The traditional knowledge about the biodiversity of edible Brazilian fruits and their pollinators: an integrative review

The database for this review was constructed with information on the dietary use of 557 species of Brazilian fruit trees, consumed in both rural and urban areas. Data on pollinators of approximately 1/3 of these plants (29.3%) were found, totaling 527 species, with most species native to Brazil associated with the class Insecta, order Hymenoptera, and family Apidae. This data analysis allows us to identify ecological patterns and trends in the richness of the pollinator–plant interaction network and the use of these plants for food.

The current understanding of pollinator interactions with economically important species is still limited, hindering the development of effective conservation strategies and the assessment of ecosystem services crucial for sustaining agricultural and extractive industries [35]. This research underscores a notable knowledge gap in pollination mechanisms, as 70.7% of the species investigated lack documented information on their pollinators and pollination syndromes.

Regarding the hypotheses tested, only the third was supported, namely, exotic plants have greater diversity of exotic pollinators compared to native plants. The other hypotheses about the relationships between species origin and pollinator richness (1—native plants have a higher total pollinator richness than exotic plants and 2—native plants have a higher richness of native pollinators) were not supported by the data.

It is important to highlight the limitations of this research. Firstly, the data on plants were collected only from scientific articles, which limits the scope of knowledge accessed in other forms of publications. There is an irregular geographical distribution of studies in the country, with some areas much more known than others, in addition to the lack of data in the literature regarding pollinators of the food plants investigated.

Apis mellifera L. has proven to be a key pollinator of native and introduced fruit species in Brazil, including star fruit (Averrhoa carambola L.), coffee (Coffea arabica L.), and lemon (Citrus limon (L.) Osbeck). Its activity appears to fulfill the pollination needs of a large proportion of Brazilian cultivars and wild plants, especially in agricultural areas [35, 36], thus becoming a central pollinator in Brazil.

This species was introduced to Brazil in the 1950s to increase honey production and other beekeeping resources [37]. Subsequent swarm escapes, coupled with its high adaptability to the Brazilian environment and associated economic value, were the elements that promoted its national conservation [37].

It is crucial to highlight that, despite its significance, A. mellifera can negatively impact plant–pollinator networks and pollinator richness in the field [38]. Studies have shown that this species exhibits dominant social behavior over pollen resources near their nests, hindering other bees from accessing these resources, leading to population decline and even the complete replacement of native bees in areas near A. mellifera nests [39, 40]. In extreme cases, its ecological replacement is the only way to meet the pollination demands of plants due to the decline of native insects [39, 40].

In anthropic environments such as agricultural areas, the abundant and generalized supply of floral resources seems to favor the activity of generalist pollinators. Species like Trigona spinipes (Fabricius, 1793) and A. mellifera are examples of generalist pollinators that actively exploit these environments, competing for resources with other pollinators, both native and exotic. This ecological behavior likely explains the high richness observed in the quantitative data collected in this study.

This result contradicts hypotheses 4 and 5, which attribute to exotic pollinators a superiority in terms of visitation richness and pollination breadth. The wide distribution and generalist behavior of A. mellifera virtually increase the contribution of other pollinator groups, both native and exotic, to Brazilian pollination.

Both Apis and non-Apis bees plays a crucial role in enhancing fruit production in Brazilian crops, with similar increases in productivity observed in plantings visited by both groups [19, 41]. Among native pollinators, stingless bees (non-Apis) are the most diverse group of species in Brazilian pollination (81 spp.). The highest concentration of these bees is in the Neotropical region, where approximately 47% of all species are described in Brazil, further justifying their relevance in local pollination [42, 43]. Asteraceae, Fabaceae, Lamiaceae, and Malvaceae are the botanical families most frequently visited by stingless bees, with Trigona and Melipona being the most diverse and important genera [43].

The functional diversity of pollinators is crucial for maximizing agricultural yields. Although bees are the primary pollinators, recent studies [44,45,46] have demonstrated the significance of other pollinator groups, such as beetles, flies, wasps, butterflies, and moths. These groups, which visit 25–50% of cultivated plant species worldwide, can significantly increase agricultural production by promoting a higher frequency of floral visits, even if they are less efficient than bees in this role. The synergy between different pollinator groups can enhance fruit production, leading to increased plant productivity or larger fruit size, highlighting the importance of conserving and promoting pollinator diversity in agroecosystems [45, 46].

Insect populations, including pollinators, have experienced significant declines in recent decades, impacting major orders like Coleoptera, Lepidoptera, Hymenoptera, and Diptera. These declines are widely attributed to anthropogenic activities, as documented in numerous countries, particularly the United Kingdom [47, 48].

Our understanding of the effects of human activities on insect diversity in tropical regions, which currently harbor the largest extent of deforestation for agriculture and extensive livestock farming, remains limited. This scenario is concerning, given that the greatest diversity of animals and plants on the planet is in the tropics yet, have been comparatively less studied than other regions [47, 48]. This lack of knowledge not only hinders our ability to accurately assess species diversity in the tropics but also prevents us from quantifying the impact of environmental pressures induced by human activities on local species.

Beyond heightened competition for plant resources, various factors contribute to the systematic decline of pollinator insect populations. Synthetic pesticides are implicated in the decimation of entomofauna diversity in agricultural landscapes. These pesticides can induce colony collapse disorder in social bees, contaminate water bodies, and kill larval stages, among other indirect effects on insects [49, 50].

Furthermore, the findings of this review highlight the abundance of food-producing fruit trees utilized by Brazilian communities. These species are accessed both through agricultural production and direct extraction from natural environments.

This situation highlights the need to seek wild food sources to supplement daily meals [51]. Rural communities have been the most studied in published articles, especially those in the northern and northeastern regions, which have the highest concentration of people with low monthly incomes and a higher predisposition to food insecurity in the country.

Additionally, Brazilian ethnobotanical research tends to prioritize the exploration of traditional knowledge and use of plants in rural environments [2, 52, 53], and preferentially in traditional communities (indigenous, quilombola, fishermen, riverine people, etc.). Furthermore, research on the use of food plants predominantly focuses on communities situated within the phytogeographic zones of the Atlantic Forest and Amazon biomes. This emphasis neglects the knowledge generated in urban areas of the country, where, when such research is conducted, it concentrates on the topic of urban home gardens. Consequently, this focus exacerbates the information gap concerning this fundamental portion of the nation.

Quilombola communities have been a focal point in ethnobotanical research. These communities, formed by descendants of enslaved Africans who escaped during Brazil's slavery era, have historically relied on surrounding natural resources for sustenance and food [54, 55]. However, there remains a significant gap in our understanding of food plant consumption in Brazil.

This is particularly concerning given the country's rich diversity of 305 indigenous ethnicities [56], of which only 13 (4.26%) have been included in ethnobotanical studies. Given the uneven geographical distribution of ethnobotanical studies within the country, with some areas being considerably more extensively researched than others, there is a lack of data in the literature concerning the pollinators of the food plants under investigation.

For traditional communities such as quilombolas and indigenous peoples in rural areas, food security is intrinsically linked to the availability of wild resources. Food insecurity increased in Brazil from the second half of the 2010s, due to the convergence of several factors, including the economic crisis, the discontinuation of public policies promoting food security in vulnerable populations, the disruption of food transfers to low-income populations, and the health crisis exacerbated by the COVID-19 pandemic in 2020 [24, 25, 57, 58], leading to increased pressure on wild resources.

This literature review highlights the importance of fruit trees in the Brazilian diet, given their high biodiversity found in Brazilian hotspot areas, such as the Amazon Rainforest, the Atlantic Forest, and the Cerrado, as a crucial factor for the food security of these communities.

Natural areas play a fundamental role in ensuring food security for both rural communities, which depend directly on natural resources for their subsistence, and urban communities, which benefit from agricultural production and the supply of food from these areas [35, 36]. Traditional communities, in turn, are crucial agents in promoting environmental conservation in these regions [53], being essential for the dissemination of good practices in land use with sustainable family agricultural production that respects the limits of the environment.

Our results align with those found on literature who indicate a consistent preference for certain plant families among traditional Brazilian communities [27]. As in their study, the Anacardiaceae, Arecaceae, Fabaceae, Myrtaceae, Passifloraceae, and Solanaceae families were the most frequently cited in our analysis, evidencing a consistent pattern in the choice of food forest resources.

The relevance of insects as pollinators is confirmed by the expressive diversity of species found in this research, corroborating previous studies [15, 35, 36]. These results reaffirm the importance of insects in the pollination of modern plants and highlight their crucial role in maintaining biodiversity and the food production chain, essential for food maintenance and the promotion of food security in rural and urban communities.

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