Important pollinating bees for Brazilian agriculture

The greatest ecological importance of bees is related to pollination. Pollination is a process of transferring pollen grains from one flower to another. It is estimated that more than 90% of flowering plants depend on animal pollinators. These, when visiting flowers to feed on pollen or nectar, end up with pollen grains stuck to their bodies. As they move between flowers, they take grains from one flower to another. The pollen grain, when deposited in the flower, fuses with the ovule, which will give rise to seeds and fruits. Thus, many plants depend on animals to produce fruits and seeds, which is directly related to agriculture.

An article was recently published in the international magazine Apidologie, which reviewed 249 scientific publications on crop pollinators of economic interest. It is important to emphasize that in this review, insects that only visit flowers were differentiated from those that actually pollinate them. This was done because not all floral visitors touch the flowers' reproductive organs and therefore, not all are able to transfer the pollen grain towards the ovule. Therefore, in this work, pollinators and visitors were analyzed separately, and emphasis was placed on species that actually act as pollinators.

The pollinators of 75 Brazilian agricultural crops were identified. These pollinators are distributed among 250 species of animals, 87% of which are bees. The bee genera cited as effective pollinators and worth highlighting are: Centris, a genus of solitary bees known as oil bees because they collect floral oil; xylocopa, large solitary bees known as carpenters, as they make their nests by digging holes in wood and; Bombus, also large bees known as bumble bees. Two other important genera belong to stingless bees: Melipona e trine. Stingless bees are social and very useful for management, as they do not have a functional sting. They had already been highlighted for their importance in pollination in agricultural crops in previous works, both international and Brazilian.

Two species of bees deserve to be highlighted: the Apis mellifera, called the honey bee or Africanized, cited as a pollinator of 28 crops and the Trigona spinipes (irapuá), cited for 10 crops. These two species are particularly interesting because they have a wide geographic distribution, allowing them to perform pollination services in different Brazilian regions, including degraded areas with low diversity. In addition to these, we also highlight the Xylocopa frontalis (a type of carpenter bee) and the Melipona fasciculata (gray uruçu).

Another group of species that should be emphasized is that belonging to the Halictidae family, a family that has many species of bees, some of which are very striking with metallic colors that vary between green and blue. This family, however, is still little studied, and therefore, species identification is very difficult. More than half of the times this family was mentioned in the works consulted, the identification was not complete, making analysis very difficult. The crops that were cited as being pollinated by bees belonging to this family are peppers, tomatoes, cotton, jurubeba, eggplant, strawberries, camu-camu and acapu.

The data obtained were also analyzed considering the different regions of Brazil. Few data were obtained in the north and central west regions, demonstrating the lack of knowledge that still exists about the pollinators of agricultural crops in these two regions. Many plants of regional interest, mainly in the north of the country, were also little mentioned. There is a lack of basic knowledge about floral biology and pollinators, topics that still need to be better studied.

In a second review, published by the Journal of Economic Entomology, the dependence of agricultural crops on animal pollination was analyzed. It is already well known that some crops with high global production (such as wheat, corn and rice, for example) are pollinated by the wind, that is, they do not depend on animal pollinators. On the other hand, crops with high nutritional value (such as fruits and vegetables), which are often the basis of family farming and an important source of income in the regional economy, are more dependent on pollinators. Therefore, an assessment of this type is important, especially given the scenarios of bee disappearance and pollinator deficits in the northern hemisphere that have been reported.

Measurements of dependence on agricultural crops for pollination have been carried out globally since the 90s, and four classes of dependence have been suggested: essential, large, modest or small. This attribution was based on studies that revealed that some crops, when not pollinated, presented a reduction of between 90 and 100% in production (dependence considered essential); others, between 40-90% (dependence considered large); between 10-40% (modest ); and between 1-10% (small).

Thus, in order to have a dimension of dependence on pollinators, a review was carried out based on 57 works published in the scientific literature on the topic. These works cited 85 crops as showing some degree of dependence on animal pollination, with more than a third of these crops (30 crops) being cited as showing essential or great dependence on pollinators.

The crops that were cited as showing essential dependence on pollinators are: pumpkin, acerola, cajazeira, cambuci, Brazil nut, cupuaçu, fruit do conde, gliricidia, jurubeba, passion fruit, sweet passion fruit, watermelon, melon and annatto. Those that were cited as showing great dependence were: gabiroba, guava, red jambo, murici, cucumber, sunflower, guaraná, tomato, avocado, jatropha, apricot, cherry, peach, plum, adesmia and araticum.

Furthermore, the same article cited above and published by the Journal of Economic Entomology also estimated the economic value of pollination for agriculture. The method used to calculate this value was proposed by international authors in the 90s. Although other methods have been proposed since then, this one is particularly useful because it is low in complexity.

The economic value of pollination is calculated as a function of two factors: each crop's dependence on pollination and the annual production value of each crop. As stated above, pollination dependence is estimated based on the four classes already mentioned (essential, large, modest or small) and each of these classes is assigned a dependence rate (respectively, 0,95; 0,65; 0,25 .0,05 and XNUMX). This rate is then multiplied by the annual production value of each crop. In the case of Brazil, the annual production value of some crops is available on the website of the Brazilian Institute of Geography and Statistics (IBGE).

It was possible to establish the pollination value for only 44 crops, which had both dependence and production value defined. The total production of these 44 crops in 2013 (the year for which the assessment was made) was approximately 45 billion dollars. The economic value of pollination obtained for these crops in the same period was approximately 12 billion dollars, which is equivalent to almost 30% of the total value.

It is important to emphasize that almost half of the pollination value obtained is equivalent to soybeans, a crop widely produced in Brazil and, therefore, with a high total production value. This crop has been classified as having a modest dependence on pollinators, but this dependence still needs to be further evaluated, as there are many different varieties being cultivated in the country today. Other crops besides soybeans that stand out with high pollination values ​​are coffee, tomatoes, cotton, cocoa and oranges. Of these, only cocoa has an essential dependence on pollinators; the others have small or modest dependence, but due to the high production values ​​in the country, the pollination values ​​obtained are also high.

This type of measure is important to draw attention to the value of biodiversity. Often, this recognition is still low on the part of the general population, or farmers, or decision makers. Therefore, currently, the concept of ecosystem services has been emphasized, which are the benefits that ecosystems bring to human beings due to their intrinsic functioning. Thus, the pollination service occurs naturally due to the inherent processes of natural areas, which serve as habitat for animals that work in agricultural areas, pollinating crops. This makes it clear that the protection of areas of native habitats interspersed in crops is important for ensuring pollinators and these, agricultural production, being of interest not only to those who appreciate the scenic beauty of natural areas, but also to the local economy and for food production.

Especially the recognition of the role of insects is of paramount importance. These animals are still little researched and little protected. However, many of them have crucial roles in nature and their importance would need to be better known and publicized. Therefore, pollinators are an excellent example of how nature acts, in sometimes subtle ways, in maintaining human societies, mainly through their role in pollination and food production. Studying and protecting them ultimately amounts to contributing to the maintenance of human well-being.

Summary tables of the results obtained

Below you can find four tables that summarize the most important results of the works cited.

Square 1. Species of bees that have been cited as effective pollinators of the largest number of agricultural crops, as well as their geographic distributions and the degree of dependence of each crop on an animal pollinator. The species in bold stand out because they are cited as pollinators of many crops that have essential or great dependence on animal pollination (see also Table 2).

Abelha	Geographic distribution in Brazil*	Pollinated agricultural crop	Dependence of culture on animal pollinators
1) Apis mellifera (honey bee or Africanized bee)	all regions	1.pumpkin	Essential
		2.acapu	Indeterminate
		3.cotton	Modesta
		4.amora	Modesta
		5.café	Modesta
		6.cashew	Essential
		7.cashew	Modesta
		8.camu camu	Indeterminate
		9.canola	Modesta
		10.onion	Pollination does not increase production+
		11.sunflower	Grande
		12.guava	Grande
		13.jatropa	Indeterminate
		14.joá	Little
		15.orange	Modesta
		16.chips	Pollination does not increase production++
		17.manga	Pollination does not increase production
		18.melon	Essential
		19.strawberry	Modesta
		20.ume caa stone	Indeterminate
		21.cucumber	Grande
		22.chili	Little
		23.Bell pepper	Little
		24.Pitanga	Modesta
		25.pitanguba	Indeterminate
		26.soybean	Modesta
		27.tomato	Grande
		28.umbu	Modesta
2) Xylocopa frontalis (carpenter)	all regions	1.Brazil nut tree	Essential
		2.cumaru	Indeterminate
		3.cowpea	Indeterminate
		4.glyricidia	Essential
		5.guava	Grande
		6.jurubeba	Essential
		7.passion fruit	Essential
		8.sweet passion fruit	Essential
		9.muric	Grande
		10.umbu	Modesta
		11.annatto	Essential
3) Trigona spinipes (irapuá)	all regions	1.pumpkin	Essential
		2.acerola	Essential
		3.carrot	Pollination does not increase production+
		4.chayote	Indeterminate
		5.sunflower	Grande
		6.orange	Modesta
		7.manga	Pollination does not increase production
		8.strawberry	Modesta
		9.Bell pepper	Little
		10.pomegranate	Modesta
4) Melipona fasciculata (gray uruçu)	north of Brazil	1.acai	Indeterminate
		2.aubergine	Modesta
		3.cashew	Essential
		4.camu camu	Indeterminate
		5.chili	Little
		6.Bell pepper	Little
		7.tomato	Grande
		8.annatto	Essential
5) Bombus morio (mamangava)	Midwest, Northeast, Southeast and South	1.pumpkin	Essential
		2.eggplant	Modesta
		3.guava	Grande
		4.jurubeba	Essential
		5.passion fruit	Essential
		6.sweet passion fruit	Essential
		7.annatto	Essential
6) Centris tarsata (oil bee)	Midwest and North	1.acerola	Essential
		2.eggplant	Modesta
		3.cashew tree	Modesta
		4.guava	Grande
		5.muric	Grande
		6.murici pitanga	Grande
		7.tomato	Grande
7) Epicharis flava (mamangava)	all regions	1.acerola	Essential
		2.Brazil nut tree	Essential
		3.cumaru	Indeterminate
		4.guava	Grande
		5.passion fruit	Essential
		6.sweet passion fruit	Essential
		7.muric	Grande
8) Eulaema nigrita (mamangava)	all regions	1.Brazil nut tree	Essential
		2.cumaru	Indeterminate
		3.gabiroba	Grande
		4.guava	Grande
		5.passion fruit	Essential
		6.sweet passion fruit	Essential
		7.annatto

Abelha

Geographic distribution in Brazil*

Pollinated agricultural crop

Dependence of culture on animal pollinators

1) Apis mellifera (honey bee or Africanized bee)

all regions

1.pumpkin

Essential

2.acapu

Indeterminate

3.cotton

Modesta

4.amora

Modesta

5.café

Modesta

6.cashew

Essential

7.cashew

Modesta

8.camu camu

Indeterminate

9.canola

Modesta

10.onion

Pollination does not increase production⁺

11.sunflower

Grande

12.guava

Grande

13.jatropa

Indeterminate

14.joá

Little

15.orange

Modesta

16.chips

Pollination does not increase production⁺⁺

17.manga

Pollination does not increase production

18.melon

Essential

19.strawberry

Modesta

20.ume caa stone

Indeterminate

21.cucumber

Grande

22.chili

Little

23.Bell pepper

Little

24.Pitanga

Modesta

25.pitanguba

Indeterminate

26.soybean

Modesta

27.tomato

Grande

28.umbu

Modesta

2) Xylocopa frontalis (carpenter)

all regions

1.Brazil nut tree

Essential

2.cumaru

Indeterminate

3.cowpea

Indeterminate

4.glyricidia

Essential

5.guava

Grande

6.jurubeba

Essential

7.passion fruit

Essential

8.sweet passion fruit

Essential

9.muric

Grande

10.umbu

Modesta

11.annatto

Essential

3) Trigona spinipes (irapuá)

all regions

1.pumpkin

Essential

2.acerola

Essential

3.carrot

Pollination does not increase production⁺

4.chayote

Indeterminate

5.sunflower

Grande

6.orange

Modesta

7.manga

Pollination does not increase production

8.strawberry

Modesta

9.Bell pepper

Little

10.pomegranate

Modesta

4) Melipona fasciculata (gray uruçu)

north of Brazil

1.acai

Indeterminate

2.aubergine

Modesta

3.cashew

Essential

4.camu camu

Indeterminate

5.chili

Little

6.Bell pepper

Little

7.tomato

Grande

8.annatto

Essential

5) Bombus morio (mamangava)

Midwest, Northeast, Southeast and South

1.pumpkin

Essential

2.eggplant

Modesta

3.guava

Grande

4.jurubeba

Essential

5.passion fruit

Essential

6.sweet passion fruit

Essential

7.annatto

Essential

6) Centris tarsata (oil bee)

Midwest and North

1.acerola

Essential

2.eggplant

Modesta

3.cashew tree

Modesta

4.guava

Grande

5.muric

Grande

6.murici pitanga

Grande

7.tomato

Grande

7) Epicharis flava (mamangava)

all regions

1.acerola

Essential

2.Brazil nut tree

Essential

3.cumaru

Indeterminate

4.guava

Grande

5.passion fruit

Essential

6.sweet passion fruit

Essential

7.muric

Grande

8) Eulaema nigrita (mamangava)

all regions

1.Brazil nut tree

Essential

2.cumaru

Indeterminate

3.gabiroba

Grande

4.guava

Grande

5.passion fruit

Essential

6.sweet passion fruit

Essential

7.annatto