Palynology

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Botanical characterization of Apis mellifera honeys

in areas under different degrees of disturbance in
the southern Yucatan Peninsula, Mexico

Amayrani Córdova-Rodríguez, Alejandro A. Aragón-Moreno, Gerald A. Islebe

& Nuria Torrescano-Valle

To cite this article: Amayrani Córdova-Rodríguez, Alejandro A. Aragón-Moreno, Gerald A. Islebe

& Nuria Torrescano-Valle (2023) Botanical characterization of Apis mellifera honeys in areas
under different degrees of disturbance in the southern Yucatan Peninsula, Mexico, Palynology,
47:4, 2215290, DOI: 10.1080/01916122.2023.2215290

To link to this article: https://doi.org/10.1080/01916122.2023.2215290

Published online: 20 Jun 2023.

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PALYNOLOGY
2023, VOL. 47, NO. 4, 2215290
https://doi.org/10.1080/01916122.2023.2215290

Botanical characterization of Apis mellifera honeys in areas under different

degrees of disturbance in the southern Yucatan Peninsula, Mexico

rdova-Rodr
ıguez, Alejandro A. Arago
Amayrani Co
n-Moreno , Gerald A. Islebe and Nuria Torrescano-Valle
Departamento Conservaci
on de la Biodiversidad, El Colegio de la Frontera Sur, Chetumal, Mexico

ABSTRACT KEYWORDS
Apiculture is an important economic activity in Mexico, and deforestation, extensive agriculture, and Apis mellifera; honey;
other types of land use threaten sustainable honey production. This study aimed to determine the flo- melissopalynology; bee-
ral resources used by Apis mellifera for honey production, in vegetation types with different disturb- keeping; conservation
ance degrees in Southern Yucatan Peninsula, Quintana Roo state. A total of 24 honey samples, from
eight apiaries, were collected during the months of the highest honey production in the region
(February to May 2022). Standard acetolysis technique was applied for melissopalynological analysis. A
total of 68 pollen types were identified. Our results suggest that the disturbance degree of the vegeta-
tion does not affect the pollen diversity and honey composition, mainly because the available floral
resources remain similar. Viguiera dentata (Asteraceae) was the most abundant (>45%) herbaceous
species in honey samples of February and March. Piscidia piscipula (Fabaceae) and Haematoxylum cam-
pechianum (Fabaceae) in samples of March (16%-45%), and P. piscipula in April (>45%). Spondias mom-
bin (Anacardiaceae), Bursera simaruba (Burseraceae), and Metopium brownie (Anacardiaceae) were the
most abundant (16%-45%) arboreal species found in samples of May. Although our results can be
used to develop conservation strategies looking for sustainable honey production, further studies
should focus on vegetation with a better conservation state, during longer time periods, and during
periods with fewer resources available for honeybees.

1. Introduction 1991; Giro
n Vanderhuck 1995; Ram
ırez-Arriaga et al. 2016), a

Apiculture is an important socioeconomic activity for devel-
oping countries through honey production and other bee-
hive byproducts like pollen, propolis, beeswax, and royal
jelly. Honey, the most important product of beekeeping, has
been used for millenia as a natural sweetener and is con-
sumed globally due to its nutritional value and importance
in human health (Bradbear 2004; Machado De-Melo et al.
2018). It is produced from the nectar of flowers (Barth 1989;
Olaitan et al. 2007) and is mainly composed of carbohydrates
and water, along with some minor amounts of proteins, lip-
ids, vitamins, minerals, and organic acids. It contains bio-
active principles (flavonoids and phenols) and important
aromatic and secondary metabolites derived from its source
plants that give every honey a unique added value (Olaitan
et al. 2007; da Silva et al. 2016; Machado De-Melo et al.
2018; Weis et al. 2022). The composition and quality of
honey depend on several factors including the floral source,
geographical origin, climate conditions, bee species (Barth
2004). Every plant species contributes specific organoleptic
characteristics and other physicochemical components that
determine the success of honey commercialization (Machado
De-Melo et al. 2018).
The plant contribution to honey can be studied by melis-
sopalynological analysis (Louveaux et al. 1978; Ramalho et al.
method for identifying pollen contained in honey (Barth
1989; Bryant and Jones 2001). Additionally, melissopalynol-
ogy allows researchers to determine honey’s botanical origin
and bees’ floral preferences and to classify honey according
to its pollen content (Villanueva-Guti
errez et al. 2009; de
Almeida-Muradian et al. 2020). When honey presents a dom-
inant pollen type (>45%), it can be classified as monofloral
(Louveaux et al. 1978; Mart
ınez-Hern
andez and Ram
ırez-
Arriaga 1998; Villanueva-Gutie
rrez et al. 2009), with specific
organoleptic characteristics, and high commercial value and
acceptability in national and international markets
(Villanueva-Guti
errez et al. 2009). On the contrary, multifloral
honey presents a high variety of pollen types, with variable
properties and organoleptic characteristics (Louveaux et al.
1978; Mart
ınez-Hern
andez and Ram
ırez-Arriaga 1998;
Villanueva-Guti
errez et al. 2009).
In Mexico, apiculture is an important activity for the pri-
mary production sector, favors job creation, and generates
additional income for rural families (Magan ~ a Magan~ a et al.
2012). Although honey production in Mexico has been
declining in recent years (Secretar
ıa de Agricultura y
Desarrollo Rural 2020), it is the eighth-largest worldwide
honey producer and the third major exporter (INEGI 2021). In
2020, 54,122 tons of honey were produced nationally, with
24% of this total national production harvested in the

CONATCT Alejandro A. Arag

on-Moreno alejandro.aragon@ecosur.mx Departamento Conservaci

on de la Biodiversidad, El Colegio de la Frontera Sur,
Chetumal, M
exico.
ß 2023 AASP – The Palynological Society

Published online 20 Jun 2023

2 A. CÓRDOVA-RODRÍGUEZ ET AL.
Yucatan Peninsula (YP) and the state of Quintana Roo specif-
ically contributing 4% (Secretar
ıa de Agricultura y Desarrollo
Rural 2020). The relationship of honey with flowers, vegeta-
tion, and the blossoming periods around the apiary has
been well identified (Moar 1985). Therefore, deforestation,
landscape fragmentation, extensive agriculture, and other
land use changes threaten bees’ nutrition and plant pollin-
ation by reducing available floral resources (Roubik 2006).
Cairns et al. (2005) suggests that the disturbed vegetation in
the YP affects the bee species diversity and increases compe-
tition for resources between Apis mellifera and native bees.
In this context, most of the tropical forest loss has occurred
in the southern part of the YP, one of the most important
regions for honey production. During the last 15 years,
Quintana Roo, one of the three states that comprise the YP,
has lost a total of 194,006 hectares of tropical forest. Thus,
local honey production has suffered from increasing land-
scape fragmentation, deforestation rates, unsustainable agri-
cultural activities, and growing urban areas (Madrid-Zubir
an
et al. 2021).
Melissopalynology is the study of pollen in honey, provid-
ing valuable information of the plants honeybees use to pro-
duce it (Louveaux et al. 1978; Ramalho et al. 1991; Giro
n
Vanderhuck 1995; Ram
ırez-Arriaga et al. 2016). It can also be
used to determine the floral preferences of bees (de
Figure 1. Study site. Upper right box: Mexico highlighting the state Quintana Roo, which is the zoom in image of the bottom right square. Large left box: Apiaries
location: I: A~no nuevo, II: Esperanza III: Bacalar, IV: Reforma, V: Iturbide, VI: Remate, VII: Cementerio, VIII: La isla. See figure 2 for land use and vegetation buffer color legend.
Source: Author.
Almeida-Muradian et al. 2020). In Mexico, there are several
melissopalynological studies in honey of the European hon-
eybee Apis mellifera (e.g. Ram
ırez-Arriaga et al. 2011;
Co
rdova-Co
rdova et al. 2013; Ram
ırez-Arriaga et al. 2016).
Nevertheless, melissopalynological studies of honeybees’
honey in the YP are considerably lacking, and efforts are
needed to identify floral resources used by honeybees in the
region (Villanueva 1994; Villanueva 2002; Villanueva-Guti
errez
et al. 2009; Villanueva-Guti
errez et al. 2015). Hence, it is of
utmost importance to analyze the pollen resources used by
bees to produce honey for developing strategies that allow
the sustainability of this activity in the region. Our present
study aims to fill this gap of knowledge to determine the
palynological composition of Apis mellifera honey under dif-
ferent degrees of vegetation disturbance in southern
Quintana Roo.
2. Materials and methods
2.1. Study area
Pooled honey samples, donated by traditional beekeepers,
were obtained from eight apiaries located in the Bacalar
municipality in the southern Yucatan Peninsula, in Quintana
~ o nuevo’: I, ‘Esperanza’: II, ‘Bacalar’: III,
Roo state, Mexico (‘An

‘Reforma’: IV, ‘Iturbide’: V, ‘Remate’: VI, ‘Cementerio’: VII, and
‘La Isla’: VIII) (Figure 1). Vegetation types consist mainly of
medium and low-statured semi-evergreen tropical forests,
with different perturbation degrees, all with 1200 mm of
average annual precipitation and annual temperatures higher
than 20  C. Representative species like Manilkara sapota can
be found, along with other highly valuable commercial spe-
cies (Islebe et al. 2015). Agriculture, apiculture, tourism, and
livestock are the main economic activities, whereas maize,
soybean, pineapple, and beans are the main cultivated crops
(Mart
ınez-Falco
n 2020). Local flowering species were
recorded and collected to make a palynological reference
collection of the area.
2.2. Location of apiaries and disturbance of
surrounding vegetation
Apiaries were georeferenced on site and the land use and
vegetation types were determined with a vectorial shapefile
of land use of the Bacalar municipality during 2021
(CONABIO 2022) in QGIS software (‘Bialowieza’ Version
3.16.11). A 5 km ratio of buffer area from the apiary was
established based on the mean flight distance of honeybees
reported in the literature (Figure 2). Apis mellifera bee work-
ers can travel up to 10 km from the hive to get resources for
the colony when floral resources are scarce. When resources
Figure 2. Buffer area of apiaries with the type of land use and vegetation. I: A~
VII: Cementerio, VIII: La isla. Source: Author.
PALYNOLOGY 3
are abundant, they stay below 2 km distance from the hive
(Levin and Glowska-Konopacka 1963; Visscher and Seeley
1982; Beekman and Ratnieks 2000).
Land use and vegetation types (CONABIO 2022) in the
buffer areas were translated into quantitative data using
percentages. Disturbance degrees in each buffer area were
defined in relation to the average value of all land use
types associated with disturbance: human settlement,
grassland, seasonal and annual agriculture, and different
secondary shrub vegetation types in early ecological stages
(Figure 3).
The average value between the disturbance area of all
apiaries was calculated to differentiate apiaries into two cate-
gories. Apiaries with more than 23.6% of disturbance land
use and vegetation areas were assigned to the ‘Highly dis-
turbed’ category, whereas values < 23.6% were assigned to
the ‘Low disturbance’ category.
2.3. Honey sampling, pollen extraction, and analysis
A composite honey sample of 100 ml from each apiary was
collected during every harvest from February to May 2022
for a total of 24 honey samples. The following samples were
tagged and inventoried into the ECOSUR’s honey collection:
‘Esperanza’ (A5, A6, A12, A16, A28, and A35), ‘An ~ o nuevo’
(A15, A17, A19, A25, A26), ‘Reforma’ (A18, A27, A34, A36), ‘La
no nuevo, II: Esperanza III: Bacalar, IV: Reforma, V: Iturbide, VI: Remate,
4 A. CÓRDOVA-RODRÍGUEZ ET AL.
~o nuevo, II: Esperanza III: Bacalar, IV: Reforma, V: Iturbide, VI: Remate, VII: Cementerio,
Figure 3. Percentage of land use and vegetation surrounding apiaries. I: An
VIII: La isla.
Isla’ (A23 y A29), ‘Cementerio’ (A20 y A32), ‘Iturbide’ (A22 y
A33), ‘Bacalar’ (A21 y A30), and ‘Remate’ (A31) apiaries.
Standard pollen extraction methods were applied to 20 g
of honey of each honey sample, diluted in water and ethyl
alcohol (Bryant and Jones 2001; Jones and Bryant 2004;
Jones and Bryant 2014; Paredes and Bryant 2020; Riding
2021; Riding 2021). A tablet of Lycopodium spores (20,848
spores/tablet) was added to each sample in order to cal-
culate pollen concentration (Stockmarr 1971; Jones and
Bryant 2004), and the standard acetolysis technique was
used to highlight pollen features and ornamentation
(Erdtman 1960). A minimum of 500 pollen grains were
counted and identified (Lau et al. 2018) using the palyno-
logical reference collection of the herbarium in El Colegio de
la Frontera Sur, acetolyzed flowers collected in the apiaries’
periphery, and published palynological atlases from the area
(Palacios-Ch
avez et al. 1991; S
anchez-Dzib et al. 2009). Pollen
concentration was used to categorize honey samples using
the following groupings (Maurizio 1975): Category I (<20,000
grains/10g), honeys with very low pollen concentration due
to different possible factors like low (high) pollen (nectar)
producing plants, artificially fed bees, or altered honey;
Category II (20,000–100,000 grains/10g), the standard pollen
concentration range of almost every natural honey in the
world; Category III (100,000–500,000 grains/10g), for honey
produced mainly from high pollen-producing plants, or
honey harvested from combs with pollen reservoirs;
Categories IV (500,000–1,000,000 grains/10g) and V (more
than 1,000,000 grains/10g) used rarely for honey produced
from floral resources with exceptionally high pollen produc-
tion (Paredes and Bryant 2020).
Pollen counts were used to calculate the Shannon-
Weiner diversity index (H’) of each honey sample (Moreno
2000; Lau et al. 2019), and pollen types were classified
according to their frequency (Louveaux et al. 1978):
Dominant (D; > 45%), Secondary (S; 16–45%), Important
minor (I; 3–15%), and Minor (M; < 3%). The pollen percen-
tages of samples were used to plot a single pollen diagram
in Tilia software version 2.6.2 (Grimm 2019). The cluster ana-
lysis (CONISS) tool was used for sorting samples according
to their similarity.
3. Results
Apiaries Iturbide, Remate, and An ~ o Nuevo are located in high
perturbation zones (> 23% of disturbance surface), while apia-
ries Cementerio, Esperanza, Bacalar, Reforma, and La Isla are
found in low disturbed cover (< 23%) (Figure 3). Sixty-eight
pollen types were identified in the 24 honey samples: 26 trees,
20 shrubs, 19 herbs, two palms, and one vine (Figure 4), dis-
tributed across 29 botanical families. Fabaceae is the most rep-
resented family (17 pollen types), followed by Asteraceae (7),
Figure 4. Pollen diagram showing the percentages of taxa identified in Apis mellifera honey samples and the results of the cluster analysis.
PALYNOLOGY
5
6 A. CÓRDOVA-RODRÍGUEZ ET AL.

Table 1. Honey harvest, categories of pollen concentration (PC) and pollen glabra y Cecropia peltata. A subdivision within these was
diversity (Shanon-Weaver, H’) of Apis mellifera honey from the eight apiaries
seen due to the high percentage of Spondias mombin in the
of Bacalar, Quintana Roo.
samples from the Reforma apiary as compared to the rest.
Sample Honey PC
name Apiary harvest (category) H’ The second main group is characterized by a similar abun-
A5 Esperanza Early February 72968 (II) 1.7 dance of Piscidia piscipula, Haematoxylum campechianum,
A6 Esperanza End February 26730 (II) 1.5 Dalbergia glabra and Viguiera dentata in samples from
A12 Esperanza Early March 12249 (I) 1.9
February to April. It is divided into two subgroups. The first
A15 A~no nuevo Early March 39187 (II) 1.7
A16 Esperanza End March 178945 (III) 1.8 one is composed of high percentages of Viguiera dentata in
A17 A~no nuevo End March 197683 (III) 1.7 samples of February and early March, whereas the second sub-
A18 Reforma March 62176 (II) 1.9
A19 A~no nuevo Early april 85955 (II) 2.1
group by high values of Haematoxylum campechianum in
A20 Cementerio March 75644 (II) 2.4 March samples from Bacalar, Cementerio, Iturbide, and
A21 Bacalar March 79346 (II) 2.5 Reforma apiaries.
A22 Iturbide March 55319 (II) 2.2
A23 La isla March 70744 (II) 1.5
A25 A~no nuevo End april 224516 (III) 1.4
A26 A~no nuevo Medium april 57863 (II) 1.5 4. Discussion
A27 Reforma April 374519 (III) 1.9
A28 Esperanza April 92049 (II) 1.4 The cluster analysis showed that the flowering phenology,
A29 La isla May 48462 (II) 2.3 floral preferences, land-use cover, and plant species in the
A30 Bacalar May 37692 (II) 1.6
A31 Remate May 168087 (III) 1.9
surrounding vegetation of the apiaries were used to differen-
A32 Cementerio May 62659 (II) 2.3 tiate the honey samples. They were grouped first by month
A33 Iturbide May 44674 (II) 2.1 as a result of the blooming periods. Another subdivision was
A34 Reforma Medium May 104830 (III) 2.2
A35 Esperanza May 29296 (II) 2.7
based on the diversity of pollen types. Although all the apia-
A36 Reforma End May 299979 (III) 1.8 ries have similar surrounding vegetation, the abundance of
I: Category I, II: Category II, V: Category V. certain floral resources varied. For example, Haematoxylum
campechianun (Fabaceae) grows in wet and seasonal-flooded
Euphorbiaceae (6), and Sapindaceae (4), which altogether areas. Some of the apiaries have higher vegetation cover,
account for 50% of the total identified pollen. Poaceae (3), with more plant individuals of H. campechianum. This taxon
Convolvulaceae (3), Arecaceae (2), Sapotaceae (2), Rubiaceae is also a preferred floral resource of honeybees, and has
(2), Amaranthaceae (2), and Malvaceae (2) were also present been reported as an important species for honey production
with more than one pollen type. Urticaceae, Nyctaginaceae, in other areas of the YP (Porter-Bolland 2003).
Anacardiaceae, Burseraceae, Combretaceae, Polygonaceae, The low pollen concentration in sample A6 (Apiary
Ulmaceae, Cannabaceae, Myrtaceae, Commelinaceae, Esperanza, End of February) suggests that it was pressure-fil-
Lamiaceae, Salicaceae, Meliaceae, Bixaceae, Anacardiaceae, tered or from sugar-fed honeybees (Paredes and Bryant
Moraceae, Malpighiaceae, and Vitaceae were each represented 2020). Nevertheless, the palynological analysis of this sample
with one single pollen type. Classification of honey samples indicates high percentages of Viguiera dentata and other
according to their pollen concentration and diversity indexes Asteraceae, species reported as high-nectar producers
(H’) are summarized in Table 1. (Villanueva-Guti
errez et al. 2009). This relatively low pollen
Ten honey samples presented dominant (> 45%) pollen concentration is also present in other honey samples with
types: Viguiera dentata in February and early March samples similar pollen content (A12 and A15). The samples classified
(A5, A6, A12 and A15), Celtis iguanaea in the May sample as Category III presented pollen from different nectariferous
from Bacalar apiary (A30), Dalbergia glabra in the March sam- species, but also high pollen producers like Piscidia piscipula
ple from Esperanza apiary (A16), Piscidia piscipula in the (Fabaceae), Dalbergia glabra (Fabaceae), and Spondias mom-
March sample from La Isla apiary (A23) as well as the April bin (Anacardiaceae) (Porter-Bolland et al. 2009).
samples from An ~ o nuevo and Esperanza apiaries (A25, A26 According to the Shannon-Weiner diversity index, the
and A28). Secondary pollen types Dalbergia glabra (44.6%) samples with dominant pollen were less diverse, as described
and Haematoxylum campechianum (42.6%) presented high- by Villalpando-Aguilar et al. (2022). These authors reported
frequency values during March’s harvest at An ~ o nuevo and lower (higher) pollen diversity in monofloral (multifloral) hon-
Reforma (A18), respectively. Spondias mombin (31.8%) was eys. The diversity index (H’) of our samples showed that hon-
dominant in the April sample of Reforma apiary (A27), and eys with dominant pollen types had lower diversity, and this
Bursera simaruba (32.9%) together with Metopium brownei condition could change between samples of different
(29.1%) were present in high frequencies in the May sample months due to the variable forage strategy driven by
of Remate apiary (A31). Other 38 pollen types were classified resource availability and floral preferences of A. mellifera.
as Minor according to their frequency (Table 2 and Figure 4). The plant families most represented in the honey samples
The cluster analyses grouped the honey samples by were Fabaceae, Asteraceae, Euphorbiaceae, and Sapindaceae
month, floral resources taxa, and abundance, regardless of (Plate 1), as previously reported in honeys of the Yucatan
the disturbance degrees of vegetation, revealing two main peninsula (Villanueva-Guti
errez et al. 2009). Fabaceae is the
groups (Figure 4). The first one is composed of all May sam- largest family in the Yucat
an peninsula with around 230
ples and represented mainly by Piscidia piscipula, Bursera described species and can be found as dominant plants in
simaruba, Metopium brownei, Spondias mombin, Dalbergia vegetation with different successional stages (Flores 1990;
 PALYNOLOGY 7

Table 2. Frequency classes of pollen grains identified in Apis mellifera honey samples from the eight apiaries.
Sample
February March April May
TAXA A5 A6 A12 A15 A16 A17 A18 A20 A21 A22 A23 A19 A26 A28 A25 A27 A29 A30 A31 A32 A33 A34 A35 A36
AMARANTHACEAE
Amaranthus spinosus M M M
Philoxerus vermicularis M M M
morphotype
ANACARDIACEAE
Metopium brownei M M M M M M M I I I I I I S I S M S M
Spondias mombin M S M M S I S
ARECACEAE
Sabal sp. M M M I M M M M M M M M M
Thrinax radiata M M M M
ASTERACEAE
Bidens pilosa I I I M M M M
Cosmos caudatus I M M M M M M
Critonia quadrangularis M M M M M
Koanophyllon albicaulis I M
Pluchea sp. M
Trixis inula M M M M
Viguiera dentata D D D D I S M M I I S I M M M M I
BURSERACEAE
Bursera simaruba M M M M M M M M I I S S I S S S I S I
BIXACEAE
Cochlospermum vitifolium M M I I M I M M
CANNABACEAE
Celtis iguanaea M M M M M M I M M M I D M I M M
COMBRETACEAE
Bucida bucera M M I M M M M M M I M M M M M I M M M
COMMELINACEAE
Commelina erecta M M M M M M M M M
CONVOLVULACEAE
Jacquemontia pentantha I M M M M M M
Ipomoea carnea M M M M
Turbina corymbosa M M
EUPHORBIACEAE
Acalypha leptopoda M M
Cnidoscolus souzae M M M
Croton punctatus M M M M M M
Croton reflexifolius M M M M M
Euphorbia schlechtendalii M M M M M M
morphotype
Jatropha gaumeri M M M M M M M M M I M M M M
FABACEAE
Acacia gaumeri M M M
Acacia collinsii M M M M M
Caesalpinia yucatanensis M M M M M M M
Dalbergia glabra M D S S I M I S M I I I M I I S M I I
Desmanthus virgatus M M
Diphysa yucatanensis M M I M M M M I I I M I M M M M M I M
Fabaceae 1. M
Gliricidia sepium M M M M M I S M M M M M
Haematoxylum campechianum M M M S S S S M I M M M M M M M M
Leucaena leucocephala M M M M M M
Lonchocarpus punctatus I M M
Mimosa bahamensis M M M M M I M I M M M M M M M
Mimosa pudica M M M M M I M S M M M M M M M M M M M M M
Piscidia piscipula M M S S I I S D S D D D S S M I S I I I I
Pithecellobium lanceolatum M M M M M M M M
Senna racemosa M M M M M I M I S M
Vigna sp. M M M
LAMIACEAE
Vitex gaumeri M M I M M M M M M
MALPIGHIACEAE
Byrsonima crassifolia M M M
MALVACEAE
Luehea speciosa M M M
Sida sp. M M
MORACEAE
Cedrela odorata M M M M M M M M
MORACEAE
Brosimum alicastrum M M M M
MYRTACEAE
Eugenia sp. M M M I M M M M M M M M I I S
(continued)
8 A. CÓRDOVA-RODRÍGUEZ ET AL.

Table 2. Continued.
Sample
February March April May
TAXA A5 A6 A12 A15 A16 A17 A18 A20 A21 A22 A23 A19 A26 A28 A25 A27 A29 A30 A31 A32 A33 A34 A35 A36
Nyctaginaceae
Pisonia aculeata M M M M M S I I I M I M M M M M M M M M
POACEAE
Poaceae 1. M I I M M I M M M M M M M M
Poaceae 2. I M M M M
Zea mays M M M M M M M M M M M
POLYGONACEAE
Gymnopodium floribundum I M M M M M M M M M M M M M M M M M M
RUBIACEAE
Randia obcordata M M M M M M
Rhachicallis americana M M M M
morphotype
SALICACEAE
Cupania sp. M M M
Serjania yucatanensis M M
Talisia oliviformis M M M M M M
Thouinia paucidentata M M M M M M M M M M M M M
Zuelania guidonia M M M M M M M M M
SAPOTACEAE
Pouteria reticulata M M M M M M
Dipholis salicifolia M M M M M M M M M M M
morphotype
ULMACEAE
Trema micrantha M M M M M M S I M M M M M M M I M M
URTICACEAE
Cecropia peltata M M M I M M M I M I M M M M S I M S I I M M
VITACEAE
Vitis sp. M M M M
D, predominant pollen (>45%); S, secondary pollen (16–45%); I important minor pollen (3–15%); M, minor pollen (< 3%).

Carnevali Fern
andez-Concha et al. 2010). Most of the
Fabaceae pollen types found in the honey samples belong to
arboreal species, with the main blooming period during the
dry season from March to May (Valdez-Hern
andez et al. 2015).
Asteraceae is the dominant herbaceous family in early
successional stages, from 1 to 2 years. They are visited by dif-
ferent insects, including bees, flies, wasps, and butterflies.
Apis mellifera is probably the most recorded visitor of
Asteraceae, while it represents one of the most important
floral resources for social bees and many other pollinators
(Pinheiro et al. 2008). Our results showed that Asteraceae
was the most important floral resource during February, as
reported in a palynological study of honeys from the Sian
Ka’an Biosphere Reserve (Villanueva-Guti
errez et al. 2015), a
nearby protected area. Asteraceae are distinctive along the
manmade trails to milpas (traditional croplands), apiaries,
and grassland borders with other herbaceous species of the
Fabaceae and Poaceae families. Nevertheless, this vegetation
is not considered in the vegetation and land-use shapefile
because of its reduced and changing surface. Viguiera den-
tata ‘tajonal’ is the most representative species of the family,
with the largest flowering period between November and
February (Villanueva-Guti
errez et al. 2009). This species, along
with other Asteraceae, is one of the preferred floral resources
of A. mellifera in the region (Villanueva-Guti
errez et al. 2009),
and other parts of the country (Granados-Argu €ello et al.
2020), representing an important resource for sustainable
apiculture.
Spondias mombin (Anacardiaceae) ‘xkinin hobo’ is a neo-
tropical tree that can be found in different parts of America,
Asia, and Africa (Tiburski et al. 2011). This tree is often
associated with secondary vegetation stages of semi-ever-
green and sub-deciduous forest (Pennington and Sarukh
an
2005; Arce-Romero et al. 2016). In Mexico, some palyno-
logical studies from the states of Oaxaca (Ram
ırez-Arriaga
et al. 2011), Tabasco (Co
rdova-Co
rdova et al. 2013), and
Puebla (Ram
ırez-Arriaga and Mart
ınez-Hern
andez 2007) have
found S. mombin as a minor pollen contributor, as also
reported in other palynological studies in the Yucatan penin-
sula (Villanueva 2002; Porter-Bolland 2003). We found high
percentages of this species only in samples from the
Reforma Apiary (A27, A34, A36), where several trees grow in
the periphery of the apiaries. Honeybees foraged them
strongly during the blooming period because of their prox-
imity (Levin and Glowska-Konopacka 1963; Visscher and
Seeley 1982) and accessibility (Ponnuchamy et al. 2014).
Other studies in Brazil (Carneiro and Martins 2012) and
Nigeria (Oyeyemi and Kayode 2013) have found A. mellifera
as a frequent and abundant visitor of S. mombin.
Bursera simaruba and Metopium brownei are high nectar-
and pollen-producing species during the dry season in the
Yucat
an peninsula (Villanueva 2002), and both pollen types
were present in most of the honey samples of April and
May. Bursera simaruba ‘chakah’ is the second most important
species for honey production in the entire Yucat
an peninsula
(Villanueva-Guti
errez et al. 2009) and is also present in honey
from Oaxaca (Ram
ırez-Arriaga et al. 2011), Tabasco (Co
rdova-
Co
rdova et al. 2013), and Veracruz (Granados-Arg€ uello et al.
2020) states of Mexico. It is a native tree species in Mexico
with a broad distribution, growing in different tropical forests
and secondary vegetation (Pennington and Sarukh
an 2005).
Metopium brownei, is also abundant in tropical forests of
 PALYNOLOGY 9

Plate 1. Photographs of some of the most common pollen types found in honey samples. (A) Piscidia piscipula (Fabaceae). (B-C) Spondias mombin (Anacardiaceae):
(B) equatorial view; (C) polar view. (D) Bursera simaruba (Burseraceae). (E) Viguiera dentata (Asteraceae). (F) Haematoxylum campechianum (Fabaceae). (G) Metopium
brownei (Anacardiaceae). (H) Dalbergia glabra (Fabaceae). (I) Gymnopodium floribundum (Polygonaceae). Scale bars – 20 lm.

southeast Mexico, but with lower abundance in low-statured
tropical forests (Anaya et al. 1999; Pennington and Sarukh
an
2005). These two species were found in most honey samples,
representing some of the most important floral resources of
honeybees in our study area. Piscidia piscipula ‘Jab
ın’ is
another pollen type found with high percentages in honey
samples from March to April. Although Villanueva-Guti
errez
et al. (2009) reported this species as the third most impor-
tant floral resource in honey samples in the Yucatan penin-
sula, this was the most important resource during March and
April in our study area, along with Dalbergia glabra.
Haematoxylum campechianum ‘palo tinto’ is a tree species
that grows in seasonally flooded forests in southeastern
Mexico (Pennington and Sarukh
an 2005), and its pollen is
commonly found in honey from Tabasco (Castellanos-
Potenciano et al. 2012). This species was found growing in
the surrounding vegetation of the apiaries, and as a second-
ary pollen type in honey samples during May from
Cementerio, Iturbide, Reforma, and Bacalar apiaries. During
our vegetation and honey sampling, this species had abun-
dant flowering, and honeybees were foraging it. Its presence
as a secondary pollen type in the samples could be derived
from their high nectar-producing flowers, making the pollen
content underrepresented. Nevertheless, it is also possible
that the flowering periods are not long enough for a better
representation of this species. This could also be the case for
10 A. CÓRDOVA-RODRÍGUEZ ET AL.
Gymnopodium floribundum ‘dzidzil che’, a small tree species
present in several vegetation types in Mesoamerica, includ-
ing the states of Tabasco, Chiapas, and the Yucatan penin-
sula in Mexico (vicario-Mej
ıa and Echazarreta 1999). It is
known by beekeepers as one of the main floral resources for
honey production in the Yucatan pen
ınsula (Villanueva-
Guti
errez et al. 2009; Villalpando-Aguilar et al. 2022).
However, this species is also reported as a highly nectarifer-
ous plant, though low polliniferous (Porter-Bolland 2003;
Coh-Mart
ınez et al. 2019), which could explain the low per-
centages in our pollen counts.
Nectarless plants like Mimosa pudica, Cecropia peltata,
Celtis iguanaea, Mimosa bahamensis, Senna racemosa and
Poaceae were frequent and abundant in the samples (> 3%),
while Commelina erecta, Leucaena leucocephala, Brosimum ali-
castrum, Desmanthus virgatus, Acacia gaumeri, Acacia collinsii,
and Zea mays had values lower than 3%. Similar results were
previously reported from honey harvested in secondary
vegetation types (Villanueva-Guti
errez et al. 2009), and
although these could represent a protein source incorpo-
rated into honey (Roubik 1992), it is also possible that they
were transported into the hive by wind (Villanueva 1994).
5. Conclusions
Our results showed that vegetation disturbance does not
influence the palynological diversity and composition of Apis
mellifera honeys. This might be due to the generalist capacity
of the species and competition with other bees that allow
them to adapt to both disturbed and conserved environ-
ments. Moreover, despite the apiaries being located in vege-
tation with different disturbance degrees, climatological
conditions, altitude, and other geomorphological conditions
are shared between all apiaries, and the main land-use is
traditional agriculture. Because of this, the available floral
resources are still similar, with shared native species like
Bursera simaruba, Metopium brownei, Piscidia piscipula,
Gymnopodium floribundum, Haematoxylum campechianum
and Spondias mombin.
Our results can be used to identify potential sites to
establish apiaries in the region, as well as to promote the
conservation of the most important plant species for honey
production in the region. Nevertheless, further research is
needed to better understand the landscape usage by A. mel-
lifera, not only for honey production but for resource avail-
ability during periods of scarcity, when colonies are more
vulnerable and prone to a decline in population. In this
sense, continuing the melissopalynological studies is crucial
to help apiculturists and decision-makers to develop strat-
egies to guarantee the sustainability of this activity.
Acknowledgements
We thank Margarito Tuz Novelo for the help in the field and translation
from Maya to Spanish with the beekeepers. Beekeepers from Bacalar,
Quintana Roo, provided us with honey samples and allowed us access
to their apiaries.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Funding
ACR received support from a CONACYT scholarship for postgraduate
studies and ECOSUR Postgraduate General Coordination scholarships
granted through the Facilitation of Remote Work Programs (sanitary con-
finement, COVID-2019) and Complementary Support for Master’s Thesis.
ORCID

n-Moreno
Alejandro A. Arago http://orcid.org/0000-0001-5188-6444
References
Anaya AL, Mata R, Rivero-Cruz F, Hern
andez-Bautista BE, Ch
avez-Velasco
D, Go
mez-Pompa A. 1999. Allelochemical potential of Metopium brow-
nei. Journal of Chemical Ecology. 25(1):141–156.
Arce-Romero AR, Universidad AC, Monterroso-Rivas AI, Go
mez-D
ıaz JD,
Universidad AC, Universidad AC, Universidad Auto
noma Chapingo.
2016. Mexican plums (Spondias spp.): their current distribution and
potential distribution under climate change scenarios for Mexico.
Revista Chapingo Serie Horticultura. XXIII(1):5–19.
Barth OM. 1989. O Po
len no Mel Brasileiro. Rio de Janeiro: Instituto
Oswaldo Cruz.
Barth OM. 2004. Melissopalynology in Brazil: a review of pollen analysis of
honeys, propolis and pollen loads of bees. Scientia Agricola. 61(3):342–350.
Beekman M, Ratnieks FLW. 2000. Long-range foraging by the honey-bee,
Apis mellifera L. Functional Ecology. 14(4):490–496.
Bradbear N. 2004. La apicultura y los medios de vida sostenibles. Rome
(IT): Food & Agriculture Org.
Bryant VM, Jones GD. 2001. The r-values of honey: pollen coefficients.
Palynology. 25(1):11–28.
Cairns CE, Villanueva-Guti
errez R, Koptur S, Bray DB. 2005. Bee
Populations, Forest Disturbance, and Africanization in Mexico.
Biotropica. 37(4):686–692.
Carneiro LT, Martins CF. 2012. Africanized honey bees pollinate and pre-
empt the pollen of Spondias mombin (Anacardiaceae) flowers.
Apidologie. 43(4):474–486.
Carnevali Fern
andez-Concha G, Tapia-Mun ~oz JL, Duno de Stefano R,
Ram
ırez-Morillo IM. 2010. Flora ilustrada de la Pen
ınsula de Yucat
an:
Listado flor
ıstico. Carnevali Fern
andez-Concha G, Tapia-Mun ~oz JL,
Duno de Stefano R, Ram
ırez-Morillo IM, editors. Centro de
Investigacio
n Cient
ıfica de Yucat
an, A.C.
Castellanos-Potenciano BP, Ram
ırez-Arriaga E, Zaldivar-Cruz JM. 2012.
An
alisis del contenido pol
ınico de mieles producidas por Apis melli-
fera L. (Hymenoptera: apidae) en el estado de Tabasco, M
exico. Acta
Zoolo
gica Mexicana (N.S.). 28(1):13–36.
Coh-Mart
ınez ME, Cetzal-Ix W, Mart
ınez-Puc JF, Basu SK, Noguera-Savelli
E, Cuevas MJ. 2019. Perceptions of the local beekeepers on the diver-
sity and flowering phenology of the melliferous flora in the commu-
nity of Xmab
en, Hopelche
n, Campeche, Mexico. Journal of
Ethnobiology and Ethnomedicine. 15(1):16.
CONABIO. 2022. Portal de geoinformacio
n 2022. Geoportal del Sistema
Nacional de Informacio
n sobre la Biodiversidad [Internet]. [accessed
2022 Dec 15]. http://www.conabio.gob.mx/informacion/gis/.

rdova-Co
Co
rdova CI, Ram
ırez-Arriaga E, Mart
ınez-Hern
andez E, Zald
ıvar-
Cruz JM. 2013. Caracterizacio
n bot
anica de miel de abeja (Apis melli-
fera L.) de cuatro regiones del estado de Tabasco, M
exico, mediante
t

ecnicas melisopalinolo
gicas. Universidad y ciencia. 29(2):163–178.
da Silva PM, Gauche C, Gonzaga LV, Costa ACO, Fett R. 2016. Honey: chemical
composition, stability and authenticity. Food Chemistry. 196:309–323.
de Almeida-Muradian LB, Barth OM, Dietemann V, Eyer M, da Silva de
Freitas A, Martel A-C, Marcazzan GL, Marchese CM, Mucignat-Caretta
C, Pascual-Mat
e A, et al. 2020. Standard methods for Apis mellifera
honey research. Journal of Apicultural Research. 59(3):1–62.

Dzib S, N
ajera S, Garc
ıa L. 2009. Morfolog
ıa pol
ınica de especies de la
selva mediana subperennifolia en la cuenca del rio Candelaria,
Campeche. Boletin de la Sociedad Argentina de Botanica. 84:83–104.
Erdtman G. 1960. The acetolysis method-a revised description. Svensk
Botanisk Tidskrift. 54:516–564.
Flores JS. 1990. The flowering periods of Leguminosae in the Yucatan
Peninsula in relation to honey flows. Journal of Apicultural Research.
29(2):82–88.
Giro
n Vanderhuck M. 1995. An
alisis palinolo
gico de la miel y la carga de
polen colectada por Apis mellifera en el suroeste de Antioquia, Colombia.
Bolet
ın Del Museo de Entomolog
ıa Universidad Del Valle. 3(2):35–54.
Granados-Arg€ uello RI, Villanueva-Guti
errez R, Mart
ınez-Hern
andez E,
Garc
ıa-Mayoral LE, Gonz
alez de la Torre JE. 2020. An
alisis melisopali-
nolo
gico de mieles de Apis mellifera L. en la zona centro de Veracruz,
Me
xico. Polibot
anica. 0(50):147–163.
Grimm EC. 2019. Tilia [Internet]. https://tilia-manual.readthedocs.io/en/
latest/get_tilia.html.
INEGI 2021. Atlas nacional de las abejas y derivados ap
ıcolas [Internet].
[accessed 2022 Dec 15]. https://atlas-abejas.agricultura.gob.mx.
Islebe GA, S
anchez-S
anchez O, Vald
ez-Hern
andez M, Weissenberger H. 2015.
Distribution of Vegetation Types. In: Islebe GA, Calm

n-Cort

e S, Leo es JL,
Schmook B, editors. Biodiversity and conservation of the Yucat
an
Peninsula. Cham (CH): Springer International Publishing; p. 39–53.
Jones GD, Bryant VM. 2014. Pollen studies of east Texas honey.
Palynology. 38(2):242–258.
Jones GD, Bryant VM. Jr. 2004. The use of ETOH for the dilution of
honey. Grana. 43(3):174–182.
Lau P, Bryant V, Ellis JD, Huang ZY, Sullivan J, Schmehl DR, Cabrera AR,
Rangel J. 2019. Seasonal variation of pollen collected by honey bees
(Apis mellifera) in developed areas across four regions in the United
States. PLoS One. 14(6):e0217294.
Lau P, Bryant V, Rangel J. 2018. Determining the minimum number of
pollen grains needed for accurate honey bee (Apis mellifera) colony
pollen pellet analysis. Palynology. 42(1):36–42.
Levin MD, Glowska-Konopacka S. 1963. Responses of foraging honeybees
in Alfalfa to increasing competition from other colonies. Journal of
Apicultural Research. 2(1):33–42.
Louveaux J, Maurizio A, Vorwohl G. 1978. Methods of melissopalynology.
Bee World. 59(4):139–157.
Machado De-Melo AA, Almeida-Muradian LD, Sancho MT, Pascual-Mat
e Roubik DW. 2006. Stingless bee nesting biology. Apidologie. 37(2):124–143.
A. 2018. Composition and properties of Apis mellifera honey: a review.
Journal of Apicultural Research. 57(1):5–37.
Madrid-Zubir
an S, Galeana-Pizan ~a JM, Navarro-Duarte CL. 2021. An
alisis
de los procesos de deforestacio
n en Quintana Roo del 2003–2018.
CentroGeo CAC, editor. Mexico City (MX): CONAFOR.
Magan ~a Magan ~a MA,
Moguel Ordo
n
~ez YB, Sangine
s Garc
ıa JR, Leyva
Morales CE. 2012. Estructura e importancia de la cadena productiva y
comercial de la miel en M
exico. Revista Mexicana de Ciencias
Pecuarias. 3(1):49–64.
Mart
ınez-Falco
n CI. 2020. Tren maya: conflictos socioterritoriales y ambi-
entales en el municipio de Bacalar, Quintana Roo. Rappo-Miguez SE,
editor. Puebla (MX): Benem
erita Universidad Auto
noma de Puebla;
[accessed 2022 Dec 19]. https://repositorioinstitucional.buap.mx/han-
dle/20.500.12371/15725.
Mart
ınez-Hern
andez E, Ram
ırez-Arriaga E. 1998. La importancia comercial
del origen bot
anico de las mieles por medio de su contenido de
granos de polen (Melisopalinolog
ıa). Apitec. 10:27–30.
Maurizio A. 1975. Microscopy of honey. In: Crane E, editor. Honey: a
Comprehensive Survey. Heinemann; p. 240–257.
Moar NT. 1985. Pollen analysis of New Zealand honey. New Zealand
Journal of Agricultural Research. 28(1):39–70.
Moreno CE. 2000. M
etodos para medir la biodiversidad. ORCYT, ORCYT-
UNESCO, Sociedad Entomolo
gica Aragonesa, editor. Zaragoza (ES):
M&T-Manuales y Tesis SEA.
Olaitan PB, Adeleke OE, Ola IO. 2007. Honey: a reservoir for microorgan-
isms and an inhibitory agent for microbes. African Health Science.
7(3):159–165.
Oyeyemi SD, Kayode J. 2013. Pollen analysis of Apis mellifera honey col-
lected from Nigeria. Bulletin of Pure & Applied Sciences-Botany. 32(2):
69–76.
PALYNOLOGY 11
Palacios-Ch
avez R, Ludlow-Wiechers B, Villanueva GR. 1991. Flora pali-
nolo
gica de la reserva de la biosfera de Sian Ka’an. Quintana Roo,
M
exico. Centro de Investigaciones de Quintana Roo.
Paredes R, Bryant VM. 2020. Pollen analysis of honey samples from the
Peruvian Amazon. Palynology. 44(2):344–354.
Pennington TD, Sarukh
an J. 2005. Arboles tropicales de M
exico: manual para

n de las principales especies. Mexico City (MX): UNAM.
la identificacio
Pinheiro M, Abr~ao BD, Harter-Marques B, Miotto STS. 2008. Floral resour-
ces used by insects in a grassland community in Southern Brazil.
Brazilian Journal of Botany. 31(3):469–489.
Ponnuchamy R, Bonhomme V, Prasad S, Das L, Patel P, Gaucherel C,
Pragasam A, Anupama K. 2014. Honey pollen: using melissopalynol-
ogy to understand foraging preferences of bees in tropical South
India. PLoS One. 9(7):e101618.
Porter-Bolland L, Medina-Abreo ME, Montoy-Koh JA, Montoy-Koh P, May-
Pacheco G. 2009. Flora mel
ıfera de La Montan ~a, Campeche: su impor-
tancia para la apicultura y para la vida diaria. Instituto de Ecolog
ıa, A. C.
Porter-Bolland L. 2003. La apicultura y el paisaje maya. Estudio sobre la

n de las especies mel
ıferas y su relacio
fenolog
ıa de floracio
n con el ciclo
ap
ıcola en La Montan~a, Campeche, Me
xico. Mexican Studies. 19(2):303–330.
Ramalho M, Guibu LS, Giannini TC, Kleinert-Giovannini A, Imperatriz-
Fonseca VL. 1991. Characterization of some southern Brazilian honey
and bee plants through pollen analysis. Journal of Apicultural
Research. 30(2):81–86.
Ram
ırez-Arriaga E, Mart
ınez-Bernal A, Ram
ırez Maldonado N, Mart
ınez-
Hern
andez E. 2016. An
alisis palinolo
gico de mieles y cargas de polen
de Apis mellifera (Apidae) de la regio
n Centro y Norte del estado de
Guerrero, M
exico. Botanical Sciences. 94(1):141–156.
Ram
ırez-Arriaga E, Mart
ınez-Hern
andez E. 2007. Melitopalynological char-
acterization of Scaptotrigona mexicana Gue
rin (Apidae: meliponini) and
Apis mellifera L. (Apidae: apini) honey samples in Northern Puebla State,
Mexico. Journal of the Kansas Entomological Society. 80(4):377–391.
Ram
ırez-Arriaga E, Navarro-Calvo LA, D
ıaz-Carbajal E. 2011. Botanical
characterization of Mexican honeys from a subtropical region
(Oaxaca) based on pollen analysis. Grana. 50(1):40–54.
Riding JB. 2021. A guide to preparation protocols in palynology.
Palynology. 45:1–157.
Roubik DW. 1992. Ecology and natural history of tropical bees. New York
(USA): Cambridge University Press.
Secretar
ıa de Agricultura y Desarrollo Rural. 2020. Servicio de
Informacio
n Agroalimentaria y Pesquera [Internet]. [accessed 2022
Dec 15]. http://infosiap.siap.gob.mx/.
Stockmarr J. 1971. Tables with spores used in absolute pollen analysis.
Pollen Spores. 13:615–621.
Tiburski JH, Rosenthal A, Deliza R, de Oliveira Godoy RL, Pacheco S.
2011. Nutritional properties of yellow mombin (Spondias mombin L.)
pulp. Food Research International. 44(7):2326–2331.
Valdez-Hern
andez M. 2015. Vegetative and reproductive plant phen-
ology. In: Islebe GA, Calm
e S, Leo
n-Cort
es JL, Schmook B, editors.
Biodiversity and conservation of the Yucat
an Peninsula. Cham:
Springer International Publishing; p. 57–96.
Vicario-Mej
ıa E, Echazarreta CM. 1999. Gymnopodium floribundum: a
major honey plant for beekeepers in Yucatan, Mexico. Bee World.
80(3):145–147.
Villalpando-Aguilar JL, Quej-Chi VH, Lo
pez-Rosas I, Cetzal-Ix W, Aquino-Luna

Alatorre-Cobos F, Mart
ınez-Puc JF. 2022. Pollen types reveal floral
VA,
diversity in natural honeys from Campeche, Mexico. Diversity. 14(9):740.
Villanueva GR. 1994. Nectar sources of European and Africanized honey
bees (Apis mellifera L.) in the Yucat
an Peninsula, Mexico. Journal of
Apicultural Research. 33(1):44–58.
Villanueva GR. 2002. Polliniferous plants and foraging strategies of Apis
mellifera (Hymenoptera: apidae) in the Yucat
an Peninsula, Mexico.
Revista de Biolog
ıa Tropical. 50(3–4):1035–1044.
Villanueva R. 2002. Polliniferous plants and foraging strategies of Apis
mellifera (Hymenoptera: apidae) in the Yucat
an Peninsula. Mexico.
Revista de Biologia Tropical. 50(3–4):1035–1044.
Villanueva-Gutie
rrez R, Moguel-Ordo
n
~ez YB, Echazarreta-Gonz
alez CM,
Arana-Lo
pez G. 2009. Monofloral honeys in the Yucat
an Peninsula,
Mexico. Grana. 48(3):214–223.
12 A. CÓRDOVA-RODRÍGUEZ ET AL.
Villanueva-Gutie
rrez R, Roubik DW, Porter-Bolland L. 2015. Bee–Plant
Interactions: competition and Phenology of Flowers Visited by Bees.
In: Islebe GA, Calm
e S, Leo
n-Cort
es JL, Schmook B, editors.
Biodiversity and conservation of the Yucat
an Peninsula. Cham (CH):
Springer International Publishing; p. 131–152.
Visscher PK, Seeley TD. 1982. Foraging strategy of honeybee colonies in
a temperate deciduous forest. Ecology. 63(6):1790.
Weis WA, Ripari N, Conte FL, Honorio M da S, Sartori AA, Matucci RH,
Sforcin JM. 2022. An overview about apitherapy and its clinical appli-
cations. Phytomedicine Plus. 2(2):100239.