The influence of recent Brazilian policy and legislation on increasing bee mortality

The decline in bee communities in recent years has been a major concern worldwide. The increase in the mortality of these pollinators is related to several factors, the main one being the intensive use of pesticides in agricultural crops. Brazil is the world leader in use of pesticides since 2008 and recent changes in legislation have facilitated the commercialization of certain pesticides whose marketing has been banned in several countries. This review addresses how current Brazilian legislation on agrochemicals has influenced the increase in bee mortality. Under the current federal government, in 2019 and 2020, 474 and 493 new pesticides were registered in the country, respectively, some of them classified as highly toxic to bees. In addition, public policies in Brazil led by certain sectors of agribusiness have also contributed to increase the number of threats and the mortality of bees, making it difficult for the beekeeping sector to act in opposition. Understanding how these policies directly affect pollinator conservation allows decisionmaking to help mitigate their environmental and economic impacts in Brazil. Otherwise, without effective actions to mitigate the abusive use of pesticides, the numerous studies demonstrating its direct impacts on the bee’s survival will be of no use.


Introduction
Interactions between pollinating plant and animal species are essential for preserving biodiversity and maintaining the functionality of terrestrial natural ecosystems and crops (Fantinato et al., 2018). It has been estimated that 300.000 plant species (almost 90% of all flowering plants) require animal pollination to reproduce (Ollerton, Winfree & Tarrant, 2011). For agricultural crops, pollination contributes by 75% to the production of world crops, representing an economic value estimated in €153 billion annually and contributing by 9.5% of world agricultural economic production (Giannini et al., 2014;Landaverde-González et al., 2017).
Bees have been considered the main pollinating agents in the nature, promoting both the spread of plants and the maintenance of genetic diversity in natural and agricultural crops environments (Woodcock et al., 2019). Brazil, one of the main producers of important crops worldwide, depends a lot on bee pollination services and it has been estimated that the economic value of these ecosystem services is around US$ 12-14 10 9 (Santos, Otesbelgue & Blochtein, 2018). According to the Brazilian Association of Honey Exporters (ABEMEL, in Portuguese), in 2017 Brazil have exported around 27 tons of honey, being the 9 th in the world ranking (ABEMEL, 2018). Regionally, the Southern region stands out as the largest producer (41.7%), followed by the Northeast (27.5%), Southeast (24.8%), Midwest (4.5%), and the North regions (1.6%). According to the data from the 2017 Agricultural Census, 101,797 agricultural establishments produce honey in Brazil, with 2,158,914 hives (IBGE, 2017a). In 2016, Brazilian beekeeping exported about R$ 470 million blossom honey (IBGE, 2017b). Thus, beekeeping is an important economic activity for the rural population, mainly for family farming. Apiculture has been considered an easy maintenance activity, with a low initial cost, also not demanding daily care and allowing the beekeeper having other sources of income. For this reason, this activity has been defined as an alternative to reduce unemployment, helping many families in the country (Sabbag & Nicodemo, 2011;Lourenço & Cabral, 2016).
However, despite the importance of beekeeping and its ecosystem services, bees are at continuous risk on a global scale.
Indeed, studies have shown a great decline in bee populations in recent decades in many countries (Meeus et al., 2018) and numerous factors assist for that; among them the use of pesticides (Woodcock et al., 2017). In Brazil, a large decline in bee populations and the collapse in Apis mellifera colonies have been reported (Pires et al., 2016). In fact, over a 5-year period the loss of ~ 1 billion bees was estimated in Brazil, including honeybees, stingless bees, and solitary ones (Castilhos et al., 2019).
In 2019, 474 new pesticides were approved and registered in Brazil, the highest release since 2005, when data disclosure began (Brazil, 2021). In recent years, it has been allowed to launch in the market active ingredients highly toxic that are prohibited or even never disclosed by several countries (Serra et al., 2016;Kim, Kabir & Jahan, 2017), many of them because are highly toxic also for human beings as already proven (Kim, Kabir & Jahan, 2017). It is estimated that between 2000 and 2012 the use of pesticides grew by 288.41% and in 2017 the Brazilian market of those agrochemicals reached US$ 8.8 billion (Friedrich, Souza & Carneiro, 2018;Costa, Rizzotto & Lobato, 2018).
Considering the social and economic importance of beekeeping for the country and the relevance of pollination in agricultural areas, in addition to native areas (Vanbergen, 2013) this review addresses how Brazilian legislation has affected the increase of bee mortality in the country, as well as its consequences on the food production. For that, besides focusing on the Brazilian legislation, research data and scientific articles, especially in the last 10 years, have been considered to address how the ongoing government policy and the agribusiness sector have negatively impacted the apiculture in the country.

Methodology
For the elaboration of the article, a descriptive and systematic narrative review was applied in order to discuss the state of the art on the increase of bee mortality in Brazil and its direct relation with Brazilian politics and legislation. Because it is a complex and broad subject, this review model was adopted because it allows the interpretation and critical analysis of the authors (Rother, 2007). In this way, the data were collected in databases including: scientific books, archives of national and international research institutions and bodies, in addition to the Brazilian legislation. The Scientific Electronic Online Library (SciELO), Elsevier's Scopus databases, as well as the scientific journals accessed from the Coordination for the Improvement of Higher Education Personnel (CAPES, in Portuguese), available at https://www-periodicos-capes-gov-br.ezl.periodicos.capes.gov.br/ were used, between March 2020 and February 2021. In order to expand the results, keywords in Portuguese and English were used, such as bee mortality, pesticides, agribusiness, apiculture, pollinators, registration of pesticides, contamination in bees, and risks to pesticides.

Bee Mortality
In 1994, French beekeepers reported signs of anomalous bee's behavior in hives. It was noticed that many bees did not return to the hives and those that returned would gather in small groups on the ground, or yet they would be hovering disoriented in front of the hive. Evidences raised pointed to the contamination of bees by the Bayer's systemic insecticide imidacloprid (Maxim & van der Sluijs, 2013). Further researches (Holder et al., 2018) on bee mortality in France also pointed to the use of the phenylpyrazole insecticide fipronil, a disruptor of the insect's central nervous system (CNS). Fipronil acts by blocking glutamate-gated chloride channels and also GABA-gated chloride channels, causing nerve and muscle hyperexcitation of insects even in low concentrations. Interestingly, restrictions on the use of this compound, as well as other insecticides (thiamethoxam and clothianidin, e.g.), started in 2008 in Italy Germany, and Slovenia, because of its relation with the bee death (Sgolastra et al., 2017). Over the years, numerous cases of bee populations decline have been reported, mainly in the USA, Europe, and Brazil, resulting from the intensive use of pesticides, causing the called "colony collapse disorder" syndrome (CCD) (Pires et al., 2016).
Bees are contaminated with pesticides while searching the environment for collecting pollen, nectar, and water (Lundgren, 2017). The chemicals used in pesticide formulations are ingested and absorbed by the bees' organism, causing toxic effects, such as physiological damages (Qi et al., 2020) or changes in behavior (Wang et al., 2017). Therefore, researches have associated different chemical groups to the rapid decline of bee colonies, e.g., organophosphates, organochlorines, pyrethroids, carbamates, and mainly neonicotinoids. The later are neurotoxic compounds that act on the CNS by binding to nicotinic acetylcholine receptors, leading to over-stimulation and paralysis (Christen, Bachofer & Fent, 2017). Tosi et al. (2018) investigated the Italian pollen visited by bees, revealing its contamination with the organophosphate chlorpyrifos. Likewise, analysis of bees collected in four locations in Spain during the citrus' flowering and fruit set periods, detected chlorpyrifos, dimethoate, and imidacloprid as the most common insecticides found in bee samples (Calatayud-Vernich et al., 2016). Importantly, these pesticides increased the mortality of these pollinators in citrus orchards.
In Mexico, the presence of organochlorine pesticides in honey and pollen samples from colonies of A. mellifera and Scaptotrigona mexicana, a stingless bee species was proved (Ruiz-Toledo et al., 2018). The authors report that for A. mellifera Research, Society andDevelopment, v. 10, n. 4, e36910414157, 2021 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v10i4.14157 4 pollen organochlorines were detected in all samples, as for the honey ones a lower, but also outstanding value, was found, i.e., 93.3%. For S. mexicana, 88.4% and 22.2% of the honey and pollen samples tested positive, respectively, for at least one pesticide.
Besides, the most frequent pesticides detected were heptachlor, γ-HCH, DDT, endrin, and DDE, which have long been banned from several countries.
Among the pyrethroid insecticides, bifenthrin was highly toxic to Apis mellifera, Apis cerana indica, and Trigona iridipennis species at 160g ha -1 (Govindaraj et al., 2017). Wang et al. (2017) point out that pyrethroid insecticides act on T-type voltage-gated calcium channels (VGCCs) in bee's brain cells, resulting in behavioral abnormalities, compromising swarming, feeding, learning, and acquisition skills of the insects.
In the case of carbamates, they act biochemically by reversibly inhibiting the activity of the enzyme acetylcholinesterase (AchE), leading to augmented amounts of acetylcholine in synapses in the brain and neuromuscular junctions, what results in cellular hyperexcitation (Gupta et al., 2017). For bees, carbamates have shown a toxic effect with a sublethal dose at 1.05 Mm (Riva et al., 2018) and even a lethal effect (LD50) (Lee et al., 2016). Studies have demonstrated the high degree of toxicity of different pesticides to bees (Table 1).  In addition, they point out that while one-third of the national territory has already been converted to agricultural lands, there is a great loss of natural vegetation and this impacts further increases of CCD cases. In addition to Brazilian universities and other research bodies involved in monitoring bee mortality, several institutions spread across the country have also carried out important researches to alert cases of bee death and colony collapses.
In addition to the studies herein cited linking the use of pesticides to the bee mortality around the world, many countries have implemented actions to minimize these harmful effects (Mengistie, 2016;Robin & Marchand, 2018;Kwakye et al., 2019).
However, Brazil has been moving in the opposite direction, which can have serious environmental and economic consequences, in addition to the damage to health, is considered a public health problem (Piccoli et al., 2016;Kim, Kabir & Jahan, 2017;Pignati et al., 2017;Queiroz et al., 2019).

Brazilian Legislation and its Relation with the Increased Release of Pesticides and Bee Mortality
In Brazil, agriculture is the main economic activity for many states, where the predominant model of production is based on agribusiness (Nasrala Neto, Lacaz & Pignati, 2014 Agribusiness was introduced in Brazil aiming to provide food security and sovereignty, but in a short time it showed to be substantially different from that initial goal, because economic factors proved to be more important. Currently, most agricultural goods produced by agribusiness are exported, either as commodities or in the form of non-food products (biofuels and ethanol, e.g.) (Friedrich, Souza & Carneiro, 2018). Agribusiness is very important for the country's trade balance, reaching a record of US$ 224 10 9 in exportation in 2019 and a commercial surplus of US$ 83 10 9 (SECEX/MDIC, 2020).
Due to the economic importance of agribusiness, recent changes in the national legislation on the regulation for pesticide release seem to have adopted mainly economic criteria. Political pressures occur both in the bodies of the Legislative Branch and in those that regulate and release agrochemicals for marketing. The performance of lobbyists in Brazil is also very strong, as they are able to directly influence lawmakers for moving and fostering the market. Indeed, nowadays an increasing number of active ingredients and products, prohibited or even never released in other countries or globally, has been allowed to be marketed in Brazil and, apparently, there is no reason to suppose that such a scenario is going to change in coming years (Serra et al., 2016). The Bill Law 6299/2002 seems to be a strategy of transnational industries who see in Brazil, under continuous political crisis, the opportunity to commercialize pesticides not easily released in other countries. In the Brazilian congress, the group called "ruralists" is considered as a major player for the release of too many pesticides in recent years (Carneiro et al., 2015).
Such a group has been known for their positions regarding the defense of landowner's interests, as they gather economical dominant classes and groups linked to rural, agroindustrial, and agribusiness activities (Bruno, 2017).
Another goal of interest of the ruralist group in the Brazilian congress focuses on the deregulation of the pesticide registration process. It has been aimed to create a National Technical Committee on Pesticides, which will define the raw materials and substances allowed or not to be used and commercialized in the internal market. Currently, the evaluation of safety parameters and toxicological traits of pesticide compounds is carried out by the National Health Surveillance Agency (ANVISA, in Portuguese) and by the Ministry of Agriculture, Livestock and Supply (MAPA, in Portuguese) (Carneiro et al., 2015).
ANVISA has historically performed an important role in retaining the release of chemical compounds highly toxic to human beings and to the environment, but it is always exposed to political influences less compromised with the human health and environmental preservation.
The commercialization of pesticides is also facilitated because Brazil has adopted a policy of tax exemption guaranteed by the current legislation, where producers of commodities are the biggest beneficiaries. Thus, small producers are forced to use pesticides, as other forms of production are not considered competitive enough to receive government incentives, also reducing the number of farmers who would like to adopt agroecological production systems (Serra et al., 2016). Besides, for producers using pesticides there are substantial rural credit available, i.e., the State encourages the use of technological package that claims to represent "modernity" in agriculture (Araújo & Oliveira, 2017).   (2017) demonstrated that in higher concentrations (1Fx10 -1 and 5Fx10 -2 , F = recommended field rate in ug active ingredient mL -1 ), dinotefuran caused 100% of bee mortality after one day of exposure. Corroborating these data, Yasuda et al. (2017) shown that among the neonicotinoid's insecticides acetamiprid, imidacloprid, clothianidin, thiamethoxam, and dinotefuran, the latter was the most toxic for bees (LD50, 1.4 ng/bee).
In Brazil, six products were also recently released based on the active ingredient sulfoxaflor, a new sulfoximine class insecticide, and three more containing lambda-cyhalothrin (pyrethroid) and sulfoxaflor, totaling nine products using that active ingredient (Agrofit, 2019). Interestingly, sulfoxaflor usage has been related to several sublethal impacts and increase in bee mortality worldwide (Siviter, Brown & Leadbeater, 2018;Chakrabarti et al., 2020;Azpiazu et al., 2021). After many member states of the European Union have banned the use of neonicotinoids insecticides such as imidacloprid, clothianidin, and thiamethoxam outside greenhouse structures, sulfoxaflor arrived on the market as a differentiated neonicotinoid, because it acts on the insect nicotinic acetylcholine receptor (nAChR) in a distinct manner relative to neonicotinoids (Millot et al., 2017).
Regarding the imidacloprid active ingredient, with 37 products registered in Brazil, it was the main asset found in food samples (16% -713 samples) assayed from 2017 to 2018, according to the Program for Analysis of Pesticides Residues in Food (Brazil, 2019). This neonicotinoid compound, as well as thiacloprid and clothianidin, have been associated with sublethal and lethal effects on bees (Woodcock et al., 2017;Raymann et al., 2018).
In Brazil, it is possible to note that the sectors of agribusiness and beekeeping have opposite interests regarding environmental issues, even though the ecological service, i.e., pollination, provided by bees benefits the former sector. In fact, pollination of crops is beneficial for beekeepers to produce honey and other bee products, as for farmers pollination service contributes to increasing the market value of their products, because both the quantity and quality of fruits and seeds increase when pollination is performed by bees (Santos, Otesbelgue & Blochtein, 2018). Thus, it is considered of great importance and mutual gains that those sectors can determine actions to minimize damages caused to pollinators by pesticides. However, from what was presented in the study, it can be seen that the current agribusiness sector's way of thinking makes it difficult to change the conventional management of cultivation systems, even though the damage to crop yields resulting from pollinator mortality has already been predicted long ago, especially for bees (Vanbergen, 2013;Novais et al., 2016).
Thus, is urgently necessary the adoption of sustainable alternatives to agrochemicals for pest control that mutually benefit the two sectors, such as the development of organic production systems combining pest management strategies through biological control and natural insecticides, such as botanicals and oils essentials (Santos, Otesbelgue & Blochtein, 2018). In this sense, organic and agroecological production have served an increasingly growing market niche, mainly related to the maintenance of health and food quality (Abreu et al., 2012;Moraes & Oliveira, 2017 With the ongoing scenario, the implementation of public policies that encourage the production of organic systems must be seriously considered, in order to protect pollinators and pollination services. In this sense, the report by Diks et al. (2016) lists 10 essential public policies for the protection of pollination services and one can highlight 5 items directly related to incentives to organic systems production, such as 1) raising the regulatory standards for pesticides, 2) promote integrated pest management, 3) develop incentives, such as insurance schemes to help farmers to benefit from ecosystem services, 4) recognize pollination as an agricultural input in extension services, and 5) finance participatory research to improve yields in organic, diversified, and ecologically enhanced agriculture.

Conclusion
Agribusiness in Brazil is undoubtedly a booming sector, with important contribution to the balance of trade, but also with serious impacts on the environment and for the beekeeping sector. With decision-making actions based mainly on economic interests, the ruralist bench has acted in modifying legislation without considering the risks that conventional cultivation systems offer to the environment and human and animal health.
As demonstrated in the review, numerous studies have recursively proven that pesticides are lethal to pollinators, such as bees, who are primarily responsible for maintaining the genetic diversity of natural and agricultural crops. Considering the risks involved, proposing practices to minimize the impacts caused by pesticides in the country is urgently necessary, especially in the current unprecedented scenario where 474 pesticides were recently released, the highest rate ever seen.
Therefore, it is important to first emphasize the need for effective public policies to protect bee species in all Brazilian states. Regulations and laws must be based on research carried out inside and outside the country. Several studies are carried out by research institutions and bodies; however, they are not taken into account for the construction of national strategies for the preservation of beekeeping.
The interaction between the agricultural and beekeeping sectors can be very beneficial for the development of strategies and collaboration for mutual growth, with no prejudice for any of the areas of activity. For the agricultural sector, it is urgent to include rules that prevent the registration of pesticides already banned in other countries. Besides, in the case of pesticides currently released in the country, greater inspection is necessary to control their usage.
Finally, the measures above mentioned can help to minimize risks to pollinators, but the impact on the use of pesticides will not be resolved yet. Therefore, the adoption of environmentally friendly practices is extremely necessary, especially in food production systems. In Brazil, organic production systems have been widely adopted in family farming systems but need greater encouragement and support for expansion by federal government agencies. Thus, as long as current interests and political forces remain active in Brazil, the increase in bee mortality will most likely continue to occur.
As a suggestion for future work, one can emphasize the need for researches aiming not only at the mortality of Apis mellifera bees, but also at other native bees and other pollinators. Likewise, there is a need to expand studies focusing on low toxicity chemical compounds, as these can impact non-target insects, leading to behavioral change and/or lethality.