

Several researches (e.g. Heinrich and Raven 1972; Kleinert-Giovannini 1982; Laroca
et al. 1982; Ramalho et al. 1991; Corbet et al. 1993; Morato and Campos 2000;
Antonini et al. 2005) mentioned that body features and physiological constraints on
bees can generate foraging patterns that favor flight under conditions that depend on
abiotic factors. In this case, bees generally prefer to forage in periods in which
temperature and light intensity are high, and relative humidity and wind speed are low.
The result of the test of correlation between the foraging activity of the bees and
luminosity corroborates the models of visits obtained in other studies (Szabo 1980;
Antonini et al. 2005; Kasper et al. 2008; Almeida-Soares et al. 2010; Polatto et al.
2012). On the other hand, considering the species of bees whose foraging activities
were not correlated with luminosity, T. spinipes collected almost exclusively pollen in
flowers of S. caracasana, while the other four species (C. tarsata, Centris nitens
Lepeletier, E. maculata and L. pygmaea) collected oil in flowers of plants of the family
Malpighiaceae. Pollen gradually becomes a limited resource in the course of the day
(Roubik 1989; Schuster et al. 1993). Concurrently, oil was another kind of resource
highly sought by the bees in flowers of the plant species studied (Malpighiaceae
family), which probably also became scarce throughout the day. The depletion on the
amount of pollen and oil over of the day could be encouraging these bee species to
maintain high foraging activity early in the day, even under weather conditions that
were not entirely ideal.
The positive correlation between the foraging activities of A. mellifera, T. spinipes
and C. varia with the temperature can also be considered an established pattern for
most bees (Antonini et al. 2005; Almeida-Soares et al. 2010). On the other hand, a
negative correlation between the foraging activity of L. pygmaea (a small-sized bee)
and the temperature was detected. This result probably is a consequence of the great
number of foraging trips performed by this bee in the initial period of the day.
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604 J Insect Behav (2014) 27:593–612

Apis mellifera Trigona spinipes

y = - 141.7235 + 5.8812 x*;r2 = 0.319 y = - 23.9814 + 1.5382 x*;r2 = 0.388
N. of foraging trips

Centris tarsata Centris nitens

N. of foraging trips

Epicharis maculata
Centris varia
y = - 7.0567 + 0.3759 x*;r2 = 0.259
N. of foraging trips

Lophopediapygmaea Oxaea flavescens

y = 54.2618 – 1.586 x*; r2 = 0.273
N. of foraging trips

Temperature(ºC) Temperature(ºC)
Fig. 1 Distribution of the number of foraging trips made by the predominant bees in a temperature gradient
(°C). For the species of bees that depended on temperature, a simple linear regression equation was developed
to explain the change in the frequency of foraging trips as a function of this abiotic factor. Equations
represented by * are significant at 5 % probability

B. campestris made a greater number of floral visits searching for oil early in the day.
This behavior may be associated with the limitation of the amount of this product in the
course of the day, as the flower visitors gradually collect the oil.
Therefore, although foraging activities of bees are partially regulated by abiotic
factors (Kleinert-Giovannini 1982; Corbet et al. 1993; Antonini et al. 2005; Polatto
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J Insect Behav (2014) 27:593–612 605

Apis mellifera Trigona spinipes

y = - 0.786 + 0.000409 x**; r2 = 0.683
N. of foraging trips

Centris tarsata Centris nitens

N. of foraging trips

Centris varia Epicharis maculata

y = 0.8476 + 0.000038 x**; r2 = 0.482
N. of foraging trips

Lophopedia pygmaea Oxaea flavescens

y = - 0.2651 + 0.000107 x*; r2 = 0.322
N. of foraging trips

Luminosity(x103 lux) Luminosity(x103 lux)

Fig. 2 Distribution of the number of foraging trips made by the predominant bees in a gradient of luminosity
(103) (lux). For the species that depended on luminosity, a simple linear regression equation was developed to
explain the change in the frequency of foraging trips as a function of this abiotic factor. The equation is set for
using the luminosity values in units. Equations represented by * are significant at 5 % probability, and ** are
significant at 1 % probability

et al. 2007, 2012; Almeida-Soares et al. 2010), these organisms carry out their
collection according to the net rate of resources produced by the flowers (Waser
1983). Taking into account this important relationship, even if the abiotic factors are
ideal after 12:00 a.m., bees are not encouraged to maintain a high frequency of foraging
trips after this time, due to the scarcity of floral resources. Only C. nitens showed an
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Table 3 Relationship between abiotic variables and the frequency of foraging trips made by Apis mellifera in the plant of each species studied in which the number of foraging trips
was higher (more than 10 foraging trips throughout the day)

Plants studied and Total number of foraging Environmental Factors – Mean [range] and value of the Pearson correlation test
record date trips and peak activity
Time Temperature (°C) Relative humidity (%) Luminosity Wind speed
(103) (lux) (m/s)

Serjania caracasana 101 – 25.4 [17–31] 46.9 [43–53] 47.4 [0.4–91] 1.3 [0–5.2]
07/22/2010 11:00 r=0.361 r=0.648* r=−0.706** r=0.664* r=0.362
Trixis antimenorrhoea 82 – 23.5 [14–29] 56.6 [42–51] 57.4 [0.7–105] 1.6 [0.6–2.1]
08/11/2010 12:00 r=0.238 r=0.608* r=−0.649* r=0.893** r=0.840**
Matayba guianensis 76 – 26.2 [21–28] 61.8 [58–66] 62.8 [1.8–124] 0.9 [0.2–1.8]
10/14/2010 12:00 r=−0.091 r=0.280 r=−0.011 r=0.674* r=0.388
Aegiphila integrifolia 59 – 25.3 [23–31] 71.7 [64–82] 49 [4.3–95] 0.5 [0–1.5]
12/10/2010 8:00 r=−0.594* r=0.635* r=0.753** r=−0.089 r=−0.307
Senegalia sp. 212 – 25.5 [21–29.3] 73.4 [63–83] 55.7 [4.9–110] 0.5 [0.2–0.8]
12/23/2010 10:00 and 11:00 r=−0.131 r=0.760** r=−0.344 r=0.561 r=−0.169
Fridericia florida 103 – 28.8 [26.9–31.9] 77.5 [68–86] 20.2 [6–42] 1 [0–2.8]
01/11/2011 11:00 r=−0.328 r=0.087 r=0.367 r=0.280 r=0.639*
Senegalia polyphylla 306 – 28.4 [25.1–29.8] 77.8 [67–90] 64.3 [13.2–93] 0.5 [0.1–1.2]
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01/13/2011 12:00 r=0.016 r=0.617* r=−0.800** r=0.827** r=0.793**

Gouania cf. latifolia 297 – 27.5 [22.7–30.6] 75.9 [66–89] 53.8 [8–96.6] 1.3 [0.1–1.4]
03/24/2011 11:00 r=−0.038 r=0.674* r=−0.600* r=0.733** r=0.232
Chromolaena maximilianii 239 – 26.3 [20.2–29.4] 71.5 [45–79] 70.6 [13–102.7] 0.6 [0.1–1.6]
04/06/2011 12:00 r=0.467 r=0.818** r=−0.398 r=0.725** r=0.678*
Grazielia cf. dimorpholepis 79 – 29 [23.1–33] 65.1 [53–78] 69.1 [7–106.3] 0.7 [0–1.5]
04/20/2011 15:00 r=0.361 r=0.780** r=−0.908** r=0.743** r=0.580*
Pyrostegia venusta 69 – 24.2 [18.5–28.9] 71.9 [62–82] 32.6 [0.1–72.7] 0.5 [0–1.2]
06/22/2011 10:00 r=0.202 r=0.472 r=−0.412 r=0.794** r=0.575*
J Insect Behav (2014) 27:593–612

* value significant at 5 % probability; ** value significant at 1 % probability

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activity peak in the afternoon (see Table 2). Except for C. nitens, the predominant bees
foraged preferentially in the morning both in summer and in winter. Thus, the model
established in different seasons was the same for the species of bees observed.
The values of relative humidity and wind speed were not extreme enough to be
considered as factors that influenced the foraging activity of the bees. Therefore, the
positive correlations between the foraging activity of the bees and the two variables
(relative humidity and wind speed) may be due to the effect of other variables, such as
luminosity, temperature and/or the availability of the floral resources exploited.
According to Kaps and Lamberson (2004), even if the linear equation indicates
correlation between two variables, it is not always correct to regard the association
between both as true because they may be dependent on a third variable. Thus, a
standard model for the dependence of the foraging activity of bees on relative humidity
and wind speed cannot be established.
Considering the results, it becomes difficult to develop efficient models to determine
the daily foraging activity of bees and other flying insects as a function of abiotic
factors. As observed in studies carried out by Stone (1994) and also in the present
study, the adjustments depend on a combination of factors that include not only climatic
variables, but also the amount of floral resources available as well as the physiological
state and behavior of the insects considered. Yet, it can be stated that the start of the
foraging activity of bees is specially regulated by increased light intensity, ending with
the decline in the amount of light and floral resources in the environment. The
temperature, luminosity, and amount of floral resources must have regulated the
frequency of foraging trips of the bees throughout the day.
Regarding the frequency of A. mellifera in different floral sources, the collection
activity by this bee occurred similarly throughout the year. This is strong evidence that
both in winter and in summer the abiotic variables did not reach values considered so
extreme as to limit the flight of foragers and cause changes in the foraging pattern
established for this species. Nevertheless, a common pattern of visits predominantly
regulated by luminosity and temperature was observed. As well as temperature,
brightness is also important for exogenous heat gain in bees (Kovac and
Stabentheiner 2011; Hartfelder et al. 2013). A rise of the thoracic temperature with
increased insolation was reported in workers of A. mellifera returning to the nest after
the foraging flights (Cena and Clark 1972; Heinrich 1979a; Cooper et al. 1985), and
during the gathering of nectar (Kovac and Stabentheiner 2011) and water (Kovac et al.
2010). In an air temperature below 30 °C, and under sunlight, Coelho (1991) and
Kovac et al. (2010) recorded an increase in the body temperature in workers of
A. mellifera while collecting water, with a reduction in the energy consumption that
would be used in thermoregulation, and an increase in the thoracic temperature from 1
to 3 °C. Kovac and Stabentheiner (2011) found that solar radiation is important in
raising the body temperature in workers of A. mellifera in about 4 °C, during the
collection of nectar.
Some researches reinforce the importance of the light on the flight activity of bees.
On cloudy days the flight activity of workers of Plebeia emerina (Friese) and Melipona
marginata marginata Lepeletier is lower than in sunny days, considering the same
temperatures (Kleinert-Giovannini 1982; Kleinert-Giovannini & Imperatriz-Fonseca
1986). A more intense occurrence of foraging trips by A. mellifera in the morning
finds support, again, in the possibility that there is a greater abundance of resources
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608 J Insect Behav (2014) 27:593–612

available in the flowers in this period. Although the abiotic conditions are not yet fully
ideal early in the day, A. mellifera, which has a well-developed physiological mecha-
nism for the regulation of body temperature (Heinrich 1979a; Woods-Jr et al. 2005;
Schmaranzer 2000; Kovac et al. 2010; Kovac and Stabentheiner 2011), can forage with
some independence from the abiotic variables, obtaining resources in greater abun-
dance at this time of day (Heinrich and Raven 1972). Kovac et al. (2010) found that
foragers of A. mellifera can collect water even under extreme environmental conditions.
On cold days they observed that the honeybee workers began collecting water when the
environmental temperature was 5 °C, whereas their thoracic temperature was kept to a
consistently high level (between 37 and 38.5 °C) even under an ambient temperature of
30 °C. On the other hand, on the hottest days, the activity of the bees ceased when the
environmental temperature reached 40 °C, while their thoracic temperature reached a
maximum of 45.3 °C. The foraging activity of the worker bees to collect nectar began
when the ambient temperature was close to 13 °C (Kovac and Stabentheiner 2011).
Kovac and Schmaranzer (1996) and Kovac and Stabentheiner (2011) also observed a
considerable variation in the thoracic temperature of workers of A. mellifera foraging
on flowers of different plant species.
In forager bees the regulation of energy expenditure for thermoregulation during
foragement is made by adjusting the temperature of their thorax in response to
profitability of foragement in a food supply (quantity and quality of pollen, sucrose
concentration and nectar flow), the distance between the individual flowers, the
distance between flowering plants and the hive, and the need of the colony for nectar
and/or pollen (Waddington 1990; Underwood 1991; Stabentheiner 2001; Nieh and
Sánchez 2005; Mapalad et al. 2008; Kovac and Stabentheiner 2011; Sadler and Nieh
2011).
A high thoracic temperature also allows an increase in temperature of the head and
keeps the temperature of the abdomen a few degrees above the air temperature (Kovac
and Stabentheiner 2011). As a result, they reported an improvement in the physiolog-
ical processes involved in the absorption of food, in respiration and energy supply.
These particularities possibly produce an expansion in the trophic niche of A. mellifera
and other large-sized bees, since they allow to explore the more profitable floral sources
less visited by small-sized bees, until the environmental conditions become more
favorable over the day.
Therefore, considering the arguments presented, it would be expected a higher
proportion of large-sized bee species in the forest fragment because they exploit floral
resources during a greater daily interval than the small-sized and medium-sized bees.
However, bees with small or medium body size constituted the majority of the species
recorded in the flowers of the plant species selected for the study, although they
presented low frequencies of foragement. Brizola-Bonacina et al. (2012) found a very
interesting relationship between three species of bees foraging from flowers of
Tibouchina granulosa (Melastomataceae). Earlier in the day (7:00 to 8:00 a.m.),
A. mellifera made the highest number of visits to the flowers. However, from the early
afternoon (1:00 to 2:00 p.m.) there was a reduction in the number of visits of
A. mellifera, increasing the visits of T. spinipes, a kind of bee with medium body size.
Near the end of the afternoon (4:00 to 5:00 p.m.), a period in which floral resources
were found in smaller amounts, Tetragonisca angustula (Latreille), a social bee with
small body size, was the most frequent visitor. Brizola-Bonacina et al. (2012) observed
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Table 4 Times of collection and data on abiotic conditions during the period of peak foraging trips by Apis
mellifera to each plant species studied

Plants studied Time Temperature Relative humidity Luminosity Wind speed

(°C) (%) (103) (lux) (m/s)

Serjania caracasana 11:00 26 45 74 0

Trixis antimenorrhoea 12:00 26 45 103 2.1
Matayba guianensis 12:00 27 62 121.5 1.3
Aegiphila integrifolia 8:00 27 82 39 0.5
Senegalia sp. 10:00 27.8 66 48 0.5
11:00 29.3 63 69 0.5
Fridericia florida 11:00 28.4 78 11.5 2.8
Senegalia polyphylla 12:00 29.7 75 83.7 0.7
Gouania cf. latifolia 11:00 29.8 70 95.6 0.5
Chromolaena maximilianii 12:00 28.1 73 97.9 1.6
Grazielia cf. dimorpholepis 15:00 30.1 53 82.2 1
Pyrostegia venusta 10:00 21.5 80 65.5 0.2
Mean ± standard error 27.3±0.7 66±3.7 73.9±8.8 0.6±0.2
Coefficient of variation 9% 19 % 41 % 136 %

that T. spinipes presented a very aggressive behavior against A. mellifera in flowers of

T. granulosa, and this reaction caused a drastic reduction in the number of visits of
A. mellifera between 1:00 and 2:00 p.m. Engels and Engels (1980) also observed many
aggressive interactions of stingless bees against foragers of A. mellifera, during the
exploitation of floral resources. Engel and Dingemans-Bakels (1980) noticed that small
species of stingless bees, as Plebeia minima (Gribodo), Tetragonisca spp. and Trigona
jaty Schwarz, foraged some types of flowers which were not visited by larger bees, and
suggested the existence of some alimentary specialization related with the size of the
species. Therefore, in environmental conditions, there is a partition of food resources
among bee species with different body sizes which allows the sympatric coexistence
among them.

Acknowledgments The authors are grateful to Daniela de Oliveira Dinato and Dr. Júlio Antonio Lombardi
who identified the plant species and prepared exsiccates for deposit into the Herbarium of Rio Claro, and also
to Dra. Silvia Regina de Menezes Pedro who identified the bee species.

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