Journal of Apicultural Research

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Local ecological knowledge of beekeeping with

stingless bees (Apidae: Meliponini) in Central
Veracruz, Mexico

Sherie Rae Simms & Luciana Porter-Bolland

To cite this article: Sherie Rae Simms & Luciana Porter-Bolland (2021): Local ecological
knowledge of beekeeping with stingless bees (Apidae: Meliponini) in Central Veracruz, Mexico,
Journal of Apicultural Research, DOI: 10.1080/00218839.2021.1965400

To link to this article: https://doi.org/10.1080/00218839.2021.1965400

Published online: 31 Aug 2021.

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JOURNAL OF APICULTURAL RESEARCH
https://doi.org/10.1080/00218839.2021.1965400

ORIGINAL RESEARCH ARTICLE

Local ecological knowledge of beekeeping with stingless bees (Apidae:

Meliponini) in Central Veracruz, Mexico
Sherie Rae Simms and Luciana Porter-Bolland
Red de Ecologia Funcional, Instituto de Ecologia, A.C., Veracruz, Mexico

ABSTRACT ARTICLE HISTORY

Beekeeping with stingless bees (Apidae: Meliponini), an ancient activity in Mesoamerica, is Received 1 May 2020
still practiced and considered culturally important in many areas. It is part of a rich legacy of Accepted 3 August 2021
biocultural diversity, as it represents cultural expressions that have developed over time as a
KEYWORDS
result of the interaction with the natural world. In this study we present the local ecological
Meliponiculture;
knowledge (LEK) associated with traditional stingless beekeeping in Atzalan, Veracruz, Scaptotrigona mexicana; bee
Mexico. We identified the diversity of managed bee species, LEK in terms of food resources management; bee-
for bees, types of bee management practices, as well as how this knowledge is transmitted landscape interactions;
and transformed. We also analyzed the terminology locally used for the practice, its uses, as biocultural diversity
well as perceptions of how beekeeping is changing in light of land use change. We found
that in Atzalan, stingless beekeeping is common among its inhabitants, and it is associated
with a strong LEK over its ecology, practice, and associated uses of bee products. Unlike
other regions in Mexico where stingless beekeeping is diminishing, in Atzalan it is flourish-
ing, driven by a market demand. However, land use changes and agricultural intensification
in the area may threaten its long-term viability. We consider that this practice should be
accompanied by integrated landscape planning for sustainable landscapes, where enrich-
ment planting and maintenance of agroforestry systems can enhance resources for bee pro-
duction. In these terms, conservation of the biocultural diversity associated with stingless
bee management can be key to bee diversity and its associated flora, while considering live-
lihood strategies.

Introduction cultures throughout the tropics (Cortopassi-Laurino

Stingless bees (Meliponini tribe of the Apidae family)
are widely distributed in the tropical and subtropical
regions of the world and about 500 species have
been described (Michener, 2007). They are consid-
ered to be of great ecological and cultural import-
ance because they contribute to the pollination of
flowering plants, many of them crops (Heard, 1999;
Klein et al., 2007), and because many stingless spe-
cies have been traditionally managed for honey and
other products (Jones, 2013; Nates-Parra & Rosso-
London ~o, 2013). Given the current pollination crisis,
in which declines in bee populations have been
increasingly reported worldwide, mostly linked to
human activities (Kremen et al., 2002; Potts et al.,
2010; Samejima et al., 2004), the study of their
role within the socio-ecological system is of
great relevance.
Beekeeping with stingless bees (referred here as
stingless beekeeping or as meliponiculture) is still
practiced and is considered culturally and economic-
ally important in many rural areas of the world (Vit
et al., 2013). The legacy of ancient management in
today’s beekeeping has been documented for
et al., 2006; Falchetti & Nates-Parra, 2002; Jones,
2013; Posey, 1983). Over the past two decades,
increasing attention has been given to documenting
stingless beekeeping (Vit et al., 2013), as well as
understanding local ecological knowledge in relation
to maintaining biodiversity while promoting sustain-
able management of natural resources (Go mez-
Baggethun et al., 2013).
Stingless beekeeping is currently a productive
activity considered part of the regional biocultural
diversity, understood as the existing variety exhib-
ited by the natural and cultural spheres and their
interconnections (Loh & Harmon, 2005; Maffi, 2005).
It results from the cultural expressions that societies
have developed under certain conditions. For its
analysis, it is important to understand its relationship
with practices, knowledge and beliefs within socio-
ecological contexts. In many cases, biocultural diver-
sity can be meaningful for environmental planning
because traditional practices can represent alterna-
tives that can lead to the maintenance of sustainable
landscapes (Katsue & Yukihiro, 2011). As part of bio-
cultural diversity, local ecological knowledge (LEK)

CONTACT Luciana Porter-Bolland luciana.porter@inecol.mx

ß 2021 International Bee Research Association
2 S. R. SIMMS AND L. PORTER-BOLLAND
implies the embodied knowledge systems that are
reproduced in the everyday behavior and language
of societies. It refers to information for the use of
plants and animals, the management and transform-
ation of landscapes, and the understanding and cat-
egorization of the world (Berkes et al., 2000).
Stingless beekeeping in different regions diverge
in its practices, depending on the particularities of
the bee species managed, as well as their socio-eco-
logical context, which also changes over time
(Cortopassi-Laurino et al., 2006; Souza, 2008). In gen-
eral, stingless bees are used either by locating nests
in tree trunks from which honey is extracted or by
managing colonies in boxes, jars, bamboo pieces,
hollow logs or other means (Arce et al., 1994; Vit
et al., 2013). It is difficult to summarize the practices
since each society has a different way of approach-
ing it, including types of management and purposes.
Aboriginal people in Australia, for example, have
managed stingless bee species, termed karbi
(Trigona carbonaria) and kootchar (Austroplebeia aus-
tralis), for at least three centuries and their manage-
ment practices have now been modernized through
technical innovation (Halcroft et al., 2013). In rural
areas of Costa Rica, mostly in the Pacific coast, 20
different species are managed, being jicote gato
(Melipona beecheii) and mariola (Tetragonisca angus-
tula) the most important ones (Herrera &
Aguilar, 2011).
In Mexico, there is evidence that beekeeping has
been important since pre-Columbian times
(Villanueva Gutierrez & Colli Ucan, 2011). The nutri-
tional and medicinal values of products harvested
from stingless beehives have been and continue to
be the main objective of traditional beekeeping
(Cortopassi-Laurino et al., 2006). Although most of
the documentation on stingless beekeeping in
Mexico is related to the management of the Xunan-
Kab, the Mayan Royal bee (Melipona beecheii) in the
Yucatan Peninsula (Gonzalez-Acereto, 2012), other
areas have been and still are important for bee man-
agement since ancient times. Furthermore, at least
20 bee species are reported to be managed through-
out the country (Reyes-Gonzalez et al., 2016).
According to Reyes-Gonzalez et al. (2016), four large
areas of Mexico have been characterized by trad-
itional stingless beekeeping management, including
the Yucatan Peninsula, the Gulf of Mexico coast, the
Pacific coast between Sinaloa and Jalisco, and the
Balsas River Basin in Guerrero and Michoacan.
Traditional knowledge and management in these
areas are still present and honey and other bee
products are mostly used in traditional medicine and
marketed regionally.
In Veracruz, which is part of the Gulf coastal area,
there is evidence of stingless beekeeping in several
regions, particularly those with indigenous influence.
The latter includes the traditional stingless bee man-
agement of the Popoluca people in southern
Veracruz. A 1942 publication by George Foster, for
example, recounts the common presence of bee-
keeping in homes of that area since the early 1920s.
In the Totonacapan region, stingless bees are also
traditionally managed by the Totonaco people
(Garcıa-Flores et al., 2006). There are other areas of
Veracruz where stingless bee management is com-
mon, such as the municipality of Atzalan (Porter-
Bolland et al., 2015), where this research took place.
In this study, we describe the presence of trad-
itional stingless beekeeping at the municipality level
in Atzalan, Mexico, as part of the biocultural diversity
of Veracruz and the importance of the associated
local ecological knowledge (LEK) in that region. For
this, we identified the diversity of managed bee spe-
cies, LEK related to bee food resources, and types of
bee management practices. We also analyzed the
terminology locally used for the practice, categorize
local uses of bee products, and recognize percep-
tions of how beekeeping is changing, considering a
context of land use change. Our research was con-
ducted at the municipality level and did not sought
for gender or intergenerational differences. However,
identifying LEK components of meliponiculture and
the factors of change that are currently shaping this
knowledge at that level, can provide insights for the
development of strategies to achieve sustain-
able management.
Materials and methods
Study site
The municipality of Atzalan is located in the Nautla
river watershed. This territory in central Veracruz is
considered the beginning of the Totonacapan region
where people have inherited elements of the
Totonac and Nahuatl cultures (Morales-Lara, 2008).
The localities where the study took place are located
between the Bobos, San Pedro and Alseseca rivers.
The mountain system has a rugged geomorphology
with a range of elevations from 200 to 2000 masl
that provide diverse ecological conditions and differ-
ent microclimates, allowing the production of a var-
iety of crops and patches of different types of
vegetation (Morteo-Montiel et al., 2020; Porter-
Bolland et al., 2015). Actually, Atzalans landscape has
a configuration in which different land uses coexist,
including grasslands, cornfields, coffee crops, fruit
tree crops, secondary vegetation, and patches of
tropical forest, cloud forest and pine-oak forest
(Morteo-Montiel et al., 2020). In this context, sting-
less beekeeping is practiced in many of the house-
holds in the municipality (Porter-Bolland et al., 2015).

Figure 1. Atzalan municipality in Veracruz State, and its altitudinal zoning. Visiting localities were information was obtained is
shown in the map, as well as the state-level protected area Rio Filobobos y su Entorno.
This municipality can be divided into three
regional altitudinal zones for research purposes
(Morteo-Montiel et al., 2020). The zoning includes:
(1) Upper zone at 1201 to 2000 masl; (2) Middle
zone at 601 to 1200 masl; and (3) Lower zone at 200
to 600 masl. Fruit tree plantations, such as citrus,
predominate the Lower zone, which has a warm and
humid weather with rainfall throughout the year.
Coffee agroforestry systems dominate the landscape
in the Middle zone but are gradually being replaced
by banana and citrus plantations. This zone has a
semi-warm and humid weather with rainfall through-
out the year. Forestry, coffee and grasslands for rear-
ing cattle are the productive activities that shape the
Upper zone that has a humid temperate climate
with rainfall throughout the year. The remnants of
native vegetation are mainly found in areas situated
in the Middle and Upper zones. This gradient pro-
vides an average temperature range in the munici-
pality of 12
to 26
C and an average annual
precipitation range of 1900 to 2600 mm (Instituto
Nacional de Estadıstica Geografıa e Informatica
(INEGI), 2010; Instituto Nacional para el Federalismo
y el Desarrollo Municipal (INAFED), 2013; Morteo-
Montiel et al., 2020). Atzalan has a large State level
protected area (“Rio Filobobos y su Entorno”) and is
considered a priority region due to the presence of
certain plant communities that are relics from the
Pleistocene (Arriaga-Cabrera et al., 2000).
Atzalan is one of the 212 municipalities in the
state of Veracruz, with a population of 48,397 inhabi-
tants living in 190 localities (Consejo Nacional de
Poblacion (CONAPO), 2010). It is considered to have
JOURNAL OF APICULTURAL RESEARCH 3
a high degree of marginalization, since 77% of its
localities are categorized as such (CONAPO, 2010;
SEDESOL, 2013). Biophysical differences in terms of
climate and soil conditions, access to infrastructure,
historical processes and attachment to traditional
activities have led to the implementation of different
activity systems within the municipality. However, in
general, most economic activities relate to the pro-
ductive sector and up to 70% of the population
practices a combination of agricultural and agrofor-
estry activities (Morteo-Montiel et al., 2020). Atzalan
is considered a municipality with a beekeeping trad-
ition due to the high presence of families dedicated
to the management of stingless bees (Porter-Bolland
et al., 2015).
Data collection
Previous research (Porter-Bolland et al., 2015) facili-
tated contact with beekeepers. The data reported in
this study was conducted during 2014 (Simms,
2016), when 65 settlements were visited (Figure 1)
and a sample of 156 beekeepers, each representing
members of a household practicing stingless bee-
keeping, was selected to provide information. Of
these, 54 were women and 102 were men. These
beekeepers were distributed throughout altitudinal
zones, although most were located in the Middle
zone (summing up to 48%; while only 23% in the
Lower zone and 29% in the Upper zone), because
this is where most beekeepers in the municipality
are located. Sixty three percent of our informants
were under 45 years old and 37% were older.
4 S. R. SIMMS AND L. PORTER-BOLLAND
Table 1. Managed bee species in Atzalan in 156 beekeeping units.
Common name Scientific name
Negrita, colmenita Scaptotrigona mexicana Guerin-Meneville
Cenicilla, mosquito, abeja real Nannotrigona perilampoides Cresson
Tenchalita, bichito Plebeia frontalis Friese
Tenchalita, gabacha Plebeia pulchra Ayala
Chivillo, chivo Partamona biliniata Say
Limoncillo Lestrimelita niikib Ayala
Abeja real o melipona Melipona beechii Bennett
They are listed in order of importance, indicating common and scientific names.
However, almost half of our informants had been
practicing beekeeping for more than 15 years (46%)
and the rest had only been practicing for a few years
or were new at it. We used methods that had been
shown to be useful in similar studies to obtain infor-
mation regarding LEK, including participatory obser-
vation, open and semi-structured interviews,
structured interviews, transect walks and free listings
(Costa-Neto, 2000; Newing, 2013).
Of the 156 beekeepers in our sample, 32 were
selected for an in-depth ethnographic study. This
qualitative part of the research implicated participa-
tory observation and open interviews to inquire
about cultural aspects related to beekeeping, local
ecological knowledge regarding bee colonies and
bee-plant interactions, formal and informal learning
about the activity, local uses of bee products, and
landscape and social change perceptions. For the
remaining 124 beekeepers, structured and semi-
structured interviews and free lists were conducted.
Free-listing were conducted in order to register
the most important plants that beekeepers should
be used by bees. These were carried out together
with studies of the ethno-ecological landscape
(Hunn & Meilleur, 2010), which consisted of 500 m
walks near beekeepers’ productive units. In these
walks, unidentified plant species were collected and
brought to the lab for scientific identification by a
botanist. Semi-structured interviews were used to
obtain specific information on LEK in relation to bee-
keeping, focusing on biocultural indicators (Maffi,
2005; Harmon & Loh, 2004). Topics of this interview
included: diversity of managed bee species, diversity
regarding beekeeping language (terms used for spe-
cies, behavior, structures, and harvested products
from beehives), types of bee management, cultural
use of harvested products of beehives, knowledge
related to bee resources to produce nectar, pollen
and resins, and perceptions regarding land use
change processes and beekeeping practices. At the
same time as this work was being undertaken, we
conducted a study of land use change using satellite
images and local perceptions of land use change
(Morteo-Montiel, 2016; Morteo-Montiel et al., 2020;
Simms, 2016). However, this information is also
insightful for the purpose of what we report here.
Previous work (Porter-Bolland et al., 2015) carried
% of total beehives registered in the sample
(n ¼ 1217 as the total number of beehives)
49 (596)
24.6 (297) mostly in the Upper zone
13.3 (162)
11.4 (139)
1.0 (12)
0.8 (10)
0.08 (1)
out in the area has led to the scientific identification
of Meliponini species managed in the area.
Results
Diversity of managed bees
According to our informants and observations, up to
seven stingless bee species can be kept in the same
beekeeping unit (Table 1). However, the most com-
mon bee species was Scaptotrigona mexicana, locally
called negrita. Actually in Atzalan, most of the honey
production comes from S. mexicana, although
Nannotrigona perilampoides, Plebeia pulchra, and
Plebeia frontalis, can also be found in beekeeping
units. Practically all beekeepers, except those in the
colder areas at the Upper zone, handle mainly S.
mexicana. According to 77% of the informants, this
bee species is very well suited to al almost all wea-
ther conditions. Although its food sources have pre-
sumably changed or decreased due to land-use
change pressures (Morteo-Montiel, 2016), wild popu-
lations of negrita were reported by 83% of inform-
ants as common. Very few cases of death from
disease were reported. Cases of death through poi-
soning from agrochemicals was also seldomly
reported, although beekeepers indicated that banana
plantations (a land use that is becoming more prom-
inent in the landscape) were not suited for bee for-
aging due to agrichemical use. Cases of mass
mortality in the past were reported by producers liv-
ing in locations above 800 masl, when, in the late
1990s, a decrease in temperature caused a frost that
affected many species of plants and animals, includ-
ing bees.
The least present stingless bee species was the
“royal bee” or Melipona beecheii and was only found
in one beekeeping unit located in the Lower zone of
the municipality. The beehive owner reported that
this bee species is difficult to manage and that its
nests in the wild were easier to find at higher eleva-
tions (specifically the transition of the Middle to the
Upper zone). M. beecheii is acknowledged by local
producers to be vulnerable to land use change, par-
ticularly to agricultural intensification and the associ-
ated agrochemical use. However, we registered three

Figure 2. Percentage of beekeeping units with different
configurations of managed bee species.
wild colonies of M. beecheii in transect walks in the
transition from the Middle to the Upper zone.
Two species of Plebeia spp. (P. pulchra and P. fron-
talis) were found both in the wild and in beekeeping
units, especially in warmer areas. There may be more
species in the wild, but this was not confirmed. N.
perilampoides is highly appreciated by beekeepers,
despite its size (half of negrita), since it is considered
to be hardworking and able to withstand colder
weather conditions. Beekeepers reported that the
internal structures of the nest allow bees to control
humidity and temperature. In fact, N. perilampoides
were mostly kept in beekeeping units located above
1700 masl, an area where 100% of the beekeepers
managed this species. Bees called chivillo (Partamona
bilineata) and limoncillo (Lestrimelitta niikib) are
known by most producers and are common in the
wild, although seldomly kept in beekeeping units.
Limoncillo is a robber bee that steals honey and
other resources from other bees and chivillo has
habits that make it unsuitable for use. However, a
few beekeepers tolerate one or both of these bee
species in their productive units (only 2%).
The number of bee species found in each bee-
keeping unit can vary from one up to seven,
although usually the number of species present in a
production unit range from 3 to 5. Fifty-two percent
of all beekeeping units kept only S. mexicana, 25%
managed S. mexicana and the two Plebeia species
(frontalis and pulchra), 11% S. mexicana, the two
Plebeia species, and N. perilampoides, and 12% man-
aged only N. perilampoides (corresponding to pro-
ducers in the Upper zone; Figure 2). Even though
several bee species are kept in the same productive
unit, only a part of the households in the Upper and
Middle zones indicated that honey is stored accord-
ing to its entomological origin. However, only 7% of
the beekeepers, those with greater experience and
generally older, specified to separate honey accord-
ing to species. For example, honey produced from N.
perilampoides is thought to be better for treating
JOURNAL OF APICULTURAL RESEARCH 5
certain ailments such as vision problems and gastro-
intestinal infections. Local demand for differentiated
honeys comes from traditional healers. However,
because Nanotrigona and Plebeia species produce so
little honey, it is most often mixed with that of
Scaptotrigona.
Local knowledge regarding foraging resources
for bees
Beekeeping units are kept within the household lim-
its, sharing spaces with the family. It is commonly
reported that cultivated garden flowers are good
sources of nectar and pollen for bees. These plant
species include both native and exotic plants.
Actually, 21% of the plant species mentioned were
species found in orchards and home gardens, includ-
ing both local and introduced plants.
Native vegetation has a different configuration in
each altitudinal zone, so beekeepers mentioned dif-
ferent species of plants as important according to
the corresponding types of vegetation: tropical forest
in the Lower zone, cloud forest in the Middle zone
and cloud forests and pine-oak forests in the Upper
zone. Productive systems also shape the landscape
configuration as well as resources availability for
bees, including subsistence agriculture such as
homegardens and milpa, agroforestry systems and
intensive agriculture (monocrops: fruit trees, sugar
cane, banana, pine, grasses, etc.). It was mentioned
in all altitudinal zones that, in special situations, bees
are fed artificially by placing containers with honey,
molasses or sugar near or inside beehives. The rea-
sons reported for artificial feeding are food short-
ages, abrupt changes in weather conditions,
weakening of beehives, transfer, and division con-
ducted in autumn-winter, attack by other bees,
among others.
Through free listings and ethno-ecological sur-
veys, interviewers listed approximately 110 plant
species important to bees. Here we list only the
most mentioned species ranked according to free
listings at each altitudinal zone. In the lower zone,
the most mentioned species was the orange tree
(Citrus sinensis; 74.1% of interviewers mentioned it),
which is directly related to the importance of local
production of citrus and other fruit trees in this area,
such as lemon (Citrus latifolia), tangerine (Citrus retic-
ulata), and lychee (Litchi chinensis). The second plant
species mentioned was the mozote (70.4%), which
includes two ruderal annual herb species: Bidens
alba and Sclerocarpus uniserialis, that bloom in the
fallows of milpas or cornfields in October and
November. The third species mentioned was the
Spanish cedar (Cedrela odorata; 66.7%), a native tree
species of economic importance. Also, commonly
6 S. R. SIMMS AND L. PORTER-BOLLAND
mentioned were the following herb species: duraz-
nillo (Cestrum sp; 63%), acahualera (that include sev-
eral species: Simsia amplexicaulis, Tithonia tubiformis,
Melampodium divaricatum, Paspalum distichum;
59.3%); which are all ruderal plants. The exotic basil,
Ocimum basilicum, was also frequently men-
tioned (55.6%).
In the Middle zone, cachichın (Oecopetalum mexi-
canum; 34.3%), a native tree species was the most
mentioned, followed by coffee (Coffea arabica;
31.4%), reflecting the tradition of growing this com-
mercial crop in the region. It was followed by
Allspice (Pimenta dioica; 25.7%), which is an econom-
ically important native tree used for its seeds, bark
and wood, and chaca (Bursera simaruba; 22.9%), also
a native tree that is frequent and often planted as
living fences. Orange trees (C. sinensis; 22.8%) were
also mentioned by beekeepers located in the transi-
tion between the Lower and Middle zones. Banana
(Musa paradisiaca; 21.4%) was also considered
important, a monocrop that is gradually displacing
traditional coffee polycultures in most of the munici-
pality (Morteo-Montiel, 2016; Morteo-Montiel
et al., 2020).
In the Upper zone, the most mentioned and
important plant for bees was coffee (45%), followed
by pine (Pinus sp.; 42.5%), which is important for
making beehive boxes. In this area there are many
pine plantations and there may also include other
forestry species such as oaks (Quercus sp.), also men-
tioned as important for bees (31.7%), as well as iqui-
mite (Erythrina americana; 7.5%). Species like
islahuate (Saurauria sp.; 13.3%), and marangola
(Clethra sp.; 14.2%) were also considered in the list.
Of all plant species considered important to sting-
less bees, mozote species (Bidens alba and
Sclerocarpus uniserialis) were the most mentioned in
general (57.3%). Coffee (C. arabica; 46.4%) ranked
second, reflecting the region’s coffee tradition. Chaca
(Bursera simaruba; 44.1%), present in native vegeta-
tion patches and live fences, occupied third place.
Although all land uses favor the growth of plants
visited by bees (excepts in the few areas where there
are pasturelands), land use change is becoming det-
rimental for beekeeping, either because diversity of
floral resources is being diminished (for example
through replacing coffee agroforestry systems by
banana plantation) or because the use of agrochemi-
cals is becoming more prominent (for example in
banana plantation).
Beekeeping LEK: types of bee management
There was no distinction regarding gender or altitud-
inal zone for the distribution of experience and
knowledge in our sample. Throughout the
municipality, the most experienced beekeepers (at
least half of our informants and the most advanced
in age), shared bee management practices grounded
on local knowledge that had been passed down
through generations. The younger beekeepers are
newer in the practice but have usually acquired their
knowledge from their parents or other family mem-
bers (at least 62% of our beekeeping sample). It is
important to make the observation that the bee-
keeping practice at Atzalan is generally a familiar
one, in which most family members, be it the man
or the women, including children, participate one
way or another, becoming a way of learning by
doing since early ages. A smaller portion of our bee-
keeping sample, usually young producers also, have
recently started the activity through external aid that
has implicated training and equipment (i.e., modern
boxes for keeping bee nests). Given the above, we
identified three types of stingless beekeeping
depending on technology and associated practices:
1. Local management: This is the most traditional
type of management, in which beehive boxes
have large dimensions, averaging 45 cm wide,
28 cm high, and 30 cm deep, allowing hands to
be introduced into the nest for handling when
dividing or harvesting. Once the beehive is har-
vested, honey pots are squeezed, and honey is
filtered two or three times. Pollen and cerumen
pots are sometimes separated and mostly con-
sumed by the family. Beekeepers are also able
to handle the nest for divisions. Elderly beekeep-
ers reported that sometimes their grandparents
used bigger boxes but more commonly bees
were kept in hollow logs or bamboos, where
the hives were originally brought from the for-
est. Almost all beekeepers harvest once a year
and only a few beekeepers reported to harvest
two times a year. Most beekeepers (67%) that
were interviewed practiced local beekeeping.
2. Modern (technified) bee management: Refers to
beekeeping based on technology developed for
easier handling, quality production and higher
yields. Technified hive boxes are smaller but
elongated in a vertical direction, with the pur-
pose of separating the nest from the production
chamber. To harvest honey, beekeepers pinch
the honey pots and turn them over, so the
honey is leaked into a filter. This leaking tech-
nique separates better the honey from the pol-
len, but wax is not harvested. Some beekeepers
with this type of management reported using
syringes to extract honey and other equipment.
Only 8% of beekeepers interviewed are limited
to modern beekeeping, and almost all of them
have recently become beekeepers and have
 JOURNAL OF APICULTURAL RESEARCH 7

Table 2. Local terminology for addressing managed bee species, including casts, structures, and products derived
from beekeeping.
Category Common name Entomological or ecological translation
Bees Negrita (little black) Scaptotrigona mexicana
Cenicita/cenicilla (small ash) Nanotrigona perilampoides
Mosquito (little fly) Nanotrigona perilampoides
Tenchalita Plebeia pulchra
Tenchalita/gabacha/tanchalita Plebeia frontalis
Colmena real (royal hive) Melipona beecheii or Scaptotrigona mexicana
Abeja real (royal bee) Melipona beecheii or Nanotrigona perilampoides
Limoncillo (little lemon) Partamona bilineata
Chivillo (little goat) Liestromelita niikib
Casts Guardianas (guardian or keepers) Guardian worker
Chambeadoras (workers) Foraging worker
Recolectoras (collectors) Foraging worker
Reina (queen) Productive queen bee
Reina virgen (virgin queen) Virgin queen bee
Palidas/nodrizas (pale/nurse) Laying workers
Huevos (eggs) Brood cells
Huevo lıquido (liquid egg) Larvae
Zanganos Drones
Structures Trompeta (trumpet) Entrance
Mun ~ecos (dolls) Set of storage pots
Potes (pots)/cantaros (jars) Storage pots
Discos (discs)/tortitas (cakes) Brood chamber
Camisa, ropa o vestido de nido (shirt, cloth or nest dress) Cerumen/batumen plate
Products Miel virgen (virgin honey)/miel puerca (brown honey)/miel Stingless bee honey
de monte (mountain honey)
Flor (flower)/polen (pollen) Pollen
Tacahuite Propolis
Cera (wax)/cera puerca (brown wax) Cerumen
Cera fina (fine wax) Cerumen/batumen plate

attended training. Honey is produced mainly for
its commercialization.
3. Mixed management: Refers to a mixture of local
and modern beekeeping and beekeepers can
perform local beekeeping along with modern
currently available techniques. About 25% of the
interviewees conducted mixed management.
These are beekeepers that are experimenting
and in most cases have been subject of external
training courses.
LEK registered in language
In general, all managed species are locally well iden-
tified by all beekeepers (probably except for the
newly forming producers) and have culturally
assigned names for their behavior and anatomy.
Geographical discrepancies in names were common.
For instance, beekeepers in the Middle and Lower
zones used the name “royal bee” in reference to M.
beecheii, however, in the Upper zone settlements
(above 1200 masl), producers used the same name
in reference to S. mexicana or N. perilampoides. Many
beekeepers from higher elevations mentioned that
M. beecheii is still found in the trees of the forest
and remember the elder talking about its medicinal
properties and its importance.
Table 2 shows a list of local names used in bee-
keeping, including terms used to refer to bees and
their structures, functions, division of labor and prod-
ucts. We generalize this knowledge for summarizing
purposes, although there may be differences in the
knowledge each family has throughout the munici-
pality. In general terms, LEK comes from an empirical
background acquired through oral transmission and
observation as part of a trial and error learning pro-
cess over time, including also more recent informa-
tion received through training. LEK regarding species
and their behavior can be associated with entomo-
logical and ecological terms. LEK through time
adopts new techniques and information, and at the
same time traditional knowledge systems brawls for
its maintenance.
We can generalize that local beekeepers differen-
tiate bee species and identify cast division within the
hive. They are also aware of the nest structure. Apart
from the common names, local beekeepers have
adopted technical terms through training. The most
recognized workers are called guardians and have
the function of protecting the nest entrance. There
may be one or more gatekeepers depending on the
species, but all of them are usually designated as
guardianas, soldados, guaruras and chismosas (care-
takers, soldiers, bodyguards, and gossipers). Foraging
workers are the motive of great moments shared by
beekeepers and their families. They are recognized
as responsible for finding and bringing the food to
the nest. “We ask each other how far they go, and
how soon will they travel back … I love to see how
they come back with stuffed paws with colored balls;
it is their food. I remember when I was a little girl, I
worried about them too much and prayed to God to
8 S. R. SIMMS AND L. PORTER-BOLLAND
help them find their way back.”1 They are called
chambeadoras or workers, foragers, and courageous.
It is recognized that these workers have structures
on their back legs (corbiculae) called bolsas, cucha-
ras, guardas, or escondites (bags, spoons, guards, cov-
ers, or hideouts).
For many beekeepers, observing the foragers
means a moment of relaxation and even introspec-
tion. Some beekeepers mentioned that they have
found the solution to their ailments through proc-
esses of concentration and meditation while observ-
ing these forage bees and their hard work bringing
food to the hive. They consider beekeeping as a
type of therapy for alcohol problems, addictions,
depression, anxiety, hypertension, and stress control.
It is reported as a medicine for the soul. “ … and
suddenly I was old and alone in life, my children all
married, my wife with God and here I was drinking
and crying … Spending time with my hives, these
gusanitos (little worms) gave value to life and now I
want to spend every resting time looking or talking to
them … ”
Another well-recognized caste is the laying
€erita or pale, and their job is to
worker. It is called gu
take care of the nest and feed the newcomer larvae.
The queen or queens are important individuals, and
everyone knows of their existence although it is
accepted that it is difficult to recognize them if they
are not fertilized queens. Some beekeepers recog-
nize them because they are slightly larger than the
workers and have brown lines on the abdomen.
Once fertilized, the abdomen expands so lines
appear in various shades of brown and yellow, and
are usually found among the brood.
The congregation of bees is well identified, since
it is very evident during the mating season.
However, it is rare for beekeepers and their families
to know that the bee congregation is conducted for
males to fertilize the queen and it is common to
believe that congregations outside the beehives
occur due to the high temperatures reached during
spring days. Some people have recently received this
information through training courses.
The entrance of negrita (S. mexicana) is called
trompeta (trumpet) and is made with resins and mud
forming a tunnel to access inside the nest.
Sometimes they are also called pistas, estrellas, hue-
cos, or tuneles (tracks, stars, trenches, and tunnels),
depending on the shape of the entrance, which is
also significant in distinguishing between bee spe-
cies. Nest structures formed by the brood cells are
called tortas, pasteles, or discos (pancakes, cakes, or
disks) and are recognized as the place where brood
is located. In some cases, beekeepers clearly identify
the royal cells located on the edges of the brood
chamber with slightly bigger dimensions than
the others.
Current beekeeping and perceptions of change
Beekeeping is a traditional activity in Atzalan that is
important on a cultural level and can have important
economic value as well. According to several inform-
ants, harvesting beehives from native forests in the
past was an activity conducted along with a ritual to
cherish the Mount deity (Sen ~ or Del Monte). The bee-
keeper’s grandparents, also beekeepers, performed
this ritual when entering the forest to harvest honey
and to extract beehives. The ritual included prayers
and offerings, including bee products. Nowadays,
before harvesting products from the hives or extract-
ing beehives from the forests, some offerings are
made to Virgin Guadalupe, Jesus, or other Catholic
saints such as San Florentino.
Like their ancestors, beekeepers of Atzalan make
extensive use of honey and propolis, and mostly for
its medicinal properties. Honey is considered a warm
element that can contribute to soothing body parts.
For example, honey is used as a remedy to keep the
pelvic cavity warm and to avoid pain in treatments
for body alignment after childbirth. It is also used for
its healing properties in injuries such as superficial
cuts and burns. The main use of propolis is to treat
internal wounds. Also, wax is still harvested by some
beekeepers that make candles for family mortuary
rituals and on the national festivity of the day of the
death, celebrated every year from October 31st to
November 2nd. The diversity of local medical practi-
ces using beehive products is being documented
elsewhere (Simms, 2016).
Although the medical importance of stingless
beekeeping is still present among the population of
Atzalan, many changes are occurring that affect the
activity. The recent demand for stingless bee honey
is currently developing a regional market that exerts
an opportunity to beekeepers, and therefore sting-
less beekeeping has been increasingly adopted by a
larger part of Atzalan’s population. Locally, the
demand for pollen, propolis and wax is increasing,
along with honey. This phenomenon is caused by
technical and scientific information that is now avail-
able through training courses and regional work-
shops of external aid (both governmental and non-
governmental). This training is helping beekeepers
to adopt modern technics that can lead them to be
more productive. Under these new conditions, and
mostly driven by the market, beekeepers’ LEK is
being enrichened and sometimes replaced by mod-
ern information, resulting in several households
developing modern beekeeping.

As a consequence of the above, while in the past,
having only a few beehives was enough for the fam-
ily’s consumption, today honey production is becom-
ing important for monetary gains. This has resulted
not only in more families producing honey but also
in more beehives being kept by families. For
example, while formerly households usually kept a
few beehives, perhaps 3 or 5, today beekeepers
have an average of 15 beehives, 15% of those inter-
viewed had over 30, and 8% more than 80 (a few up
to 200). On average, one beehive of S. mexicana may
produce from 0.5 to 1.5 liters of honey per year, and
when sold, the price ranges from $400 to $1000
Mexican Pesos per liter, depending on where and to
whom it is sold.
Nevertheless, there is no scientific information
regarding the capacity of the environment for sup-
porting a growing expansion of honey production
while at the same time land use intensification is
expanding. Eldest beekeepers reported that ten or
fifteen years ago harvesting implied up to two liters
of honey per year, arguing that the reduction in
native forests through land use change is affecting
the activity. Among current changes stands transfor-
mations in productive systems that modify land-
scapes (Morteo-Montiel, 2016), representing a
challenge for beekeeping as production can be com-
promised by diminishing floral resources while
monocrops and industrial agriculture homogenize
the landscape (Morteo-Montiel et al., 2020). In
Morteo-Montiel et al. (2020), through a land use
change study we conducted using satellite images,
we report that between 2002 and 2014, forest cover
declined in the municipality of Atzalan (in the upper
zone from 62.5% to 60.9%, in the middle zone from
57.3% to 39.2%, and in the lower zone from 24.3%
to 21.7%). At the same, banana and citrus monocul-
tures and also pastures, increased in land use covers.
Beekeepers, particularly the older and more expe-
rienced, are aware of the accelerated land use
change towards monocrops that is eroding food and
nesting sources for bees and consider it a threat to
productivity. They are also concerned about agro-
chemical use in certain productive systems such as
in banana plantations. Younger producers aiming for
honey commercialization are less aware of the eco-
logical connections of land use change and product-
ivity. However, there are efforts in the area of some
organized beekeepers (old and young) that are
becoming involved in enrichment planting activities
and have had experiences established nurseries for
the reproduction of plant species that can enhance
different areas in the landscape.
Deforestation and intensive agricultural systems
that employ agrochemicals, along with extracting
beehives from the wild to increase productive units
JOURNAL OF APICULTURAL RESEARCH 9
as part of the boom of honey production excerpted
by market demand, may be a threat to wild bee
populations. Other factors affecting the use of wild
populations are the fact that chainsaw and other
tools, as well as vehicles and paved roads, have
facilitated the extraction of beehives from the forests
or their acquisition in other regions. However, fortu-
nately, beehives division to increase productive units
is currently being spread among beekeepers. Hive
division is a technique that is reflecting a productive
trend for local beekeeping since traditionally only
the most experienced beekeepers used to practice it.
Discussion
Stingless beekeeping is an important part of the bio-
cultural diversity of Atzalan’s landscapes. Contrary to
the general tendency of decreasing importance of
this activity in different parts of Mexico, where it has
been claimed to be “on the verge of disappearing”
(Quezada-Euan et al., 2001), native beekeeping for
Atzalan’s families, seems to be flourishing. Also, and
despite the general deterioration of the forested
landscape because of the intensification of agricul-
tural practices (Morteo-Montiel et al., 2020), and the
claim, particularly from the older more experienced
beekeepers that deforestation reduces honey yields,
the number of beekeeping seems to be growing.
Younger people, driven by a market demand, are
expanding their efforts towards honey production
but may not necessarily be aware of the possible
negative effects on yields that land use intensifica-
tion may excerpt. Nonetheless, there are organized
groups of beekeepers that are becoming involved in
nursery activities for enrichment planting, aware of
the intrinsic relation of production and lan-
scape quality.
The names beekeepers provide to species, struc-
tures, characteristics and behavioral aspects of bees
show the depth of LEK that some beekeepers have
acquired over time and through current training. Oral
knowledge transmission represents an important indi-
cator of biocultural diversity that at Atzalan prevails in
some families (Gonzalez-Acereto, 2012; Zamudio &
Hilgert, 2012). LEK on important bee pollen sources
refers to different available resources for bees between
altitudinal zones due to diverse climatic conditions.
We found that many beekeepers recognize both culti-
vated plants and native vegetation as important
resources for bees. Home garden plants important for
beekeeping are usually fruit trees or ornamental
plants, as well as some aromatics and edible plants.
Coffee orchards represent diversified agroforestry sys-
tems with important resources that contribute greatly
as pollen sources for bees that include timber and
edible plants or that are important for other cultural
10 S. R. SIMMS AND L. PORTER-BOLLAND
uses. This knowledge referring to local nectar and pol-
len sources for bees is relevant when establishing
enrichment planting in different types of landscapes,
and some beekeepers are already working on this as a
beekeeping productive strategy (Porter-Bolland
et al., 2015).
LEK on the use of native bees reflects a cultural
heritage with historical roots. Other studies have
already proven that local medicinal uses of honey,
propolis, cerumen, and pollen represent an under-
standing of their properties, manifested in the ways
there are used (Gonzalez-Acereto, 2012; Reyes-
Gonzalez et al., 2014). Honey and propolis in Atzalan
were sometimes used in mixtures with medicinal
plants to make remedies for particular ailments. It is
known that complex remedies that use local ingre-
dients, usually have a historical territorial develop-
ment (Lo pez Austin, 1984). However, changes in the
aims of production from self-consumption towards
commercialization, particularly from the part of
younger producers, may be changing aspects of LEK.
Overall, migration and globalization processes are
pushing this traditional activity of stingless beekeep-
ing into a productive trend that could have serious
cultural and biological consequences locally. Local
perceptions and external inputs are heading to the
modernization of meliponiculture, where the ten-
dency is to expand in the number of colonies and
beekeepers, yet, at the same time, vegetation cover
diminishes given the accelerated land use change
into intensified agricultural systems that are reducing
native forest and traditional agroforestry systems
(Ellis et al., 2010; Morteo-Montiel et al., 2020), a con-
dition that forces the limits of ecological integrity
and could make it difficult to sustain in the long run
(FAO, 2011). Nowadays, deforestation and the conse-
quent loss of natural and semi-natural habitats is
one of the most important causes for the decline of
biodiversity and key species, such as native bees
(Fahrig, 2003; Foley et al., 2005; Kevan & Imperatriz-
Fonseca, 2002). Current pollinators crisis should
define governmental and non-governmental pro-
grams in regions where beekeeping has been trad-
itionally practiced, allowing this biocultural activity
to act as a tool to achieve sustainable landscapes
(Klein et al., 2003; Kremen et al., 2007).
Atzalan is considered a priority region for conser-
vation (Arriaga-Cabrera et al., 2000), but economic
development is driving transformation processes in
which the establishment of monocrops is gradually
shaping the landscapes (Morteo-Montiel et al., 2020).
The implementation of potentially important eco-
nomic activities, such as stingless beekeeping and
diverse agroforestry systems could be seen as a
means to provide livelihood strategies in line with
conservation, helping to guide local conservation
efforts such as the state-managed reserve named Rio
Filobobos y su Entorno. We consider that the role of
governmental and non-governmental institutions
could be key in promoting an integrated manage-
ment planning approach (Parson, 1995) in which
development efforts could be tuned using a multi-
functional landscape perspective (Ros-Cuellar et al.,
2019). The role of enrichment planting for this effort
could be a tool for landscape sustainability
(Mangueira et al., 2019). Local landscapes are at a
breaking point where inappropriate management
decisions could lead to land use simplification and
deforestation, resulting in loss of diversity at the
landscape level and life quality impoverishment
(Morteo-Montiel et al., 2020; Porter-Bolland et al.,
2015). Beekeeping is part of the biocultural diversity
of Atzalan’s landscapes and should be geared
towards sustainable local strategies for natural
resource management (Villanueva Gutierrez & Colli
Ucan, 2011).
Conclusions
The configuration of managed bee species in bee-
keepers’ units revealed slight differences throughout
the altitudinal range that goes from 200 to 2000
masl. The latter shows the distributional patterns of
managed stingless bee species, which may be useful
for understanding local distribution of these insects
and establish guidelines for future studies.
Sustainable strategies should encourage beekeepers
to manage biodiversity (vegetation diversity as well
as bee diversity). Species like M. beechei and its asso-
ciated LEK, for example, vulnerable to land use
change, could be recovered as a managed species,
since it is a known species to beekeepers but has
been disappearing from management units.
All in all, and provided the important LEK still pre-
vailing in the area and a legacy of traditional sound
landscape management that is now changing given
external forces, future studies should encourage col-
laborative work with beekeepers in order to face
some of the threats identified for the activity
(intensification of the market for bee products,
monocropping intensification, etc.). Future studies
should also consider differences in perceptions and
LEK regarding altitudinal distribution as well as gen-
der and integrational differences, which could pro-
vide a wider understanding of the changes occurring
at the municipality level.
Capacity development built on previous local
experiences as well as on LEK, could aim at raising
awareness throughout the municipality of the
importance of having rich and diverse landscapes. A
multifunctional landscape approach could lead to
the implementation of efforts for plant propagation

and enrichment planting aiming at enhancing local
landscapes with melliferous plant species favoring
stingless beekeeping. That would need coordination
with the environmental sector for pushing towards
integral landscape planning, considering the conser-
vation importance in the area. Beekeeping with
stingless bees in Atzalan, an evolving and complex
system, represents a robust knowledge system that
is constantly changing. Future challenges given by
land use change, call for integral landscape planning,
aiming towards sustainability and the persistence of
beekeeping with stingless bees.
Acknowledgements
We are grateful to the producers of Atzalan for their sup-
port in the field and their valuable contribution to this
project. Special thanks to Claudia Gallardo Hernandez,
Ricardo Quiroz Reyes, Fortunato Ruiz de la Merced, Estrella
Chevez Martın del Campo, Swany Morteo Montiel, and
Martha Bonilla Moheno for valuable assistance in the field
and in the laboratory. Particular thanks to Swany Morteo
for the aid in making the maps.
Disclosure statement
No potential conflict of interest was reported by
the authors.
Note
1. Conversation with Marıa Barreda Herrera from El
Progreso, March 2014
Funding
Scholarship support for the first author was provided by
the Consejo Nacional de Ciencia y Tecnologıa (CONACYT;
scholarship No. 299745), and the Instituto de Ecologıa, A.C.
This work was partially supported by the Comisio n
Nacional para el Conocimiento y el Uso de la Biodiversidad
(CONABIO; B1812/NE010/16), and the US Fish and Wildlife
Service – Wildlife Without Borders/Mexico (Award
#F13AP00263 and Award #F15AP00270).
ORCID
Luciana Porter-Bolland http://orcid.org/0000-0001-
8586-3267
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