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Ecology

Queens living in harmony

The colonies of a Brazilian species of bee, the guaraipo, are led by up tofive queens and form an environment with more flexible rules

EDUARDO CESARDay-to-day of the guaraipos: workers return to the nest, one of them bringing pollen (on its feet)EDUARDO CESAR

Research into a bee that is typical of the Atlantic Rain Forest, the Melipona bicolor, is bringing to light an organization in the colony that is less hierarchical and shares power more evenly between queens and workers, the two castes of this species that live side by side. In the universe of the guaraipo, as this species is known, there is almost always more than one queen – evidence of shared command – and the workers are not all that submissive.The slaves lay trophic eggs, which serve as food for the bee leaders, but a portion of the workers sometimes fools their sovereigns and lays another kind of egg – a reproductive one that makes males, the fruit of a kind of asexual reproduction.

“The nests of the guaraipo represent a society with a more flexible structure”, says Vera Lúcia Imperatriz Fonseca, a biologist from the Bee Laboratory of the Institute of Biosciences of the University of São Paulo (IB/USP). “The queens coordinate the work, but do not give that many orders.” In the nests of the honeybee, Apis mellifera, which is the point of reference for the scientists, internal relations are more rigid. There is just one queen, a centralizer, and the obedient workers toil on the construction and maintenance of the nest. The slaves lay practically no reproductive eggs – hormones produced by the queen inhibit the development of their ovaries. The honeybee workers never lay trophic eggs.

First described over 160 years ago, the guaraipo is a gentle, stingless bee, about 1 centimeter long, that usually makes its nest close to the ground, inside a tree trunk. It became the star in the project that Vera Lúcia is coordinating because of the behavior and apparently unprecedented social structure it displays. Her team, which includes researchers from the State University of São Paulo (Unesp) and collaborators in Europe and the United States, is studying the organization of the colony and the reproductive patterns of over a dozen species of bees native to Brazil, above all those of the Meliponinae subfamily.

These indigenous bees – thus called since they were already here, together with the first inhabitants of our territory – are important for several reasons. From the ecological point of view, they help to conserve biodiversity: they are superb pollinators of the Brazilian forests. For science, they are a unique subject of interest. Being typical of tropical regions, they are little studied abroad, and, to judge from the first results of the work on M. bicolor, they point to a formidable new line of research. In economic terms, the native bees generate earnings from the production of honey – usually in smaller quantities and more expensive than the honey made by A. mellifera – and they may be great allies of Brazilian farming,thanks to a peculiarity. Unlike the well-known and aggressive honeybee, they have no barbs and do not sting. This makes it less risky to handle them and makes them unrivaled pollinators for greenhouse cultures.

Only one thousand of the 30,000 known species of bees in the world form organized colonies and societies – the rest live in a solitary manner, or in colonies with a less complex organization. The classic model of structure for the colony is A. mellifera, with one queen leading the workers and the drones – the males – living outside the nest.

According to the foundations of behavioral ecology, the most efficient way of perpetuating the species – that is, to preserve its genes – calls for the workers to give up their reproductive function. The workers accept working for the queen – who is fertilized by more than a dozen males – just because this is the way that will generate individuals that are closest to them: other workers, all sisters, with whom they share their genes. If they had daughters, the complete workers (daughters of the same father and the same mother) would pass on only 50% of their genes. From the genetic point of view, it is more advantageous for them to have sisters than daughters.

With the guaraipo, as there is more than one queen in the colony, not all the workers are sisters. Some are cousins or have some other degree of kinship, in view of the fact that the multiple queens tend to be mother and daughter or sisters. In compensation, to strengthen family links, each guaraipo appears to mate with only one male, unlike what happens with the leading A. mellifera queen. But, in the end, the result is similar to that of the honeybee: there are genetic differences between the bees, regarded as sources of conflict in the colonies.

Tendency to split
In the guaraipo colonies, as in those of any species of bee, the queens are not lowered in rank, nor can a worker gain control of the nest or dominate their colleagues. Even so, fascinating things go on there. Although she has seen nests led by just one queen, Vera Lúcia has observed that the typical social structure for the guaraipos are hives with two or three queens, or sometimes four or five. This characteristic has been seen sporadically in other species, but not as a pattern for the species. “Nests commanded by more than one queen are a trait that is more common in colonies of wasps and ants”, she says.

But why are there colonies of guaraipo with many queens, when the pattern for social bees seems to be the A. mellifera? Nobody knows yet. It is thought that they may descend from more primitive species, or it could be the fruit of environments with little space, which would favor the coexistence of several leaders in just one nest.

The Dutch biologist, Dick Koedam, has beenin Brazil for four and a half years now. He left the University of Utrecht, to become a collaborator at USP’s Bee Laboratory (IB), and he has observed in guaraipo queens a behavior that is completely out of the usual. Like modern aristocrats, they even work. Once in a while, they produce wax, as has been proved by chemical analyses. “Melipona bicolor is fascinating”, says Koedam, who has already studied in Costa Rica the habits of another stingless species that is abundant in Brazil, the jataí (Tetragonisca angustula).

Another surprising fact withguaraipos: the queens live together in tranquility, with no great disputes, in a world where sharing leadership seems to be no obstacle to the development of the group. Experiments at the IB show that the removal of one of the queens in a colony with double command does not alter its organization. In the majority of cases, after a few months a second leader is created and accepted by the whole of the group, even by the first queen. This shows that for this stingless bee it is better to rely on multiple leadership than on a single command.

Fooled queens
The base of the guaraipo’s social ladder also provides some equally extraordinary facts. Vera Lúcia has gathered evidence that some workers can show individualistic behavior and cheat the queens. Her team has filmed nests in which a worker – a member, therefore, of the caste responsible for providing food and to build the cells where the queens deposit the fertilized ovule that will generate a descendent – plays a trick. She waits for one of the queens to lay an egg, and, when the leader leaves the place, she lays a reproductive egg, and, finally, closes the cell. Sometimes, another worker notices her colleague’s trick against the queen and decides to intervene: with an equally individualistic gesture, she devours the egg of her colleague in the caste and the queen’s egg, and – she too – lays a reproductive egg. Often there are a dozen workers acting like this, one after the other.

In nests of the A. mellifera, it is common for a worker to police the behavior of the others. It is not a banal event, but nor is it rare. If, in this species, the intention of policing is to guarantee the integrity of the queen’s eggs and to punish the workers who break the rules, with the guaraipos this surveillance can lead to a further transgression. In spite of this rebelliousness, the guaraipo workers seem to show no preference as far as the boss is concerned. They serve all the queens in the colony with the same dedication.

Vera Lúcia and her collaborators are convinced that some guaraipo workers are in fact specialized in laying reproductive eggs, an indication that the internal division of tasks in this species may show significant differences, compared with what happens in the nests of the A. mellifera. The attribution of functions among the workers of the honeybee is made basically in the light of the age of the members of the colony. In the course of its brief life (40 days in the summer, or 140 in winter), an A. mellifera worker performs all, or the majority, of the tasks reserved for this caste. With the guaraipo, this pattern is partly maintained, but some workers seem to dedicate themselves almost exclusively to laying reproductive eggs.

Sex of the bees
The reproductive behavior of the queens still intrigues. How many males do they mate with? It has still notproved possible to prove whether it is with just one or with several. The most accepted hypothesis comes from the work done in the USA with 70 colonies of several species of stingless bees. The conclusion is that a queen has to be fertilized by just one male. Vera Lúcia thinks that this ought to be the pattern for guaraipo behavior as well.

The studies of the system of communication between guaraipo queens and workers – in the hands of Carminda da Cruz-Landim, a biologist from the Institute of Biosciences at Unesp in – are at the initial stage. But there are already some results. It has been shown that the language of these stingless bees is fundamentally chemical in nature, based on pheromones; these are substances produced by glands, like the Dufour glands and the mandibular and tegumentary glands, which trigger off certain behavior, often with a sexual or reproductive meaning.

“We want to discover how the queens and the workers behave when faced by each substance produced by these glands”, says Carminda. “If we understand how these native species behave and structure their colony, we may be able to learn to handle the nests of the guaraipo and of others of the Meliponinae family. This knowledge may also have great commercial interest.”

Artists in pollination
The indigenous stingless bees, the so-called Meliponinae family, are allies of Brazilian farming. As spontaneous pollinators of the country’s native forests and more gentle than Apis mellifera, they can be used in hothouses to increase the productivity and quality of the crops. There are now studies that show that fruit pollinated exclusively by these bees are larger and taste better. In the Northern Hemisphere countries, where there is a generalized decline in natural pollinators, this kind of research is now quite commonplace”, says Vera Lúcia Imperatriz Fonseca, from USP.

In Brazil, bees have still not been adopted to pollinate plantations – not even the A. mellifera, which is seen just as a supplier of honey. But the situation is starting to change. In Atibaia, Kátia Malagodi Braga, a biologist, is testing the use of native bees to pollinate greenhouses of strawberries, a crop that is typical of the region. Of the five species of the Meliponinae family that were analyzed, one of them, the jataí (Tetragonisca angustula), shows itself to be an excellent candidate to perform this role.

Specimens of jataí would visit the flowers of the crop regularly, taking the pollen needed for fertilizing the plant. And when the actual strawberries were born, the jataís, unlike other bees, would do not damage to the edible part of the fruit. “The fruit that the jataís pollinate seem to me to be bigger and better”, says Osvaldo Maziero, a strawberry grower and the owner of the property where the experiment is being carried out. Katia also is satisfied with the results of the research. “To make headway, we now have to master the handling of the jataí inside strawberry greenhouses”, she says.

The Project
Organization of the Colony and Patterns of Reproduction in Indigenous Bees (nº 96/11093-2); Modality Thematic project; Coordinator Vera Lúcia Imperatriz Fonseca -Institute of Biosciences at USP; Investment
R$ 161,883.17 and US$ 106,471.00

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