Stingless bee survey and identification

During the field trips, a total of 36 individuals were collected using the different sampling methods. Twelve morphospecies of stingless bees were identified, which belonged to 8 genera (Lestrimelitta, Melipona, Paratrigona, Plebeia, Scaptotrigona, Scaura, Tetragonisca, and Trigona), with Plebeia being the most abundant species (Table 1).

Table 1 Number of stingless bee species (n) collected and identify to genera in the municipality of Muyupampa, Bolivia

It was confirmed that the sampling effort was adequate since high values (94.88%) of completeness of the sample were reached. For q = 0, it was estimated a species richness of 13 species, only one more species than observed (Fig. 4a). As for the exponential of the Shannon index (q = 1), an equivalent number of 10 equally common species was observed and 12 estimated (Fig. 4b).

Fig. 4

a Sample completeness curve. b Rarefaction and extrapolation curves of species diversity base on the Hill numbers q = 0 (species richness) and q = 1(exponential of the Shannon index). The bands of each curve correspond to the confidence intervals calculated by 95%

Local knowledge on stingless bees

The interviewees reported 15 different species of honey-producing bees with their local names (Table 2). Fourteen of them are stingless bees, and one is the Africanized honeybee (Apis mellifera), locally known as Abeja extranjera. Among the stingless bees, the most cited and valued species were Señorita which was mentioned by all interviewees, followed by Tancarillo and Negro. Other the species locally managed in the meliponaries were identified as Tetragonisca angustula, Melipona rufiventris and Scaptotrigona sp. As summarized in Table 2, local people identified bees based on morphological and behavioral characteristics, and for some species, they were also able to describe their nesting biology.

Table 2 Local knowledge on stingless bees at the municipality of Muyupampa and Monteagudo, Chuquisaca

The well-known Señorita (T. angustula) was recognized by its slim body, small size, yellow–black colors (sometimes also described as dark brown), and very docile behavior. Local people know that this bee builds its nest in a variety of places, including hollow trunks, branches, or logs, underground or even on the wall or poles of the houses, and they build a small yellowish cylindrical cerumen entrance. Another well-known species (mentioned by 71.7% of the interviewees) is the totally black bee Negro (Scaptotrigona sp1), characterized by its medium size, and by the long cylindrical ornament, they build at the entrance of its nest at hollow trees or underground. According to most people, they have very aggressive behavior; however, some people described it as docile, which could be a confusion with another Scaptotrigona species. One person said that the bees were aggressive when the entrance was big, and the bees were docile when the entrance was small. Almost half of the local people (45%) mentioned the bee Tancarillo (M. rufiventris), distinguished by its large size, its yellow/orange color with black stripes, and its docile behavior. It was mentioned that this bee nests on hollow trees and logs and is hard to find since it builds small entrances. Two other black bees, Burro and Burra (cited by 23.3% and 10% of the interviewees, respectively) were described very similarly to the Negro, as docile, midsize, completely black, and nests with long cylindrical entrances built on hollow trees or underground. The bee known as Boca de sapo or Sapito was mentioned by 21.7% of the interviewees and identified by its small size, black color, and docile behavior. They nest in hollow trees and build around the entrance a characteristic ornament that reminds of a frog’s mouth. The other eight stingless bee species were cited by 5% or less of the interviewees. There was no significant difference neither in the influence of age (p = 0.698) or ethnicity (p = 0.554) on the number of species known by the local people, nor in the interaction between age and ethnicity on the number of known species (Additional file 1: Appendix 1 and Appendix 2).

When asked about the places where stingless bees were most commonly seen, 70% of the interviewees answered the forest with Señorita being the most common bee. These bees can also be seen in other places, such as the riverside, open fields, crops, or orchards, but not as often as in the forest. Nevertheless, many of the interviewees (43%) affirmed that in the last 5 years the population of bees had decreased and that this was principally because of the wildfires, climate change and pesticides, but also because the nests were withdrawn from the forest to be bred in boxes. On the other hand, another 39% of the interviewees said that the bee population had actually increased in the last 5 years mostly because of artificial breeding (Table 3). Despite these different perceptions, most of these local meliponiculturists (95%) agreed that bees generally benefit humans and the environment. Honey production was the most mentioned benefit that bees brought (mentioned by 62% of the interviewees) followed by politization (47%), propolis production (23%), and medicine (10%).

Table 3 Informants’ perception on the abundance and conservation status over the last 5 years of local stingless beesManagement techniques

Most interviewees had between 1 and 4 training courses held mainly through the PASOS Foundation. The most attended topics were the following: (1) management of modern hives, attended by 48 of the interviewed women. This course focused on the breeding of bees: the parts of a rational hive (boxes), artificial feeding to strengthen the colonies, divisions, and how to move wild colonies to rational hives. (2) Harvest of honey and other bee products, attended by 41 of the interviewed women. This course aimed to show how to harvest and later to preserve the honey and other hive products, taking into account sanitary measures. (3) Main characteristics of stingless bees, attended by 33 of the interviewed women. This course explained most of the characteristic traits of these bees, such as their social behavior and caste system, reproduction, what they feed on, and how honey is produced.

The most frequently managed stingless bee of this region is Señorita which is being bred by all the interviewees (100%), followed by Negros bred by 20% of the interviewees, Tancarillos 14%, and Sapitos 8.5%. Every meliponiculturist owns between 1 and 25 hives of Señorita, between 1 and 10 hives of Negro, and between 1 and 3 hives of some of the other stingless bee species. On the other hand, A. mellifera is being managed by 68% of the interviewees. Adding all the hives reported by the interviewees, there are in total 702 hives of honeybees, 617 hives of Señorita, 38 hives of Negro, and 27 hives of Tancarilo. A strong significant positive correlation (p = 0.0072, r = 0.881) was found between the percentage of people that own hives of a bee species and the mentioned index of such species, as shown in Table 2.

Some meliponiculturists (22%) obtained their hives by buying them, probably from other local meliponiculturists, while others (6%) got them through traps, dividing them, or as a donation. But most of the stingless bee hives (93%) owned by the interviewees originated from wild hives that were removed from their natural environment in the forest and placed inside wooden boxes. To remove these hives, around 33% of the times the trees or branches supporting the nest were cut off; in the other cases, the hives could just be removed since it was inside a dead log, or it was easier to remove them without cutting off the tree or branch. The survival rate of the hives that underwent these transfer processes was very high according to 55% of the interviewees, but 30% stated that some or most of the hives did not survive the transfer to the box. Once the hives were in the boxes, they were kept mostly around the house or in the meliponaries, where they were taken care and managed in different ways. In 88% of cases, hives hosted some pests in the last 5 years, mostly Phoridae flies, and attacks by other bees or ants. Most interviewees said they gave their hives artificial food (a mixture of water and sugar) to strengthen them when they looked weak, but less than 30% said they took preventive measures against ants, cleaning out the spiders’ nets or others. Regarding the artificial division of the colonies, 62% of the interviewees reported that they practiced this normally once a year, and most of them were successful.

Meliponiculturist who succeeded in artificial division of hives had taken a significantly higher number of training courses compared with those who did not perform artificial divisions (p = 0.0423). Similarly, those meliponiculturists who gave supplementary food to the hives, had taken a significantly higher number of training courses compared with those who did not perform this practice (p = 0.0095). On the other hand, there was no significant difference between the number training courses taken and the success or failure on racking (p = 0.723) or in the presence or absence of practices to fight pests (p = 0.340) (Table 4).

Table 4 Results for the generalized linear models for the influence of the number of training courses on the use and success of management techniquesStingless bees’ products, productivity, and commercialization

When questioned about the harvesting of the honey, 17% of interviewees said they did not harvest their hives, at least not yet, and the rest said they usually did it once a year. Honey production of the colonies of Señorita varied between 0.5 and 1 L per colony per year, and rarely more than 2 L. In contrast, the colonies of Tancarillo and Negro produced a larger volume of honey, yielding between 1 and 4 L per colony; however, these species are rarely bred. Besides honey, most interviewees also harvested pollen, propolis, and cerumen in lesser amounts. This activity was mostly done in the company of a son or a daughter.

In the communities, honey, pollen, propolis, and cerumen are used but in very different proportions. Honey was the most used product from the hive. Over 90% of the meliponiculturists harvested honey from their hives, most of them at least once a year, in some cases two (26%) or even three (6%) times a year. It is valued for its medical uses, specially to treat eye diseases and common cold, as well as food and as a source of income since it is a very valued product in the market. Despite this fact, just 38% of the meliponiculturists produced enough honey to sell it, approximately half was sold to the public, and the other half was sold in bulk to local NGOs at a price of around USD 21 per liter. This price is four to five times higher than honey sold in bulk from A. mellifera which can be sold for USD 4 to 5 [50]. The rest consumed the honey themselves as food or as medicine. As mentioned previously, Señorita is the most managed bee in this area, although it normally produces between 500 mL and 1 L, whereas Negro or Tancarillo produce on average 4 L and 2.3 L, respectively. The second most harvested product was pollen, locally called “pan de abeja,” being harvested by 35 women (59%). Pollen is mostly used as food, but some women also have medicinal use for it as energizer or nutritional supplement mostly for kids with anemia. Pollen is eaten pure, mixed with banana or with honey. It is rarely sold to the public, generally with a price of USD 15 per kg. Propolis was harvested by 42% of the interviewed women, and they used it equally as medicine or for sale. It was sold principally to the public with a very wide range of price oscillating between USD 3 and 12 per 100 mL. Cerumen was collected only by 31% of women. It was mostly purified and used to strengthen other hives. Three interviewees said they used the cerumen as food; one said she used it as medicine, and just one sold it at USD 22 per kg. Finally, the brood cells were the least harvested and used product of the hive. Just two interviewees (3%) mentioned this medicinal/traditional use; by eating the brood cells, it is believed that it enhances fertility.

The use of honey and its medicinal properties

There is a consensus among the interviewees that the honey produced by Señorita is the most beneficial and the one with more medicinal properties, being used for treating several diseases. According to the frequency of citations, the main therapeutic use was for respiratory system treatments. Treatment of eye problems was cited almost as frequently (18 times), but in this case, honey was not consumed/eaten; instead, a drop or two are released directly on the affected eye. Ten interviewees also mentioned that consuming honey helped with digestive problems, and 9 said it strengthened the body and the immune system. In just a few cases (2), it was mentioned that honey could cure skin damages.

Regarding the uses of the honey produced by the other bees, in three different occasions it was informed that the honey produced by Burro and Burra was used to increase fertility, and two women mentioned that the honey produced by Negro was also helpful to treat digestive and respiratory problems.

The interviewees also shared some recipes and treatments they used to treat diseases (Table 5). Although some of the secondary ingredients varied, mostly there was a consensus on which ingredients to use for certain illnesses and how to prepare them.

Table 5 Recipes and treatments based on honey and other products of the hiveRelative cultural importance

The interviewees reported 30 different specific uses (#U) for the products of five stingless bee species: Señorita (T. angustula), Negro (Scaptotrigona sp.), Tancarillo (M. rufiventris), Sapito (Plebeia sp.), and Burro/Burra (Scaptotrigona sp.). These specific uses were grouped into 4 categories (#C): commercialization, food, medicine, and others (Additional file 1: Appendix 3). Based on the RCI index, T. angustula was the most culturally important bee in the region, followed by Scaptotrigona sp. (Table 6). There was a significative positive relationship between the percentage of people that managed a bee species and the relative cultural importance index (r = 0.875, p = 0.0044).

Table 6 RCI relative cultural importance index