by Colin Tudge
Flies are only bit players in the life of Annona sericea, but flies including midges are the prime pollinators of many a plant, including many a tree – and including the cocoa tree, Theobroma cacao. Again, the cocoa flower sacrifices part of itself – sterile parts of the flower – to encourage the midges: and again, the flower is organized in such a way that as the midge feeds it is brushed with pollen. The flowers are produced on the trunks and branches (this is ‘cauliflory’, so typical of tropical forest trees), and the midges breed mainly in the fruit pods which fall to the ground and decay. If the cocoa grower is too tidy, and clears away the pods, the cocoa loses its pollinators. Here, as in all of life, too much hygiene doesn’t pay. Many flowers that are pollinated by flies smell horribly, incidentally, imitating the rotting flesh that flies prefer; and some of them heat up to make it worse. (Most famous is the world’s biggest flower, Rafflesia, from Indonesia.)
But the best-known insect pollinators and probably the most important, are the bees. Some bees are very small. Some are extremely large, like the carpenter bees and bumble bees. Others are in between, like honey bees and the long-tongued (‘euglossine’) bees. Many are solitary, some live in small colonies like the bumble bee, and some in very large colonies like the honey bee. Many are generalist pollinators but some – especially among solitary species – are adapted to pollinate particular flowers, which in turn are highly adapted to them. Bees are strong fliers: studies in the Amazon in the early 1970s showed bees of the genus Euplasia returning to their nests when released from a distance of 23 kilometres. In the normal course of foraging they commonly fly many kilometres in a day, following a regular route from flowering tree to flowering tree according to the strategy known as ‘traplining’.
Some trees attract many species of bee: one study in Costa Rica in the 1970s showed that one leguminous tree (Andira inermis) attracted seventy different kinds, from middle-sized long-tongued bees to big carpenter bees. By the same token, many species of bee visit many different species of plant. But a few – particularly solitary bees – do have very close, specific relationships with particular trees, requiring a great deal of co-evolution between the two.
If a bee, on any one foraging trip, visited many different kinds of plant indiscriminately, then it would not be much good as a pollinator. It wouldn’t help England’s wayside roses, for instance, if visiting bees flew off and distributed their pollen among the local clover. But it turns out that on any one trip, most bees (more than 60 per cent in one study in the Amazon) focus on only one plant species and very few (only 15 per cent) visit three or more species per trip – and this of course makes them far more efficient as pollinators. Perhaps this focus reflects an ‘optimum foraging strategy’: a method by which feeding efficiency is maximized. Optimum foraging strategy has been studied most closely in birds. For example, if a pigeon is given a lot of barley with a few peas, it ignores the peas altogether. Confronted with a lot a peas and a few grains of barley, it ignores the barley. It pays a forager to get its eye in. By focusing on whatever food source is commonest, and is known to be reliable, the pigeon does not have to waste time in wondering whether any one item is a pea, or a barley grain, or a pebble. By the same token, if a bee once establishes that roses are in bloom, it tends to stick to roses. Let others focus on clover.
Furthermore, other studies have shown that once back in the hive, colonial bees exchange pollen with each other – not deliberately, but just as they mill about. So a bee that picks up pollen 5 kilometres to the east of the hive, may pass some pollen to another that is foraging up to 5 kilometres to the west – and trees that are 10 kilometres apart may thereby find themselves exchanging pollen. Of course, at different times of year the generalist bees switch from one species to another, as each comes into bloom, and thus ensure a year-round supply (or season-round, in temperate latitudes). Then again, although the bees may be generalists, individual species of tree seem to adjust their flowering strategy to the needs of particular types. Thus, in the Amazon, some trees flower in a ‘big bang’ fashion – a brilliant show of flowers in a short season; which ensures that bees in general will notice them. Others, however, favour the ‘steady state’ approach. They produce only one or a few inflorescences per day over a long period – and this tends to attract the kinds of bees, like the carpenter bees, that habitually fly long distances, and follow the same kinds of routes every day. This, then, seems to be a particularly good strategy for trees that are very widely spaced; but of course it relies on the regular habits and industry of a few species of bee.
In the forests of Amazonia the pristine ecology has been much interrupted and to a large extent pre-empted this past few decades by bees imported from Africa: the so-called ‘killer bees’. These are simply an African race of the familiar honey bee; and very good honey-makers they are too, favoured by many bee-keepers. They got into South America in the 1970s from a research laboratory in Sao Paulo in the south of Brazil, and spread at more than 200 kilometres per year. By 1982 they were already crossing Colombia, thousands of kilometres to the north of Sãao Paulo. ‘Killer’ is well over the top, but they are certainly aggressive both to people and to other insects. Thus in 1973 Ghillean Prance, near Manaus, observed the insects that came to pollinate Couroupita subsessilis, a relative of the Brazil nut. The visitors included wasps and bees. The only visitor the following year was the honey bee; not necessarily, but very probably, the African interloper. Presumably what Professor Prance saw in Manaus is common all over South America. Presumably, too, the African bees will sometimes do a good job; but in general, it seems unlikely that any one generalist, however aggressive, can pollinate the trees of the neotropics as efficiently as the droves of insects that have evolved specifically to the task.
Yet the Brazil nut itself might well be a beneficiary. Brazil nut trees are wonderful. They are emergent species, half as tall again as most canopy trees. Of course, too, their nuts are extremely valuable and so the Brazil nut is among a shortlist of Amazonian trees that it is forbidden to fell. So it is that when forest is cleared, the pastureland that is sown or grows up in its wake is punctuated by isolated Brazil nut trees, rather like the big solitary oaks in England’s stately parks, although the parkland oak trees are to the manner born and spread themselves most opulently while the Brazil nut trees, deprived in middle age of their companions, seem forlorn, magnificent but somewhat haggard. Furthermore, although the Brazil nut trees have been conserved mainly because of their nuts, when they are in the middle of nowhere they are liable to remain unfertilized. Most of their pollinators won’t fly over big open spaces. But isolated oaks in English parks, served by wind that’s laden with pollen from surrounding woods, have no comparable problem.
Enter, though, the African bee. Its aggression is matched by its energy, and it does apparently make the long trek out to the isolated Brazil nut trees. Introduced species on the whole are a bad thing – in fact, ‘exotics’ seem to be the chief cause of extinction of native species, apart of course from gross loss of habitat. But here at least, just for once, there is some compensation. ‘It’s an ill wind’, as the adage has it.
Birds are great pollinators too – notably, but by no means exclusively, hummingbirds. Like butterflies, they typically prefer red, which they see best. Mammals also. Some, like the honey possums in Australia or the desert rats in South Africa, are highly specific. Others, like the capuchin monkeys of Amazonia or giraffes in Africa, may pollinate their prey trees inadvertently (but nonetheless usefully) as they forage. But among the mammals, as with all creatures, the most efficient pollinators are the fliers: and with mammals that means bats.
There are well over 800 species of bats – among mammals, only rodents have more species. They are of two main kinds. The micro-bats live all over the world. Many – like the familiar bats of temperate lands – eat insects; but others live on mammalian blood (the vampires) or on frogs, or nectar and fruit. The mega-bats, which include the flying foxes, live exclusively in the Old World
. For the most part they are big and live largely or exclusively on nectar and/or fruit. They rely heavily on scent to find their food, as most mammals do. By contrast,
Trees (including many cacti) hold their flowers high for bat pollination
the micro-bats locate their prey, whatever it may be, by echo-location: sending out a high-pitched squeak and analysing the echo. Both groups of bats are nocturnal. If they fly by day – as they sometimes are obliged to do, particularly in cold weather when there are too few insects flying at night – they are quickly picked off by hawks. Some studies have shown that day-flying bats rarely survive for more than a few hours. Mammals and birds both flourished in the wake of the dinosaurs and flying reptiles. But while the mammals came to dominate the ground, birds very definitely dominate the air. Bats are very successful – ubiquitous and various – but they are advised to stick to the hours of darkness. Even then, they must avoid the owls.
Trees that would be pollinated by bats must adapt to them – just as they must to specialist bees, butterflies or moths. None has adapted to them more spectacularly than a relative of the mimosa: the Amazonian tree Parkia. Parkia has been studied in particular by Dr Helen Hopkins but it is everybody’s favourite, like a favoured sister, endlessly endowed. It is beautifully shaped, like a great flat-topped umbrella. Its leaves are doubly compound, like feathers. Its bark is smooth but not too smooth, in some species dotted with red. But most glorious of all are the flowers, pompoms of stamens and styles, bright red or pale yellow or bronze depending on species, that hang from on high on long thin threads like Christmas baubles.
The topmost flowers in each inflorescence are sterile, with copious nectar, which begins to flow early in the morning. By mid morning the first flowers begin to open, and all of them are open by mid afternoon. At dusk, the flowers begin to release their pollen. Then the bats come. By morning all the nectar has gone, the filaments that bear the anthers have wilted, and the flowers have faded. One of nature’s most glorious shows lasts only one night. Showbiz is not the point. Replication and multiplication is the point. One night is enough: as we have seen already, animal pollination can be remarkably efficient. The would-be pollinators are constantly alert.
So there are many specific, mutualistic relationships between many different kinds of tree and many different kinds of animal pollinators. But the most stunning relationships of all are between the world’s figs and their pollinating fig-wasps. Here we see, writ large, all that is involved: the exquisite precision of co-evolution; the sacrifice that the figs must make to entice the wasps; the constant temptation on both sides to renege; and the inevitable imposition of freeloaders (including parasites).
OF FIGS AND WASPS
All organisms are different but some, as George Orwell might have said, are more different than others. There is nothing quite like an octopus. There is nothing quite like a human being. And there is nothing, absolutely nothing, like a fig. Figs, as described earlier, are of two main kinds: the kind that grow as other trees do, when planted in the ground; and the kind that begin as epiphytes. The epiphytes in turn may be stranglers, encircling and throttling their hosts, or non-stranglers which, like banyans, begin aloft but contrive to make contact with the ground without crushing their hosts. (In the Solomon Islands, too, a few kinds of fig grow as climbers.) In all kinds, the young fruits take the form of ‘syconia’ (not ‘synconia’ as often printed). They are like fleshy cups, though almost closed at the top. The flowers, often hundreds of them, are borne inside the cups, facing inwards. The effect is womb-like, as D. H. Lawrence was not slow to observe. Each female flower contains only one ovule which, when the flower is pollinated, develops into a seed. If the flowers are not pollinated, then the entire fruit aborts – or that at least is what usually happens; for as we will see, there are twists. (Strictly speaking, a syconium does not become a fruit until the seeds are fertilized. But it is convenient to use the term ‘fruit’ to mean syconium.)
The flowers inside their syconia are pollinated by small black fig-wasps. A female fig-wasp enters the syconium through the hole at the top, and lays her eggs in some (up to half) of the flowers. A wasp that colonizes a fruit establishes a new generation of wasps; and so she is called a ‘foundress’. After she has laid her eggs, she dies. The fruit becomes her sepulchre. Each egg hatches into a larva, which feeds upon the developing seed within its allotted flower (which of course kills the seed). Then the larvae pupate, each one still in its flower, until they emerge as adults. At least half, and often more than 95 per cent, of those new young wasps will be females; less than half, and often fewer than 5 per cent, will be male. The males are wingless. They emerge before the females, chewing their way out of their respective seeds. Then they chew their way into seeds containing females, and mate with them while the females are still inside. Then they too die. The newly-emerged females, already with sperm on board, now fossick around inside the syconium, picking up pollen from the male flowers, although they do not apparently feed on it. Then they fly off to found a new generation in a new syconium. These young females are laden with pollen and so they fertilize the flowers of the next syconium.
Some species of fig-wasp are ‘active’ pollinators, and some merely ‘passive’. The active pollinators have specific adaptations that include special sacs for carrying pollen, which they conscientiously fill; and when they reach the new fig tree, they equally conscientiously place the pollen on the stigmas of the female flowers within the syconium. The passive pollinators merely mill about before they leave the syconium of their birth and so become covered in pollen; and scatter it equally haphazardly in the next fruit they visit in the next fig tree, in which they lay their own eggs. However, some apparently passive pollinators also have specific pollen sacs – suggesting that they are descended from ancestors that were more meticulous.
The syconium (fruit) of a fig is both womb and sepulchre
The net result is a wonderful mutualism. The figs benefit, because they get their flowers pollinated, and so are able to set seed. The wasps benefit, because they are supplied with a good, safe place to lay their eggs, and a food supply for their larvae. Without the wasps, the figs could not reproduce, and so would die out; and without the figs, the wasps could neither reproduce nor feed. Although the wasps are small they fly prodigious distances, so any one fig tree may spread its pollen over 100 square kilometres. Indeed, in the gallery forests of Africa it seems that individual wasps may carry the pollen from some trees hundreds of kilometres: presumably the wasp rises into the upper air currents, and is whisked along (though how it knows when to descend again, and how it does so, is not at all obvious). This has been discovered not by studying wasps directly, but by DNA studies of the figs, which reveal that any one fig may have daughters living a very long way away.
Figs are immensely successful. More than 750 species are known – more even than oaks or eucalyptus – and they thrive throughout the tropics, both Old World and New, and into the subtropics. Extraordinarily – indeed it all starts to seem miraculous – each kind of fig has its own species of symbiotic wasp. Each wasp co-evolved with the fig it pollinates.
This, at least, is the basic story. It was beginning to unfold even by the 1940s, and has been steadily expanded since by generations of biologists. The research has been outstanding. It is difficult to do, but figs are of tremendous ecological importance – the sole or the stand-by food supply for hosts of forest creatures; and the study of mutualisms, as Darwin himself first noted, is a rich source of evolutionary hypotheses which also offers the means to test them. Modern techniques, including molecular methods that enable researchers to explore the evolutionary and genetic relationships between different figs and different wasps, are enriching the insights month by month. The following account is based mainly on the extraordinary studies over the past two decades by Dr Edward Allen Herre and his colleagues at the Smithsonian Tropical Research Institute (STRI) in Panama (which I was privileged to visit in 2003).
To begin
at the chronological beginning: How did the precise relationship between fig-wasps and figs – basically one fig per wasp, with hundreds of species of each – first evolve? It is impossible to reconstruct history with certainty, but modern investigations are providing many intriguing insights. ‘
First, genetic and anatomical studies show that all the wasps that pollinate figs are descended from a common ancestor. Comparable studies suggest that all modern figs are also descended from a common ancester. The two facts together imply that the present-day mutualism of figs and their pollinating wasps evolved only once. All the 750 species of fig and their corresponding wasps are descended from one kind of fig and one kind of wasp that first appeared a very long time ago. Furthermore, as each lineage of figs divided to form two daughter species, so the wasps that pollinated them also divided into two new species: a new kind of wasp for every new kind of fig.
What was the first of these wasps like? Genetic studies suggest that of all the several genera of present-day fig-wasps, the most ancient is Tetrapus. This is a passive pollinator, and its various species pollinate a group of closely-related figs that live in South America. Perhaps, then, the first ever fig–wasp mutualism was established between the ancestor of those South American figs and a Tetrapus-like wasp; and presumably it was first established in South America, where the most ancient kinds of fig-wasps, and their corresponding figs, still reside.
When did this fateful liaison take place? A few years ago such a question would have led only to the waving of arms, but modern studies of DNA provide at least the outline of an answer. For DNA changes little by little over time – not simply because of pressures from natural selection, which cause it to evolve in quite new ways; but spontaneously, simply because, as it is copied and re-copied, generation by generation, mistakes creep in. The point of DNA is to provide the code on which proteins are based. But in plants and animals (and fungi and protozoans and seaweeds) most of the DNA does not seem to code for protein. Indeed it seems to be more or less functionless, or at least its function is unknown. Small mistakes in the ‘non-coding’ sections of DNA seem to make little or no difference to the life of the creature, and natural selection fails to weed them out. Thus over time such mistakes accumulate. They do so, furthermore, at a fairly regular rate – so that by measuring the difference between the non-coding bits of DNA of two different creatures, it is possible to see when they last shared a common ancestor. The (fairly) steady change of DNA over time is sometimes said to provide a ‘molecular clock’.
