Open access journal: http://periodicos.uefs.br/index.php/sociobiology
ISSN: 0361-6525

DOI: 10.13102/sociobiology.v69i4.7894Sociobiology 69(4): e7894 (December, 2022)

Introduction 

Bees, wasps and ants are insects that take part in various 
ecological interactions; among them, flower-visitation. The 
visitation of flowers by hymenopterans may result in plant 
pollination, although other phenomena, such as nectar robbing 
and competition with real pollinators, may also be observed. 
(Vizentin-Bugoni et al., 2018). Bees are key pollinators, 
responsible for the pollination of several botanical species 
and the absence or population decline of these animals is 
substantially risky for crops and the native flora, because, 

Abstract  
The Hymnoptera order includes several flower-visiting insects (e.g. ants, bees, and 
wasps) and the coexistence of many different species in the same community can 
generate interspecific competition. Notwithstanding shared communities, research 
which evaluates how these taxonomic groups influence a whole community of 
flower-visiting Hymenoptera is lacking. Moreover, abiotic factors can also impact 
these floral visits, because each organism responds differently to climatic variations. 
The goal of this study is to evaluate abiotic factors, specifically relative air humidity 
and air temperature, which may be able to impact the number and the frequency of 
interactions between hymenopterans and flowers and to assess the composition and 
niche organization, by making use of interaction networks, of the entire community 
of flower-visiting Hymenoptera at the botanical garden of the Universidade Federal 
Rural do Rio de Janeiro. For the duration of a year, we took samples in that botanical 
garden, compartmentalizing the collections temporally in accordance with the time 
of the insects’ shift (morning or afternoon). We observed a positive influence of 
air temperature on the number of ant interactions and visits.  It is also possible 
to observe that most of these interaction networks exhibited a nested and non-
modular pattern and an average level of network specialization. In addition, bees 
stood out as the species with the highest frequency of visits and with the most 
generalist behavior. This study demonstrates how a botanical garden can sustain 
a diverse community of floral visiting Hymenoptera in an urban environment and 
why it consists in an important tool for biodiversity conservation.

Sociobiology
An international journal on social insects

Mariana R. Menezes¹, Bianca F.S. Laviski¹, Adriano P.L. dos Santos², Eder C.B. de França²,³, Mariane S. Moreira²
Ricardino da Conceição-Neto¹, Jarbas M. Queiroz²

Article History

Edited by
Wesley Dáttilo, Instituto de Ecología A.C., 
Mexico
Received                        28 March 2022
Initial acceptance         14 April 2022
Final acceptance           29 August 2022
Publication date           28 December 2022

Keywords 
Hymenoptera, abiotic factors, pollination, 
niche overlap. 

Corresponding author 
Mariana R. Menezes
Universidade Federal Rural do Rio de 
Janeiro, Instituto de Floresta 
Rodovia BR 465, Km 07 - Zona Rural
CEP: 23890-000 - Seropédica-RJ, Brasil. 
E-mail: mariana_romenezes@hotmail.com

since many species depend on these pollinators for sexual 
reproduction, it can lead plant species to extinction and 
affect food production (De Marco Jr. & Coelho, 2004; Klein 
et al., 2007). On the other hand, the role of wasps as plant 
pollinators may be considered unusual because certain wasps 
visit flowers to prey on other arthropods, to collect or to steal 
nectar collected by other hymenopterans or because they 
are attracted by hormones released by the plant (Torezan-
Silingardi, 2012; Nagasaki, 2021). The importance of ants 
as plant pollinators is still a matter of debate while some ant 
species can contribute to the pollination process (Gonzálvez 

1 - Programa de Pós-Graduação em Biologia Animal, ICBS, UFRRJ, Seropédica-RJ, Brazil
2 - Departamento de Ciências Ambientais, IF, UFRRJ, Seropédica-RJ, Brazil
3 - Programa de Pós-Graduação em Entomologia, UFPR, Curitiba-PR, Brazil

RESEARCH ARTICLE - SoCIAL ARTHRoPoDS

Flower Visitation by Bees, Wasps and Ants: Revealing How a Community of Flower-Visitors 
Establish Interaction Networks in a Botanical Garden

mailto:mariana_romenezes@hotmail.com


Mariana R Menezes et al. – Hymenoptera Flower-Visitors in a Botanical Garden2

et al., 2013; Wang et al., 2015), other species can chase 
away potential pollinators (Villamil et al., 2018; Nogueira 
et al., 2021). Notwithstanding shared communities, research 
which evaluates how these taxonomic groups influence the 
composition and the organization of a whole community of 
flower-visiting Hymenoptera is lacking. 

When focusing on the interactions of Hymenoptera 
and flowers, several factors can impact the amount of 
these interactions and their frequency. Some of them are 
abiotic, such as relative air humidity. In another study on a 
community of floral-visitors, Barbosa et al. (2016) observed a 
negative correlation between relative air humidity and flower 
visits by Hymenoptera, which may be related to the fact that 
nectar changes its concentration and viscosity according to 
relative air humidity (Winkler et al., 2009). Another factor 
possibly related to the hymenopteran-flower interaction is 
air temperature. Air temperature can modulate the foraging 
behavior of hymenopterans, as the energy cost of foraging 
varies in accordance with changes in air temperature (Classen 
et al., 2015; Kovac et al., 2015). In warm environments, 
Hymenopterans tend to increase their foraging and, 
consequently, their floral visitation, what can change the 
community’s characteristics (e.g. specialization, diversity, 
richness, resource supply) (Classen et al., 2015; Classen et al., 
2020; Luna et al., 2021). However, because this community 
consists of organisms biologically and behaviorally unique, 
these factors can affect each of these taxonomic groups 
differently: ants are expected to respond better to increases in 
temperature once they are more resistant to high temperatures 
than bees and wasps are (Heinrich, 1993; Kovac et al., 
2015). Therefore, assessing how abiotic factors relate to 
each taxonomic group separately may be a proper strategy 
to understand how these factors influence interactions in the 
community of flower-visitors.

When different species of flower-visitors interact 
with the same group of plants, they can be functionally 
redundant and end up increasing interspecific competition, 
which would reduce the diversity and richness of these 
visitors (Blüthgen & Klein, 2011). The co-occurence of 
many species in the same community of flower visitors can 
be facilitated by the specialization of some groups and by 
the differentiation of niches (Blüthgen & Klein, 2011; Watts 
et al., 2016). To help us to understand how this particular 
community's organization and  species composition, we can 
use a tool that has been widely employed to study insect-
plant interactions: interaction networks (e.g. Dáttilo & Rico-
Gray, 2018). Measures of specialization on the network level 
can show us the degree of niche division among species of 
floral visitors in the community studied (Blüthgen et al., 
2006). Moreover, some other network metrics can help us 
understand community organization. To assess whether a 
group of selective species interact with a set of plants visited 
by generalist floral-visitors, we can calculate the nestedness of 
networks in that community (Fortuna, 2010; Dehling, 2018). 

And to assess the tendency of a subset of species to relate 
more frequently to each other than to other species, constituting 
modules, we can calculate the modularity of the networks in that 
community (Fortuna, 2010; Dehling, 2018). We must be careful 
when treating insect-flower interactions as mutualistic networks 
because some visits have negative effects on plants (Vizentin-
Bugoni et al., 2018). What usually happens in mutualistic plant-
insect networks (e.g. flower visitors, extrafloral nectaries or seed 
removers) is that, due to the insects’ behavior, they display low 
specialization, high nestedness and no modularity (Campos-
Navarrete et al., 2013; Lange & Del-Claro, 2014; Anjos et 
al., 2018; Laviski et al., 2021). Although all hymenopteran 
networks follow the assumptions for insect-plant mutualistic 
networks, metric values are expected to be quite different 
for networks with each group of organisms, because they are 
different taxonomic groups (Campos-Navarrete et al., 2013). 
Bees, for instance, are responsible for the pollination of 
many botanical species and tend to be more generalist when 
it comes to flower visitation (De Marco Jr. & Coelho, 2004; 
Klein et al., 2007; Torezan-Silingardi, 2012). Thus, we expect 
the interaction networks which present bees to be more nested, 
less specialized and not to feature modularity (Blüthgen et al., 
2006; Fortuna, 2010; Dehling, 2018).

While specialization indicates a niche division in a 
community, identifying its generalist species is of utmost 
importance, because they are crucial to the stability and 
operation of community organization, mainly because the 
core species interact with nearly all species in the community 
(Bascompte et al., 2003; Guimarães et al., 2006; Dáttilo et 
al., 2013a).  We can evaluate the most generalist species 
in a community based on the analysis of core species in 
the network (Dáttilo et al., 2013a). As stated earlier, bees 
usually present generalist flower-visiting behavior, therefore 
they are commonly the species with the highest frequency 
of interactions in flower-visiting hymenopteran networks 
(Campos-Navarrete et al., 2013). Another factor for assessing 
similarities or differences between niches is time: observing 
the species composition and activities during a day, during a 
year or even over decades allows us to compare the species 
that interact during each interval and calculate the overlap of 
these temporal niches (Díaz-Castelazo et al., 2013; Dáttilo et 
al., 2014a). On an even smaller scale, we can evaluate how 
the temporal niche divides itself throughout the day. Some 
bees exhibit a peak behavior of flower visitation at different 
times (Tschoeke et al., 2015) and ant species can also have 
different peaks of activity in a 24-hour period (Fellers, 1989), 
as well as wasp species (Brito et al., 2020). However, there 
are no studies which consider the overlap of temporal niches 
during the day for a floral-visitor community with more than 
one hymenopteran group. 

In this work, we used samplings of floral-visitors of a 
botanical garden’s community collected over a year, both in 
the morning and in the afternoon, to understand how some 
abiotic factors correlate with the number and frequency 



Sociobiology 69(4): e7894 (December, 2022) 3

of floral visitation interactions and also to comprehend the 
organization and composition of this community by using 
floral-hymenopterans networks. Regarding the influence of 
abiotic factors on increased foraging and how these factors 
correlate with the number and frequency of floral visitations, 
we hypothesized that relative air humidity would negatively 
impact the number and frequency of floral visits, while air 
temperature would positively affect the interactions. Regarding 
the organization and composition of this community of floral-
visitors, we also hypothesized that interaction networks 
would show patterns similar to other insect-plant mutualistic 
networks: they will be nested, lack modularity and have low 
specialization. In addition, we presumed that bee species 
would be most prevalent network core species. We also expect 
communities to be different according to the daily temporal 
niche: in the morning, with a higher frequency of bees in 
interactions, we expect the networks to be more nested, less 
specialized and non-modular; in the afternoon, with a higher 
frequency of ants, we expect the networks to be less nested, 
more specialized and non-modular. 

Material and Methods

Study area

We conducted the study at the Botanical Garden of the 
Universidade Federal Rural do Rio de Janeiro (22°45’56”S; 
43°41’33”W), a 16.5 hectare area, located in Seropédica, Rio 
de Janeiro State, Brazil. The site is located in a degraded region 
of the Atlantic Forest, where some botanical species, native 
and exotic, were planted, aiming to create a living botanical 
collection; the area has also a pond, a small secondary forest 
fragment and a separate area for crops (Cysneiros et al., 2011). 
Seropédica is located 26 meters above sea level, has an annual 
precipitation of 1294 mm and an average annual temperature 
of 23.9 °C (Oliveira Jr. et al., 2014). According to Köppen 
(1948), the region’s climate is classified as ‘Aw’: tropical, 
with drier winters and rainy summers. The garden’s local 
collection includes 125 dicotyledonous species, of which 94 
are native (Cysneiros et al., 2011).

It is important to highlight that botanical gardens as 
urban parks are key instruments to preserve biodiversity in 
urban areas and maintain the community previously established 
in that area (Maruyama et al., 2019; Marín et al., 2020); also, 
they are unvaluable for scientific investigations (Chen & Sun, 
2018), such as this one.

Sampling

We did the sampling of flower-visiting hymenopterans 
from December 2018 through December 2019, twice a month, 
when the weather conditions were favorable. We collected 
from 8:30 am to 11:00 am and from 1:30 pm to 3:00 pm, in 
accordance with the method established by Sakagami (1967). 
We chose these periods because the organisms studied are 
more active in them (Silveira et al., 2002; Barbosa et al., 2016).

We surveyed sixty-nine plant species inside the Botanical 
Garden. On the day before the sampling, we monitored 
flowering plants, regardless of each one’s flowering stage. 
Then, we collected samples from the previously observed 
plants with an entomological net, tweezers and brush. From 
each plant individual, we sampled visiting Hymenoptera 
for ten minutes. In the case of ant collecting, an animal that 
recruits to dominate resources (Hölldobler & Wilson, 1990), 
we collected only one specimen per plant. At the beginning 
of each sampling period, we measured the air temperature 
and the relative air humidity at the time with a portable 
digital thermo hygrometer, THAR-300 - Instrutherm. We 
took the collected insects to the laboratory for mounting and 
subsequent identification.

We considered an interaction as every relationship 
between a flower-visiting Hymenoptera and a plant species, 
while visits are the frequency of the interactions.

Data Analysis

For each sample, we correlated the number of visits 
and interactions of bees, wasps and ants with the relative 
air humidity and air temperature at the time, separately, at 
the moment of sampling. We discarded the data relative to 
when there were no visits. Thereafter, we had 39 replicates 
for bee visits, 31 for wasp visits and 29 for ant visits. With 
the Kendall’s rank correlation coefficient, we assessed the 
influence of relative air humidity and air temperature, 
independently from one another, on the number of visits and 
interactions, also independently from one another, for each 
sample. We previously tested the assumptions of normality 
and homogeneity of variances. We performed the test on the 
software R, version 4.1.0 (R Core Team, 2020). 

With the data of all the collected hymnopterans and all 
the sampled plants, we built 12 networks of flower-visiting 
hymenopteran interactions. There were four groups: one 
consisting of ants and bees, another consisting of bees and 
wasps, another consisting of ants and wasps and another 
consisting of the three taxonomic groups. For each of those 
groups, we built three networks: one for the morning period, 
one for the afternoon period and one for the period of a whole 
day. We built the networks in this way to check how each 
group impacts the community of hymenopterans. For each 
network, we used weighted matrices to analyze specialization 
and discover the central species and binary matrices to analyze 
nestedness and modularity.

Primarily, on the software R version 4.1.0 (R Core 
Team, 2020), we evaluated specialization by employing 
the specialization index H₂’, which ranges from 0 (low 
specialization, generalist network and many overlapping 
interactions) to 1 (high specialization, specialist network and 
low or no overlapping interactions) (Blüthgen et al., 2006). 
Making use of null models, we calculated the significance of 
specialization by looking at the actual value of specialization 



Mariana R Menezes et al. – Hymenoptera Flower-Visitors in a Botanical Garden4

and comparing it to a sequence of values randomized a 
thousand times. The p-value reflects the position of the 
observed value in the probability distribution which was 
plotted (Mello et al., 2016). Next, to assess non-random 
patterns of hymenopteran-flower interaction, we measured 
nestedness. We calculated the nestedness of the network using 
the NODF metric in the ANINHADO software (Guimarães 
& Guimarães, 2006), using 1000 networks generated by null 
model II. Values range from 0 (not nested) to 100 (perfectly 
nested) (Bascompte et al., 2003).  Then, we assessed whether 
there were groups of Hymenoptera that only associate with 
one plant set and are extremely specialized; to do this, 
we calculated the modularity of the networks. We used 
MODULAR software (Guimerà & Amaral, 2005) to verify 
the modularity of the networks. The modularity index ranges 
from 0 (no modules) to 1 (completely separated modules). 
We used a thousand networks randomized by the null model 
II with constant total margins (Bascompte et al., 2003). 
Thereafter, we used the methodology described by Dáttilo et 
al. (2013a) to discover the core species in that community. 
This allowed us to verify the flower visitors’ species with the 
higher frequency of interactions, in other words, the most 
generalist species in the community. We also discovered the 
plant core species. Moreover, to measure the turnover in the 
hymenopteran community composition between the morning 
and the afternoon periods, we calculated the temporal niche 
overlap. We used Jaccard’s similarity for the networks of 

mixed assemblages and the networks of all communities; as 
follows: A/(A + B + C), where A is the number of flower-
visitor species shared between the two sampling periods, B is 
the number of flower-visitor species present only during the 
morning and C is the number of flower-visitor species present 
only during the afternoon (Dáttilo et al., 2014a). 

Results

In our study, we found 10 different bee species, 9 
different wasp species and 18 different ant species (Table 1) 
interacting with twenty different plant species (Table 2). The 
total number of visits by bees recorded over the whole sample 
period was 231, resulting in 49 different interactions with 
17 plant species; visits by wasps were 77, distributed in 34 
interactions with 13 plant species; and ants accounted for 175 
recorded visits and 65 interactions with 16 plant species.

Average relative air humidity in samplings was 69.01 ± 
7.56%. The relative air humidity was not shown to impact 
the amount of visits or interactions of any hymnopteran. 
Neither the number of bee visits (p = 0.2243, τ = -0.1427) 
nor the amount of bee interactions were influenced by relative 
humidity of air (p = 0.2717, τ = -0.1571), as were not the 
number of wasp visits (p = 0.7777, τ = -0.0391) and the 
amount of wasp interactions (p = 0.3538, τ = -0.1293) or the 
number of ant visits (p = 0.1359, τ = -0.1982) and interactions 
(p = 0.1488 τ = -0.1937). 

ID Family Hymenoptera species

#01 Apidae Plebeia sp1

#02 Apidae Plebeia sp2

#03 Apidae Apis mellifera Linnaeus, 1758

#04 Halictidae Augochlora sp1

#05 Halictidae Augochloropsis sp1

#06 Apidae Trigona spinipes (Fabricius, 1793)

#07 Apidae Scaptotrigona sp1

#08 Apidae Nomada sp1

#09 Apidae Bombus sp1

#10 Colletidae Actenosigynes sp1

#11 Vespidae Charterginus sp1

#12 Vespidae Polybia paulista von Ihering, 1896

#13 Vespidae Angiopolybia sp1

#14 Vespidae Polybia sp1

#15 Vespidae Ceramiopsis gestroi Zavattari, 1910

#16 Vespidae Polybia sp2

#17 Vespidae Polybia sp3

#18 Vespidae Charterginus sp2

#19 Vespidae Charterginus sp3

Table 1. The flower-visiting hymenopterans at the UFRRJ Botanical Garden, in Seropédica, Rio de Janeiro, Brazil; from December 2018 
to December 2019.

#20 Formicidae Pseudomyrmex sp1

#21 Formicidae Pseudomyrmex sp2

#22 Formicidae Brachymyrmex heeri Forel, 1874

#23 Formicidae Solenopsis invicta Buren, 1972

#24 Formicidae Crematogaster sp1

#25 Formicidae Camponotus crassus Mayr, 1862

#26 Formicidae Wasmannia auropunctata (Roger, 1863)

#27 Formicidae Cephalotes atratus (Linnaeus, 1758)

#28 Formicidae Solenopsis sp1

#29 Formicidae Brachymyrmex sp1

#30 Formicidae Camponotus sp1

#31 Formicidae Brachymyrmex admotus Mayr, 1887

#32 Formicidae Crematogaster curvispinosa Mayr, 1862

#33 Formicidae Crematogaster limata Smith, F., 1858

#34 Formicidae Pseudomyrmex sp3

#35 Formicidae Camponotus novogranadensis Mayr, 1870

#36 Formicidae Brachymyrmex sp3

#37 Formicidae Brachymyrmex sp2

ID Family Hymenoptera species



Sociobiology 69(4): e7894 (December, 2022) 5

Average air temperature during the sampling period 
was 27.65 ± 3.83 °C. Ambient temperature did not affect the 
number of bee visits (p = 0.6062, τ = -0.0605) or interactions 
(p = 0.3514, τ = -0.1094) or the number of wasp visits (p = 

0.6592, τ = -0.0610) or interactions (p = 0.7618, τ = -0.0422), 
but it did positively influence the number of ant visits (p = 
0.0010, τ = 0.4360, Fig 1) and the number of interactions (p = 
0.0010, τ = 0.4420, Fig 2).

Fig 1. Kendall regression of temperature and number of ant visits to flowers at the UFRRJ botanical garden, in Seropédica, Rio de 
Janeiro, Brazil; from January 2019 to December 2019. The x-axis represents temperature and the y-axis represents the number of visits.

Fig 2. Kendall regression of temperature and number of ant interactions with flowers at the UFRRJ botanical garden, in Seropédica, Rio de 
Janeiro, Brazil; from January 2019 to December 2019. The x-axis represents temperature, and the y-axis represents the number of interactions.



Mariana R Menezes et al. – Hymenoptera Flower-Visitors in a Botanical Garden6

In August, bees had the highest average number of 
visits and the highest average number of interactions (Fig 3; 
Fig 4), whereas the highest average number of wasp visits 
was observed in May and August (Fig 3), especially in the 
former (Fig 4); for ants, March had the highest average 
number of visits and interactions (Fig 3; Fig 4). In December 
2019, the lowest average numbers of visits and interactions by 
bees (Fig 3; Fig 4) and no wasps foraging on any flowers were 
observed, while no ants visited any flowers in the period from 
September through October of that same year (Fig 3; Fig 4).

The networks of the community of flower-visiting 
Hymenoptera were nested during the morning (NODF = 
23.17, p = 0.03), the afternoon (NODF = 19.96, p = 0.01) and 
all day (NODF = 25.41, p < 0.001). These networks exhibited 
no modularity and showed significant specialization (morning: 
H₂’ = 0.35, p < 0.001; afternoon: H₂’ = 0.39, p < 0.001; all 
day: H₂’ = 0.37, p < 0.001) (Table 3). The Hymenoptera core 
species were: in the morning - Apis mellifera, Plebeia sp.1, 

Fig 3. The average number of visits by groups of flower-visitors at the UFRRJ Botanical Garden, in Seropédica, Rio de Janeiro, 
Brazil; from December 2018 to December 2019. In red, the number of ant visits; in green, the number of bee visits; in blue, the 
number of wasp visits. The x-axis represents the average number of visits, and the y-axis represents the month of the sample.

Plebeia sp.2, Trigona spinipes, and Camponotus crassus; in 
the afternoon - Apis mellifera, Plebeia sp.2, Trigona spinipes, 
Camponotus crassus, and Wasmannia auropunctata; on 
the whole day - Apis mellifera, Plebeia sp.1, Plebeia sp.2, 
Trigona spinipes, Camponotus crassus, and Wasmannia 
auropunctata (Table 3). The plant core species were: in the 
morning, in the afternoon and on the whole day, respectively: 
Stifftia chrysantha, Clerodendrum x speciosum, Callistemon 
viminalis, and Antigonon leptopus (Table 3).

The networks for ants and bees assemblages were 
nested during the afternoon (NODF = 19.31, p = 0.05) and 
during the whole day (NODF = 14.64, p < 0.001), but were 
not nested during the morning. These networks showed no 
modularity and displayed significant specialization (morning: 
H₂’ = 0.38, p < 0.001; afternoon: H₂’ = 0.43, p < 0.001; whole 
day: H₂’ = 0.40, p < 0.001) (Table 3). The Hymenoptera 
and plant core species in these nets were the same as the 
core species obtained for the community nets (Table 3).  



Sociobiology 69(4): e7894 (December, 2022) 7

Fig 4. The average of interactions by groups of flower-visitors at the UFRRJ botanical garden, in Seropédica, Rio de Janeiro, Brazil; 
from December 2018 to December 2019. In red, the number of ant visits; in green, the number of bee visits; in blue, the number of 
wasp visits. The x-axis represents the average number of interactions and the y-axis represents the month of the sample.

ID Family Plant species n

P01 Anacardiaceae Schinus terebinthifolia Raddi 7

P02 Arecaceae Phoenix sp1 1

P03 Asteraceae Stifftia chrysantha Mikan 9

P04 Boraginaceae Cordia superba Cham. 4

P05 Cactaceae Cactaceae sp1 1

P06 Chrysobalanaceae
Microdesmia rigida (Benth.) Sothers 
& Prance

3

P07 Ericaceae Rhododendron sp1 2

P08 Fabaceae Bauhinia variegata L. 3

P09 Fabaceae Cassia fistula L. 3

P10 Fabaceae
Paubrasilia echinata (Lam.) Gagnon 
& Lewis

1

Table 2. Plants involved in interactions of floral-visiting hymnopterans at the botanical garden of UFRRJ, in Seropédica, Rio de Janeiro, Brazil; 
from December of 2018 to December of 2019.

P11 Lamiaceae Clerodendrum x speciosum W. Bull 5

P12 Lamiaceae
Clerodendrum speciosissimum 
Drapiez

4

P13 Lecythidaceae Couroupita guianensis Aubl. 4

P14 Malvaceae Hibiscus sp1 5

P15 Malvaceae Hibiscus sp2 1

P16 Melastomataceae Tibouchina granulosa (Desr.) Cogn. 1

P17 Myrtaceae Callistemon viminalis G. Don ex Loud. 6

P18 Polygonaceae Antigonon leptopus Hook. & Arn. 6

P19 Sapindaceae Sapindus sp1 1

P20 Verbenaceae Duranta repens L. 2

ID Family Plant species n



Mariana R Menezes et al. – Hymenoptera Flower-Visitors in a Botanical Garden8

The networks for bees and wasps assemblages were nested 
during the morning (NODF = 16.89, p = 0.01), the afternoon 
(NODF = 16.25, p = 0.02) and the whole day (NODF = 17.35, 
p = 0.02). These networks exhibited no modularity and the same 
specialization in every period (H₂’ = 0.29, p < 0.001) (Table 3). 
The Hymenoptera core species were: in the morning and on 
the whole day – Apis mellifera, Plebeia sp.1, Plebeia sp.2, and 
Trigona spinipes; in the afternoon – A. mellifera, Plebeia sp.2, 
and T. spinipes (Table 3). The plant core species were: in the 
morning, in the afternoon and on the whole day, respectively 
– Stifftia chrysantha, Callistemon viminalis, and Antigonon 
leptopus (Table 3). At last, the networks for wasps and ants 

assemblages were nested during the afternoon (NODF = 
11.43 p = 0.02) and during the whole day (NODF = 17.35, p = 
0.01), but weren’t nested during the morning. These networks 
showed no modularity and significant specialization (morning: 
H₂’ = 0.37, p < 0.001; afternoon: H₂’ = 0.42, p < 0.001; all 
day: H₂’ = 0.43, p < 0.001) (Table 3). The Hymenoptera core 
species were the same in all networks: Angiopolybia sp1, 
Camponotus crassus, and Wasmannia auropunctata. The 
plant core species were: in the morning – Clerodendrum x 
speciosum, and A. leptopus (Table 3); in the afternoon and on 
the whole day – Cordia superba, Clerodendrum x speciosum, 
and A. leptopus (Table 3).

H₂’ Modularity Nestedness Hymenoptera Core Plant Core
All groups
Morning 0.35 (p < 0.001) 0.30 (p = 0.88) 23.17 (p = 0.03) #01; #02; #03; #06;  #25 P03; P11; P17; P18
Afternoon 0.39 (p < 0.001) 0.33 (p = 0.90) 19.96 (p = 0.01) #02; #03; #06; #25; #26 P03; P11; P17; P18
All day 0.37 (p < 0.001) 0.26 (p = 0.91) 25.41 (p < 0.001) #01; #02; #03; #06; #25; #26 P03; P11; P17; P18

Ants + Bees
Morning 0.38 (p < 0.001) 0.41 (p = 0.30) 13.11 (p = 0.11) #01; #02; #03; #06; #25 P03; P11; P17; P18
Afternoon 0.43 (p < 0.001) 0.46 (p = 0.32) 19.31 (p = 0.05) #02; #03; #06; #25; #26 P03; P11; P17; P18
All day 0.40 (p < 0.001) 0.35 (p = 0.65) 14.64 (p < 0.001) #01; #02; #03; #06; #25; #26 P03; P11; P17; P18

Bees + Wasps
Morning 0.29 (p < 0.001) 0.37 (p = 0.66) 16.89 (p = 0.01) #01; #02; #03; #06 P03; P17; P18
Afternoon 0.29 (p < 0.001) 0.38 (p = 0.65) 16.25 (p = 0.02) #02; #03; #06 P03; P17; P18
All day 0.29 (p < 0.001) 0.33 (p = 0.86) 17.35 (p = 0.02) #01; #02; #03; #06 P03; P17; P18

Wasps + Ants
Morning 0.37 (p < 0.001) 0.45 (p = 0.27) 12.65 (p = 0.11) #13; #25; #26 P11; P18
Afternoon 0.42 (p < 0.001) 0.46 (p = 0.32) 11.43 (p = 0.02) #13; #25; #26 P04; P11; P18
All day 0.43 (p < 0.001) 0.36 (p = 0.79) 14.15 (p = 0.01) #13; #25; #26 P04; P11; P18

The organism code in the Hymenoptera central species column is in Table 1.
The organism code in the plant central species column is in Table 2.

Table 3. Network metrics of all matrices obtained based on the observation of a community of flower-visiting hymenopterans at the 
botanical garden of the UFRRJ, in Seropédica, Rio de Janeiro, Brazil. During December of 2018 to December of 2019. Specialization = H₂’. 
Hymenoptera core species = Hymenoptera Core. Plant core species = Plant Core. 

The Jaccard similarity index of the networks of all 
taxonomic groups was 0.73, which means that 73% of 
observed hymenopteran species are the same in the morning 
and in the afternoon periods; networks of bees and wasps 
and of wasps and ants exhibited a higher similarity (Jaccard 
similarity index = 0.76; 0.79, respectively); ants and bees 
networks displayed the highest composition similarity among 
all networks (Jaccard similarity index = 0.80).

The morning network of all groups indicates a 
predominance of interactions made by ants; however, the 
number of visits made by bees was higher. Because of that, 
bee visits were the most often, mainly the visits made by Apis 
mellifera and Trigona spinipes (Fig 5a). The most visited 
plants in the morning were, respectively, Antigonon leptopus 

and Callistemon viminalis (Fig 5a). In the afternoon network, 
A. mellifera occupied the position with the highest number 
of visits, in other words, a greater frequency of interaction, 
followed by the ant species Camponotus crassus (Fig 5b). It is 
remarkable that in the afternoon the frequency of ants became 
higher and they were still the group with more interactions. The 
plants with the highest number of visits also changed during the 
afternoon: species that occupied prominent positions were C. 
viminalis and Stifftia chrysantha (Fig 5b). The all-day network 
showed similarities with both nets, in different aspects: 
regarding flower visitors, the all-day net was similar to the 
afternoon network, with a greater frequency of interaction 
of the species A. mellifera, but with a large frequency of 
interaction of ants; regarding the plants visited, the all-day 



Sociobiology 69(4): e7894 (December, 2022) 9

network was closer to the result obtained by the morning 
network, with the species A. leptopus and C. viminalis being 
the plants with the highest number of visits (Fig 5c).

Discussion

In this study, we correlated the number of observed 
visits and interactions of each group of organisms with two 
abiotic factors – air temperature and relative air humidity. 
Our results showed that relative air humidity did not affect 
the number of visits or interactions of any of the assemblages 
and that air temperature did not affect the number of visits 
or interactions of bees or wasps; however, the higher the 
temperature, the more visits and interactions ants made. We 
also used the networks constructed from the floral-visitor 
community to assess the interaction pattern and composition 
of this community and the influence of each group of 
organisms on the community in different temporal niches. 
Our results showed that most networks exhibited the same 
interaction pattern in the morning and in the afternoon, except 
for the ant-bee and wasp-ant networks: these networks were 
nested, non-modular and of low specialization. On the other 
hand, in all networks, the core hymenopteran species changed 
when comparing the morning and the afternoon periods, 
which means that the composition of this community differed 
according to temporal niche. The assemblages also showed 
that the entire community of floral-visitors displayed different 
compositions and interaction patterns: the networks with bees 
displayed greater nestedness, while the networks with ants 
exhibited greater specialization; the morning ant-bee and 
wasp-ant networks were not nested; in addition, the central 
plant species visited in the wasp-ant network differed from 
the central plant species visited in the other networks.

Relative air humidity, despite influencing nectar 
composition (Winkler et al., 2009), did not impact the number 
of floral visits or interactions in any communities. Elements 
of the study area may have contribuited to the the irrelevance 
of this factor to visits and interactions, such as the presence 
of a lake, irrigation and plant management (Cysneiros et al., 
2011). Irrigation is one of the anthropogenic tools which can 
alter the microclimate, influencing not only plants but also 
the distribution of insect species (Federman et al., 2013). Air 
temperature had a positive role on the number of ant visits 
and interactions, exhibiting a strong correlation. Visits tended 
to be more frequent between 30-33° celsius, which is the air 
temperature range of highest insect activity (Paaijmans et 
al., 2013; Carvalho et al., 2014). Air temperature shapes the 
foraging behavior of ants and these are very heat resistant 
organisms, with activity recorded at air temperatures above 
60 °C (Heinrich, 1993; Luna et al., 2021). Thus, a positive 
correlation of air temperature with ant visits and interactions 
had been expected and was duly confirmed, whereas air 
temperature had no effect on the number of bee and wasp visits 
and interactions. Bee and wasp visits and interactions may 
be affected by other abiotic factors which were not analyzed 

Fig 5. Networks of all groups of floral visiting hymenopterans at 
the UFRRJ botanical garden, in Seropédica, Rio de Janeiro, Brazil; 
from December 2018 to December 2019. The network is organized 
according to the frequency of interactions (visits). On the left are 
the visiting insect species and on the right are the plant species. In 
yellow are highlighted visits by bees, whereas visits made by wasps 
are highlighted in blue and visits made by ants are highlighted in red. 
A: Morning network; B: Afternoon network; C: All-day network.



Mariana R Menezes et al. – Hymenoptera Flower-Visitors in a Botanical Garden10

in this work, such as rainfall, wind speed and solar radiation 
(Simões et al., 1985; Loyola & Martins, 2006; Oliveira et al., 
2012; Kovac et al., 2015; Marinho & Vivallo, 2020).

Almost all networks showed low specialization, 
nestedness and no modularity, what points to the presence of 
highly generalist species which used the resources of several 
plants (Blüthgen et al., 2007; Blüthgen & Klein, 2011; Blüthgen, 
2012). Low specialization also indicates that this network 
has a functional ecological niche redundancy; this may be 
due to the nestedness of niches among the present species or 
the fact that the species interacted with many different plant 
species, displaying generalism. Networks which present niche 
redundancy usually are observed in communities which are 
more stable in the face of adversity; however, as many species 
exploit the same resources, that can generate an increase in 
interspecific competition (Blüthgen & Klein, 2011; Blüthgen, 
2012). Several factors may explain the nestedness and non-
modular patterns of insect-plant community networks; some 
are abiotic (e.g. air temperature, rainfall, soil pH, elevation) 
and others are biotic (e.g. flower-visitor size, animal behavior, 
nectar characteristics) (Chamberlain et al. 2010; Rico-Gray et 
al., 2012; Lange et al., 2013; Dáttilo et al., 2013b; Dáttilo et 
al., 2014a; Santos et al., 2014; Giannini et al., 2015; Petanidou 
et al. 2017; Adedoja et al., 2018). Regarding the community 
studied, what possibly explains the nested pattern is the 
presence of super-generalist and dominant species (such as 
Apis mellifera, Trigona spinipes, Camponotus crassus, and 
Wasmannia auropunctata), which visit most of the plant 
species in the area and also interact with the set of plants 
visited by peripheral species (Dáttilo et al., 2014a; Dáttilo et 
al., 2014b; Giannini et al., 2015). Moreover, it is important to 
note that the ant-bee and wasp-ant networks did not achieve 
nestedness during the morning period, probably because the 
frequency of visitation of important super-generalist species 
(such as Camponotus crassus, and Wasmannia auropunctata) 
decreased, what promoted nestedness in the afternoon and all-
day networks (Díaz-Castelazo et al., 2013), and because of a 
greater presence of peripheral species (Díaz-Castelazo et al., 
2010; Lange & Del-Claro, 2014). The likely explanation for 
the non-modular pattern of these networks, besides a small 
specialization and a mostly generalist community, is the 
behavior of the flower-visiting Hymenoptera (Dáttilo et al., 
2014a; Dáttilo et al., 2014b). Wasps and ants do not use only 
floral resources in their feeding; these organisms are occasional 
floral-visitors, often associated with the predation of other 
arthropods, the exploitation of other botanical resources (e.g. 
extrafloral nectary, fruits) and the consumption of other 
types of food sources, what makes their interaction more 
generalized and does not facilitate the constitution of modules 
in the networks (Brodmann et al., 2008; Rico-Gray & Oliveira, 
2008; Mello et al., 2011; Dáttilo et al., 2014a; Brock et al., 
2021; Lavisky et al., 2021). Bees, while exclusively floral-
visitors, interact with different types of plants according to 
availability, which can even affect the density and abundance 

of these organisms (Ebeling et al., 2011; Grass et al., 2016).  
The low diversity of vegetation in a botanical garden can 
affect these patterns too since vegetation structure is important 
for the composition of insect communities (Clemente et al., 
2012; Junker et al., 2012; Rico-Gray et al., 2012). Although 
non-modular networks are a common pattern in generalist 
mutualistic networks (Del-Claro et al., 2018), the small number 
of plant species sampled may have impacted the result of this 
metric, because pollination networks with less than 50 plant 
species tend to lack modularity (Olesen et al., 2007).

When we looked at the metrics of the combined 
taxonomic group network, we found that most core species 
in the nets were bees and that the nestedness of bee-wasp and 
bee-ant networks was higher, except for the morning period of 
the bee-ant network. This may be explained by the behavior 
of the bees. Bees receive much attention for being crucial 
for the pollination of a large number of plants; their body 
is adapted to collect and store floral resources (Imperatriz-
Fonseca et al., 2012) and they are the only animals capable of 
consuming all available floral resources (Torezan-Silingardi, 
2012). Oligolectic bees visit either a restricted group of 
plants or only one type of plant, being highly specialized and 
performing pollination with great efficiency (Schlindwein, 
2004; Imperatriz-Fonseca et al., 2012). No bee species found 
in the locality of this study are classified as oligolectic, 
which is probably caused by the low plant diversity, since 
no plants pollinated by these bees are found in the study 
area (Schlindwein, 2004). That can also explain why the 
specialization is lower in nets combined with bees. A higher 
specialization value in networks which feature ants may also 
be explained by the presence of peripheral species, but the 
value obtained was lower than that obtained for ant-plant 
interaction networks observed in other studies (Guimaraes 
et al., 2006; Junker et al., 2012). The networks were not 
highly specialized, as specialization is one of the strategies 
which may be adopted by organisms involved in floral 
visitation to decrease competition (Junker et al., 2012); another 
strategy which they can adopt is to perform visits at different 
times (Tschoeke et al., 2015). The similarity of community 
composition between the morning and the afternoon periods 
may be considered high, possibly indicating that this is not a 
strong strategy found in this community. However, there were 
differences between the morning and the afternoon networks 
and those differences may be greater according to the size 
of the community, the study area and the time discrepancy 
between niches (Díaz-Castelazo et al., 2013; Dáttilo et al., 
2014). The difference which stands out the most is the change 
of some core species organisms when comparing the periods. 

On the community level, the core species in the all-day 
network are four bee species and two ant species; although the 
greater presence of bees in this position is already expected, 
it is important to understand the biology and behavior of 
these animals to comprehend the important characteristics 
of the community and the study site. In the morning period, 



Sociobiology 69(4): e7894 (December, 2022) 11

there was a higher presence of bees as core species; in the 
afternoon, the frequency of visits by ants increases, adding 
one more ant species to the group of core species. Apis 
mellifera, a generalist bee, with an average size of 11-13 mm, 
which has a high foraging and pollination efficiency, having 
a very large foraging range for an arthropod (Beekman & 
Ratnieks, 2001; Costa et al., 2015) was firstly observed as the 
species with the highest number of visits, being the main key 
species of the community studied. Despite being an important 
species in the network, linked to several plant species, this 
bee is an exotic species, which has been pointed out as a risk 
to the conservation of native species (Paini, 2004; Russo et 
al., 2021). The genus Plebeia had two species pointed as core 
species. The genus belongs to the Meliponini tribe of stingless 
bees and includes species native to Brazil. The bees of the 
genus are small, with an average size of 3-4 mm, generalists 
and responsible for the pollination of several native plants 
(Pick & Blochtein, 2002; Wittmann, 2008). Trigona spinipes 
was also considered a key bee species. It is also from the 
Meliponini tribe, measuring approximately 7 mm, a native 
pollinator capable of pollinating several plant species, super-
generalist and associated with improved fruit production 
(Chalegre et al., 2020; Tschoeke et al., 2015). Highlighting 
the core species of ants, Camponotus crassus belongs to the 
Formicidae subfamily and is a species which measures 20 
mm and has no metapleural gland, being unable to produce 
harmful substances in the pollen (Del-Claro et al., 2019); it 
is a dominant forager in vegetation, exploits resources which 
do not come from flowers alone (Lange et al., 2019) and 
has already been associated with effective pollination (De 
Vega et al., 2014; Del-Claro et al., 2019). Finally, Wasmannia 
auropunctata is an ant from the subfamily Myrmicinae; the 
smallest of the key species, measuring 1.5 mm, it is invasive, 
commonly found in urban areas, often involved in cases of 
environmental impact and may have medical importance 
(Azevedo et al., 2022; Gruber et al., 2022). There are no 
studies relating this species to pollination, so it competes with 
pollinators once it recruits massively to dominate resources 
(Azevedo et al., 2022). Wasps had occasional interactions with 
flowers and were not often observed (except for Angiopolybia 
sp.1) having a greater presence as a peripheral species (Díaz-
Castelazo et al., 2010; Lange & Del-Claro, 2014); therefore, 
no wasp species was considered core in the all-group networks. 
In almost all the other networks, the species core remained 
the same, except for the wasp-ant networks, which featured 
a wasp as a key species. Angiopolybia is one of the genera 
of Polistinae and presents native representatives from Brazil; 
this genus is abundant in Atlantic forest areas and, despite 
adaptations to the necrophagic habit, consumes other resources 
(Lima et al., 2010; Togni et al., 2014), as observed in this study. 

In addition to the core species of floral visitors, the 
core species of plants visited also reveal to us important 
characteristics of this community. In the community nets and 
the ant-bee nets, the core plant species were the same, not 

varying according to time of day. In the bee-wasp networks, 
the composition was very similar to the general network, minus 
one core plant species – Clerodendrum x speciosum. However, 
for the wasp-ant networks, the composition was different from 
the community network and there were differences between 
the most visited plants according to the time of day. Only in 
the networks with bees, Stifftia chrysantha and Callistemon 
viminalis were part of the core species, indicating a greater 
interaction of bees with these species. S. chrysantha is a native 
tree, which can reach 5 meters in height, has inflorescence 
of tubular flowers, displays shades of orange and is most 
frequently pollinated by hummingbirds, while rarely by bees 
(Nishida et al., 2014; Lorenzi, 2020; Gobatto et al., 2021). C. 
viminalis is an exotic species, one of the several honey trees 
pollinated by bees; it reaches up to 7 meters in height, has 
terminal, pendulous and spike-like inflorescence and flowers 
of numerous red stamens (Latif et al., 2016; Lorenzi, 2018; 
Guallpa-Calva et al., 2019). In the case of Clerodendrum x 
speciosum, it is a core species only in networks with ants. It is 
a woody shrub, a hybrid of exotic species, with inflorescence 
in terminal racemes and red flowers whose genus’ species are 
commonly pollinated by bees; herbivorous ants, plunderers 
and attendant ants have already been associated with these 
plants (Carver et al., 2003; Rohitash, 2010; Lorenzi, 2015; 
Groutsch et al., 2018; Mukhopadhyay & Quader, 2018). It is 
noticeable that in the wasp-ant networks there was a smaller 
amount of plants in the core species and also a plant which 
was not present in any core species of any other networks: 
Cordia superba. This native tree can reach up to 10 meters 
high, has large white flowers, is pollinated by small insects 
and bees and is not uncommonly visited by nectar pillagers 
(Agostini & Sazima, 2003; Vale et al., 2013; Silva & Rossa-
Feres, 2016; Lopes et al., 2015; Lorenzi, 2020; Gobatto et 
al., 2021). One of the plants was in the core species of all 
the community networks, indicating that it is a well-visited 
plant by all three organisms: Antigonon leptopus, a semi-
herbaceous climber from Mexico with inflorescence of many 
durable flowers in pink or white colors (Lorenzi, 2015); it is a 
flower species visited frequently by bees, decently by wasps 
and rarely by ants (Raju et al., 2001; Lorenzi, 2015; Gobatto 
et al., 2021; Lima et al., 2021).  

Studies on plant-pollinator networks in the tropics 
have been conducted more often in forests than in open 
habitats, with sampling concentrated over a single season 
(Vizentin-Bugoni et al., 2018). However, deforestation in the 
tropics has created an increasing proportion of open habitats 
(e.g. in the Atlantic forest domain) (Hirota, 2003) and it is 
crucial to assess information about ecological interactions in 
this kind of habitat, now predominant in most landscapes. The 
loss of green areas can impact the richness and abundance 
of flower-visitor communities in cities, what can jeopardize 
the biodiversity and functional richness of that community 
(Spiesman & Inouye, 2013; Geslin et al., 2016). Controlled 
environments may be critical for the preservation of flower-



Mariana R Menezes et al. – Hymenoptera Flower-Visitors in a Botanical Garden12

visiting species in urban areas (Smith, 2006; Larson, 2014; 
Twerd & Banaszak-Cibicka, 2019; Twerd et al., 2021), what 
demonstrates that even small green areas are important for 
insect conservation. However, urban administrators should 
ideally plan to create urban parks which support, attract and 
maintain flower-visitors and have a large vegetation cover 
and a high variety of plant species, preferably with different 
morphologies (Garbuzov & Ratnieks, 2014; Banaszak-Cibicka 
et al., 2016; Hall et al., 2017). In this context, botanical gardens 
stand out as a good tool for the conservation of flower-visitor 
communities, as they serve as ecological corridors, shelter 
and foraging sites (Hall et al., 2017; Maruyama et al., 2019; 
Marín et al., 2020; Gobatto et al., 2021). Our study endorses 
that a botanical garden can sustain a diverse community of 
flower-visiting Hymenoptera in an urban environment (Ito 
et al., 2001; Mazzeo & Torretta, 2015; Marinho & Vivallo, 
2020), being an important tool for biodiversity conservation 
(Hall et al., 2017; Maruyama et al., 2019; Marín et al., 2020; 
Gobatto et al., 2021). When it comes to botanical gardens in 
Atlantic Forest areas, especially in the state of Rio de Janeiro, 
it is clear that our results corroborate other studies already 
conducted, as the botanical garden studied clearly supports 
a diverse community of floral-visiting Hymenoptera, whose 
composition, which includes many pollinating species, is 
very similar to communities observed by other researchers 
(Pimentel & Rangel, 2017; Santos et al., 2017; Silva et al., 
2018; Marinho e Vivallo, 2020; Gobatto et al., 2021). Being 
close to an area of forest fragments, the botanical garden 
studied has the potential to be an ecological corridor, as well 
as the Botanical Garden of Rio de Janeiro (Gobatto et al., 
2021). However, future work is necessary to prove that this 
urban park is effectively an ecological corridor. Moreover, the 
current study can serve as a comparison for following works 
that investigate the response of flower-visiting Hymenoptera 
to climate change (Hofmann et al., 2018). 

From the above, our study can contribute by showing 
that there is a correlation between the number and frequency 
of ant floral interactions and ambient temperature and by 
strengthening data on network patterns of flower-visitor 
communities. Moreover, it highlights the importance of 
botanical gardens for the maintenance of flower-visiting 
hymenopteran communities in urban environments. Future 
studies can further explore whether pollination is performed 
by floral-visitors and their niche in their communities.

Acknowledgments

We are grateful to Dr. Marcelo da Costa Souza for his 
help with botanical identification. APLS and MSM would like 
to thank the Proverde Program (Jardim Botânico - UFRRJ), 
and MRM and RC are thankful to CAPES (Coordenação 
de Aperfeiçoamento de Pessoal de Nível Superior; finance 
code-001) for the scholarships. We also thank two anonymous 
reviewers for their valuable comments on an earlier version 
of the manuscript.

Authors’ Contribution

MRM: Conceptualization; formal analysis; investigation; data 
curation; writing-original draft; writing-review and editing; 
resources.
BFSL: Conceptualization; formal analysis; investigation; 
writing-original draft; writing-review and editing.
APLS: Methodology; validation; data curation.
ECBF: Methodology; validation; data curation; organism 
identification.
MSM: Methodology; validation; data curation.
RC-N: Methodology; validation; formal analysis.
JMQ: Methodology; validation; writing-review and editing; 
supervision; project administration; funding acquisition.

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