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A ladder to investigate the sex of trees on the Unicamp campus

Biologist braves rainy mornings to watch the opening of flowers and the visit of pollinators to rare species with economic potential

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A long ladder, carried with the help of fellow researchers to reach the flowers of trees 7 to 10 meters high, was a fundamental tool that biologist Marília Claudiano Tavares used for her master's thesis. She investigated whether a species of tree that is part of an economically important genus in Brazil, fortunately found on the Unicamp campus in Campinas, was capable of reproducing naturally even outside its original environment threatened by deforestation. “It was not easy to spend the night on top of the trees following the anthesis (opening) of flowers, observing flower visitors and making crosses. At some collection times it was raining. So I really needed someone there to encourage me”, recalls the biologist.

A long ladder, carried with the help of fellow researchers to reach the flowers of trees 7 to 10 meters high, was a fundamental tool that biologist Marília Claudiano Tavares
Biologist Marília Claudiano Tavares at the top of the long ladder to reach the flowers of trees 7 to 10 meters high

Marília Tavares studied the “Reproductive biology and floral morphology of Spondias macrocarpa Engl.”, supervised by professor Sandra Maria Carmello-Guerreiro, from the Department of Plant Biology at IB-Unicamp. “It is very difficult to find this species in natural areas, precisely because of the loss of territory through deforestation and perhaps because its reproduction is being interfered with. Within the genus there are several sexual systems, from monoecy to dioecy, and several subtypes. There are plants that need to save resources when reproducing and, therefore, these variations arise to optimize their reproduction. Nothing was known about the sexual system of this species.”

The author of the research explains that species belonging to the genus spondias are very close relatives, sometimes identified only by the morphology of the fruits, such as cajá (Mombin spondias), umbu (tuberous spondias), seriguela (spondias purpurea) and cajá-manga (Spondias dulcis). More recently it was discovered that the cajarana (or umbu-cajá) was another species, called Spondias bahiensis. “The fruit of our species in question, Spondias macrocarpa, has several popular names and, therefore, there is some confusion, being also called cajarana in some places and cajá-mirim in others. The fruit is edible and is mostly used for juices, as it is sour and 'tastes' the mouth.”

For Marília, finding the Spondias macrocarpa on the Unicamp campus it was a find, as it is very rare in the natural environment and is also not cultivated. Of the 13 trees found, all of them distributed in front of Cecom (Community Health Center), eight were marked and studied, due to the difficulty of the height. “It is an endemic tree species with a very limited distribution, occurring only in the Atlantic Forest areas of the Northeast and Southeast (Bahia, Minas Gerais, Espírito Santo and Rio de Janeiro). It is considered a vulnerable species since many specimens in herbarium collections come from areas that are no longer forested.”

The biologist believes that her research, carried out from October 2017 to December 2018, can contribute to reproductive success and fruit production. Spondias macrocarpa. “We discovered, for example, that this species is self-incompatible, that is, it cannot reproduce if it is completely isolated in the environment, as it depends on pollen from another plant for fertilization. Which led us to another conclusion: its dependence on pollinators for fruit formation to occur; and, even so, fruit production was relatively low when there was this cross-pollination.”

One hypothesis raised by the author of the research is that perhaps the pollinators available in urban areas, as in this case, are not as efficient as pollinators from original areas, which shows the importance of conserving their natural habitat, which is the Cerrado, to ensure the perpetuation of the species. “For cross-pollination to occur, it is essential that plants offer resources to attract floral visitors. In the species on the Unicamp campus, the main pollinators were bees, with Trigona spinipes [arapuá, without sting], Tetragonisca angustula [yellow jataí] and Apis mellifera [European] those that contributed to the greatest number of visits.”

Professor Sandra Guerreiro
Professor Sandra Carmello-Guerreiro, supervisor of the study with Marília Claudiano Tavares and Elisabeth Tölke

According to Marília Tavares, in addition to pollen, other resources may be present, such as nectar, oils and resins. It is in the flower that the main resources are located and where the production and shelter of gametophytes occurs. The most common floral type is the bisexual flower, which has a calyx, corolla, androecium and gynoecium. Some flowers appear to be hermaphrodites, but with non-functional gynoecium or androecium. “When the latter case occurs, determining the sexual system may be difficult due to erroneous interpretations of morphological studies. Species of the genus Spondias L. have different descriptions in the literature for the sexual system, making the genus interesting, from a morphological point of view, to understand the different strategies used by plants in search of reproductive success.

Thus, the biologist clarifies that her work aimed to determine the sexual system of Spondias macrocarpa through detailed floral morphological analysis, pollen viability, stigmatic receptivity and controlled pollination experiments. All collected material was processed and analyzed under optical light and scanning electron microscopy. Furthermore, the development and architecture of the inflorescence, floral longevity, stigma receptivity, pollen characteristics, reproductive system and floral visitors were monitored. “In morphological studies we identified bisexual flowers and functionally male flowers in the same individual, characterizing the andromonoic sexual system.”

Holding the ladder

Professor Sandra Carmello-Guerreiro, dissertation advisor, was one of the people who contributed with Marília holding the ladder and keeping her company during the early hours of the morning observing the trees, together with post-doctoral students Elisabeth

Tölke and Carlos Pereira Nunes. They are all involved in studies of Anacardiaceae, which is from the same family as Spondias macrocarpa. "The family Anacardiaceae It is widely distributed in the tropics and in particular in Brazil. Several species of the family are cultivated outside their natural environments, due to their ornamental, food (mango, cashew, pistachio and others) or timber (mastic) importance”, explains the IB professor.

Post-doctoral student Carlos Eduardo Pereira Nunes contributed to the study by identifying pollinators, crossings and statistics
Post-doctoral student Carlos Eduardo Pereira Nunes contributed to the study by identifying pollinators, crossings and statistics

According to Sandra, although the species in the family Anacardiaceae present a certain homogeneity in relation to floral morphology, this homogeneity hides a great variation in reproductive processes, which is the research object of this master's thesis. “This is just one of the important aspects of deeply studying sexual processes in these species, as they can act, together with other biotic and abiotic factors, in the diversification or extinction of clades [organisms originating from a single ancestor]. Understanding how this occurs in a small universe, whether of a species or a genus, will help us collect data that will be useful in macroscale analyses, the focus of our future research.”

Elizabeth Tölke¸ master and doctorate from Unicamp and now postdoctoral student at USP, contributed to this study on Spondias macrocarpa in terms of morphology, anatomy and above all in motivation, even during collections in the rain, as the author of the dissertation recalls. “Marília’s work made a significant contribution to our research group. We already have a lot of experience with the family Anacardiaceae and the reproduction of these plants has always intrigued us, as they exhibit an enormous diversity of sexual and reproductive systems, without almost anyone dedicating themselves to studying them. I guided her in the experimental part and in processing the results.”

Remembering that there are several species of the genus spondias taking place in Brazil, Elisabeth justifies the choice of S. macrocarpa as it is within the Unicamp campus, facilitating experimental work in very tall trees, which would be unfeasible in open areas such as the Cerrado. “Marília was very brave in her observations and experiments, climbing trees to bag the flowers and carry out artificial crossings. The result was an article with a lot of new information for the species and genus. We describe the andromonoic sexual system for S. macrocarpa and their dependence on pollinators for reproduction.”

The postdoctoral Carlos Eduardo Pereira Nunes, better known as Coquinho, contributed to the study by identifying pollinators, crossings and statistics – the ecological part – and also carrying the ladder and equipment. “Although the flowers all look the same, the same bunch has male flowers and others with two sexual functions (hermaphrodites) – this is what we call andromonoecy. Large trees depend exclusively on small insects to carry pollen from one tree to another and generate fruits and seeds. There is probably an incompatibility genetics between the pollen and the female structures of the same tree, meaning that self-pollination fruits do not form: pollen from a flower on the same flower or on another flower on the same tree. The job of carrying pollen from one tree to another is done by small insects, mostly stingless bees, but also beetles and flies that visit the flowers in search of food.”

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The main floral visitors of Spondias macrocarpa were bees

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