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Night in the arid outback

Botanists from Pernambuco State throw light on the peculiarities of pollination in the Caatinga

isabel machadoThe bat Glossophaga soricina visits the cactus Pilosocereus catinguicola: reciprocal benefitsisabel machado

When night falls, bats take over the skies of the Caatinga (scrubland). Not in search of blood, not just because they are a minority in the blood sucking species of these mammals, but in search of nectar – especially from the flowers of the cacti that bloom in the twilight, white or greenish, sort of glowing in dark. Less numerous among the pollinators of other Brazilian ecosystems, bats correspond to 13% of the animals that, by transporting pollen, guarantee the reproduction of plants in the Brazilian Semi-Arid region. They lose out only to bees and hummingbirds, according to a study carried out by a team from the Federal University of Pernambuco (UFPE) that evaluated the peculiarities and the frequency of pollination of one hundred and forty-seven vegetal species within the Caatinga – both trees and creeping plants. In the Cerrado (Wooded savanna), on sand bars and in the humid forests, bats are generally found at the bottom of the list of pollinating agents, with a percentage up to ten times smaller, even falling behind wasps, beetles, moths, butterflies and flies.

Probably attracted by the abundance of cacti or by the caverns, these impressive animals take up the role of angelical cupids in the middle of the outback’s flora. In this case the arrow is a prolonged snout and the target is the stigma – the structure of the flower that receives the pollen, a fine powder formed by the male reproductive cells, liberated by stalks called anthers. And it is while searching for nectar, a liquid rich in sugars that serves as a food, which the nectar feeding bats extend out their straight, cylindrical and reddish tongue, on whose point there are tufts of short hairs called papillas, and they end up rubbing their snout or another part of their body on the pollen. Stuck onto the shin of the bat, the pollen is then transported to the female reproductive organ of the flowers. Almost always pollen depends on an external agent – the wind, animal or water – in order to reach the stigma of the same or of another flower: and when this occurs the male and female cells meet up and fertilization occurs.

This is the way that the bat enters into the life cycle of the cacti, which belongs to one of the most abundant plant families in the Caatinga, with forty one species that are endemic or restricted to this ecosystem, the only one exclusively Brazilian, spread over 800,000 km2 in the interior of the Northeast Region. Everything between the two – bats and cacti – seem to fit together, in an intricate evolutionary puzzle. The flowers of many of the cacti species are nocturnal, like the bats, and as well they are lightly colored, since in the dark red and orange make little difference to these animals as they see badly.

Scent, this for sure, is the big attraction. “The bat’s sense of smell is more developed than its vision, and for this reason the strong and sweet odor of the cacti’s flowers, very nauseating to us, makes more difference than colors”, says the biologist Isabel Cristina Machado, the study’s coordinator, carried out in conjunction with Ariadna Lopes, also from the UFPE, and published in the British magazine Annals of Botany. These flying mammals also have their incisor teeth atrophied, which facilitates the passage of their extensive tongue with which they collect the sweet nectar. This is the case of the Glossophaga soricina, a small bat – weighing around 10 grams – with dark brown skin and close to 20 centimeters in wingspan. It looks like a rat with wings.

Fear and cold
Taking photographs to register and identify the bats was a test of fire for Isabel, who did not hide the fear that she sometimes felt towards them. “There were moments when they were so close, that I thought they were going to run into me”. Other difficult moments for her and Ariadna were the hours and hours of observation, at night, when it gets cold in the outback. “We ended up with pains in the neck as we had been so attentively targeting the flower so as not to loose a photo in the case of a visit, which lasts only fractions of a second”, says Isabel. She and her partner Ariadna confirmed the processes of pollination of ninety nine (99) species of plants in three areas of the Caatinga in the state of Pernambuco: the vicinity of the municipality of Alagoinha, some 200 km from the coast; the National Park of the Catimbau Valley, at Buíque, some 285 km inland; and an experimental station reserve of the Farming Research Company of Pernambuco State at Serra Talhada, some 700km from the capital city Recife.

A single flower of Xique-Xique (Pilosocereus gounellei) or of Facheiro (Pilosocereus pentaedrophorus), species exclusive to the Caatinga, or of any other chiropterophilous cactus – pollinated by bats -, produces up to 200 micro liters of nectar per day, a volume fifty to one hundred times more than that liberated by other plants, which, being more stingy, offer to their pollinators only 3 to 5 micro liters of sweet food. “This quantity of nectar of the cacti flowers is a reward for the bat’s visit, a pollinator which is much larger and needs more food than a bee”, underlines Isabel.

The greedy bat is only matched by the hummingbird, another pollinator of the semi arid region, which replaces the energy needed for its flight with lots of nectar. This is the case of the hummingbird known as the Broad-tipped Hermit (Phaethornis gounellei), a species with a long and curved beak, native to the Northeast, found in stretches of the Caatinga from the states of Piauí to Bahia, which normally visits bromeliads during the daytime. With the hummingbirds the relationship is different: instead of smell, as happens with the bats, what attracts these birds is the color of the flowers. Red is the favorite color not only of the humming birds, but of birds in general.

Bees, on the other hand, appear to be less demanding: they visit lilac, blue, yellow, violet and orange colored flowers. However, the two botanists from Pernambuco drew attention to the fact that it is not possible to deduce who  the pollinator is only by the color of the flower. The most detailed analysis have taken into account a series of other characteristics of the flowers, such as their shape, smell, size, the moment during the day in which they blossom and the reward that they offer to the animals that transport the pollen to the stigma – some also offer floral oils as well as nectar. “One variable could well exclude another”, says Isabel. “The red flower of a bromeliad or of a cactus, generally without smell, is associated with pollination by way of humming birds and other birds, which don’t have a well developed sense of smell. Bees, for their part, don’t see red very well, but they sense the smell.”

With the legs
Average and large sized bees, from 1.2 to 3.0 centimeters in length, are the leading pollinators in the Caatinga, where they help in the fertilization of 30% of the plants. They are also the main group of pollinators in the Cerrado with 65%, in sand bars (41%) and in the humid forests, such as the Amazon and Atlantic Rainforests (25%). It is also the animal that best makes use of the resources offered by the flowers of the interior of the Northeast Region. There are bees that collect everything: nectar, a high calorie food; pollen, rich in proteins; floral oils, a food for the larvae; and resins, used in building hives. Even at that there are particularities. “Neither bats, nor humming birds, nor flies, indeed no other pollinator but the bee collects floral oils”, says Isabel. If a plant offers only oils, one can conclude that we are dealing with a plant whose pollination is restricted to bees. Even at that, it is not just any old bee: only those bees of determined families, such as the Anthophoridae, with brown species and others almost black, whose back and middle legs have rigid bristles that form a sort of comb and facilitate the collection of the oil produced by the flowers.

After dozens of observations each of more than four consecutive hours duration, which resulted in lots of insect bites, Isabel discovered that the bees that landed on the lilac, bluish or even purplish flowers of a small bush called Angelonia pubescens carried out the pollination of the plant whilst they collected oils from the flower in two bags located in the petals. “The bees collect the nectar with their tongue, but the oil has to be with the legs”, observes the researcher from Pernambuco. “In both situations, the collecting of the pollen in the flowers is passive, non-intentional.”

The bee named Centris hyptides literally fits itself into the flower in order to collect the nectar. Brown, of around 1.5 centimeters in length, this species, unique to the Northeast outback, lands on the flower to pick up the oil which is in the smaller petals. It’s as though it grabs the flower with its legs. The back of the insect rubs against the stamen – the flower’s masculine structure – and conducts the pollen to the stigma. This species has elongated hind legs, a peculiarity that confers to it more efficiency in the collecting of the oils of the Angelonia flowers. The most common situation for the three legs that the bee has on either side of its body, is that the longest pair is those in the middle.

Another bee exclusive to the Caatinga and adapted to the pollination of a small herbaceous plant is the Tapinotaspis nordestina, which is almost 1.0 centimeter in length, and this one indeed has its middle legs elongated. This species was registered by Isabel’s group in 2002, starting from examples collected near Buíque. This was not the only one. During these two years, specialists in the classification of bees have given names to another four species up until then unknown, based on the examples that
Isabel and her group collected in the Caatinga.

There is the Tapinotaspis nordestina that guarantees the pollination of Angelonia cornigera, one of the creeping plants studied, as it lands on the flower at the time of oil collecting, in a kind of hug. It is with this oil, rich in lipids (fats), that these insects feed their larvae. Because of situations such as this, advised Dr. Isabel, very often the pollination does not secure the reproduction of only the plants, but also of the pollinators themselves.

This dependency of a determined flower in relation to a species of animal and vice-versa, nevertheless, is more of an exception than the rule. What predominates is a generalized relationship. Or that is to say, a plant is ornithophilous (pollinated by birds), but its flowers are not visited only by a unique species of bird. “In the majority of cases”, the researcher explained, “the dependency is not on a one to one scale, but to a group of animals to a plant or group of plants. For example, humming birds are generally not just pollinators of a particular species, but of various”. Very often the plant’s reproduction structure itself, especially when the flowers are more open, allows for pollination by more than one group of animals. One is dealing with a survival strategy, since, the more the number of pollinating species, the smaller are the chances the plant has if one pollinator were to become extinct.

Orchids are an exception, by being pollinated by specific groups of bees and they maintain their flowers open for up to a month, whilst the norm is that the flowers last a morning or a night. Nevertheless, in one thing the orchids are the same as the almost one thousand known plants in the Caatinga, as in other ecosystems and in our own back gardens: after receiving a visit from the pollinator their petals become soft and fall off. To maintain a flower open and attractive for days on end requires a lot of energy.

If this extra dose of energy already demands a lot from the plants living in humid environments, imagine this in the Caatinga, where it rains 50 to 90 centimeters per year, less than half of that which annually falls in the Atlantic Rainforest. During the dry season, which can extend up to a period of six months from July until December, many plants lose their leaves as a way of reducing transpiration and of resisting the lack of water. But it is exactly during this period that flowering can be at its most exuberant. The result is a spectacle of red, yellow and lilac points in the middle of the gray of the branches and dry tree trunks.

The Project
Syndromes of pollination, Sexual systems and floral resources
of the Caatinga species  in Pernambuco State and the Pollination systems of species occurring in the Caatinga vegetation: ornithophilic and chiropterophilic; Modality Research Assistance (Facepe) and a Scholarship for Productivity in Research/CNPq; Coordinator
Isabel Cristina Machado – UFPE; Investment R$ 11,023.00 (Facepe) and R$ 24,000.00 (CNPq)