by Colin Tudge
As a preliminary observation, the scientists showed that when the temperature is only 5° to 10° C higher than the ambient temperature at midday, the pollinator wasps of Panama (or at least two species of them) are incapacitated or die. But, say Dr Herre and his colleagues in a paper published in 1994, ‘Such lethal temperatures would be expected in objects exposed to full sunlight.’1 And ‘such objects’ include the syconia of figs, hanging on their trees. So they measured the temperature inside syconia – and found that they stayed more or less as ambient: still comfortable for the young wasps developing within them. Even on the fiercest days, the temperature within small syconia never rose above 32°C, which wasps find perfectly acceptable.
Yet there was a greater oddity. For although the physical theory is complicated, it suggests that small fruits should find it easier to stay cool than large fruits do. But in fact, the larger fruits were often even cooler than the small ones. So how do figs in general stay cool? And how is it that the large ones – apparently in defiance of physics – tend to be the coolest of all?
Perhaps, the scientists surmised, the large fruits cooled themselves by evaporation, as leaves do, or as mammals do when they sweat. Evaporation would be effected, as in leaves, via holes (stomata) in the syconium surface. To test this idea, the scientists simply covered the figs in grease, to block the stomata. Sure enough, the temperature inside the big syconia then rose by about 8°C. When the outside temperature was at 29°C (which is common enough), the temperature inside the big greasy fruits rose to around 37°C – hot enough to kill the wasps inside within about two hours. Small fruits do not need such refinements. They have no stomata, or very few.
So the big fruits can keep themselves cool – but only at a cost. They have to waste a considerable amount of water to do so. We have already seen two reasons why small syconia seem preferable to large ones. There are more male wasps in the big syconia (because there are more foundresses), which is wasteful. The nematodes are more virulent in the big fruits (because there are more foundresses), which is wasteful again. Now, to cap it all, the big fruits have to waste water, a precious commodity, just to keep themselves cool. So why do any figs have big fruits? How could natural selection have favoured such an apparent absurdity?
I must delay the answer still further. It lies under the heading of seed dispersal, the generalities of which we should look at first.
SCATTERING OF SEED
Many plants, temperate and tropical, rely on animals to disperse their seeds. As with the pollinators, the relationship is mutualistic, with give and take on both sides. The tree gets its seeds dispersed, to be sure. But animals cannot afford to run charities, and they must have their quid pro quo. Sometimes they expect to eat a proportion of the seeds, and so squirrels typically eat at least as many acorns as they scatter. When trees produce fleshy fruits, animals may simply consume the pulp and then either spit out the seeds (as monkeys may often be seen to do with machine-gun efficiency) or else allow them to pass through their guts (whereupon they are deposited with their own consignment of fertilizer).
Always, though, and inevitably, there is tension. If a particular tree evolves to become dependent on a particular disperser, and the disperser disappears, then the tree might disappear with it. Thus many a seed seems simply to languish in tropical forests – though perhaps in the past dispersed by long-gone dinosaurs or some extinct giant mammal. On the other hand, if the dispersers become too common then they may eat too many of the seeds, and then the tree is also liable to die out. Balance is all. Many thousands of examples could be cited, but a couple must suffice.
The first is the almendro tree, Dipteryx panamensis, from the Fabaceae family, which grows on Barro Colorado Island in the heart of Panama, which for many years has been studied by scientists of the Smithsonian Tropical Research Institute. Egbert Leigh, who has worked on the island for the past thirty years, introduced me to the almendro one very rainy morning. It is indeed lovely, with bark the colour of pale pink salmon and a trunk that forks and forks again to produce, says Dr Leigh, ‘a graceful, somewhat hemispherical crown of compound leaves spiralled around its twigs’.
There is only about one almendro per hectare on Barro Colorado: but that is a fairly typical number for a tropical forest tree. Come June and July, it produces fine bunches of pink flowers at the ends of its twigs. These are apparently triggered by the onset of the rains, in late April and early May. Certainly if the start of the rainy season is not clearly marked – if, for example, the previous dry season is not as dry as it should be – then the almendro produces far fewer flowers, and so far fewer fruits. This is bad news for Barro Colorado’s animals, for the almendro is a serious food tree. Thus small quirks of weather can have far-reaching effects. As global warming continues to bite, we can expect the weather to become quirkier and quirkier.
The fruits, as befits a legume, are produced in pods: a hard wooden pod covered in a thin layer of sweet green pulp, with a single big seed inside; twenty or more fruits per square metre of crown in a good year. This is a prodigious crop and, says Dr Leigh, ‘swarms of animals flock to the feast’. Some take the fruit directly from the trees. These include some carnivores like the kinkajou and coati (many carnivores are omnivorous – notably bears), and also monkeys, bats and squirrels. Some take the fruits from the ground, including agoutis and pacas, which are big relatives of the guinea pig (and resemble small antelope or deer), spiny rats (also related to guinea pigs, rather than to rats), peccaries (New World pigs), and the occasional tapir. Many of these feasters simply eat the sweet pulp around the wooden pods. But some – notably peccaries, squirrels, spiny rats and agoutis – gnaw through the hard casing as well, to the bean inside.
Most of the feasters are bad news for the almendro: they eat, but they do not disperse. Squirrels eat but are poor dispersers. Monkeys can be useful: sometimes they eat the fruit where they find it, but sometimes they carry it away from the tree. A young almendro, as is commonly the way with tropical forest trees, will not grow close to its parent. Wide dispersal is necessary. For this, the most important disperser by far is Barro Colorado’s largest fruit-eating bat (although it still weighs only 70 grams). Fruit bats do not hang around on fruiting trees. If they did, they would be picked off by the meat-eating predators that also lurk in trees (waiting for the fruit predators), or by owls. Instead bats carry the fruit some distance away to a quiet roost where, says Dr Leigh, ‘they can chew off the pulp in peace’.
But mere dispersal is not enough. The seeds of the almendro also have to be planted. Bats do no planting. But when they drop the pods (they are interested only in the pulp around the outside), these are found by agoutis, which eat some of them with the seeds inside, but also – like temperate squirrels with acorns – bury some against leaner times. In some years almendros bear fruit while other trees bear very little, and then the agoutis eat all the almendro fruit. If other fruit are available, then some almendro fruit pull through.
Clearly, this process of seed dispersal is extremely chancy. The fruits and seeds of the almendro must first run the gauntlet of a whole range of animals, most of which simply gobble them up. Eventual success depends on the good offices of two very different kinds of animal: the fruit bat in the air, and the agouti on the ground. The bat does not eat the seeds themselves, and so is a reasonably safe ally. But the agouti does eat the seeds and is useful to the tree only because it sometimes fails to eat all of them. Partly this may be because it is simply forgetful (although it is always likely to find the young germinating almendros). Agoutis may fail to recover all their buried booty too because, between the burial and exhumation, they are themselves eaten, notably by ocelots, the mid-sized spotted cats of South America. But the almendro also contrives to satiate the agoutis – to produce more seed in a given year than the agouti ever gets around to eating. Big crops matter. This is why the almendro and other such trees need to produce good crops. A poor crop (caused by quirky weather) means total wipe-out for the particular ye
ar.
But, says Dr Leigh, the almendro has not been replacing itself on Barro Colorado. There are very few young trees. Perhaps, he says, this is because the island has too few ocelots, and so has too many agoutis: too much of a good thing. So perhaps we should say that the safe dispersal of almendro seeds requires three kinds of animal – fruit bats, agoutis, and cats to keep the agoutis in check. It seems a very precarious existence. But up to now it has clearly worked, or there would be no almendros – and this year (2004) there are some saplings since such ocelots as there are have apparently reduced the agoutis.
Clearly, though, overall diversity is necessary for the survival of any one species. The elusive concept of natural balance matters. Trees are not adapted simply to the presence of particular animals. They are adapted to their whole environment – climate, flora and fauna. But among the whole, they are particularly reliant on particular allies.
My second tale is an anecdote from a different continent – but it again shows how the fate of trees depends so much on the caprices of environment, and (increasingly) on the whims of human beings.
At the magnificent Forestry Research Institute in Dehra Dun, near the foothills of the Himalayas, Dr Sas Biswas likes to show his students an impressive row of Chukrasia velutina that form one side of an avenue along one of the main streets across the institute’s huge campus. Chukrasia is a relative of the mahogany, and these trees grow tall and straight — and, along this roadside, they are perfectly evenly spaced. The question he puts to the students – and to me – is, ‘Who do you think planted them?’ All who are asked pluck various plausible bigwigs out of the air while Dr Biswas looks on with mounting glee. Pandit Nehru? Gandhi himself? Some passing British royal? Finally when the students run out of steam he reveals the answer: ‘Ants!’
How can it be? It is easy to see how ants might help to plant a tree. They could carry the seeds to their nests if the seeds are small enough. Those of Chukrasia ate. only a couple of millimetres long and ants are prodigiously strong. But how could they space the seeds so neatly? Colonies of ants are often compared to armies, yet they receive no military training. They do not naturally distribute themselves so evenly, or in lines as straight as the cavalry’s tents at Balaclava.
On the sites where the trees now stand, there once were small beds of the white-flowered Tabarnaemontana coesnana, a relative of the oleander, planted for decoration in brick containers and regularly spaced. Sas Biswas remembers them from the 1970s as he rode past them every morning on his bicycle (people tend to stay a long time at the FRI). This plant repels most insects. Only the ants have learned to live with it. So they did carry seeds to the beds of flowers – from an old, big, mother tree that’s still growing on the other side of the road’ – and the seeds that the ants didn’t eat themselves escaped the attentions of other insects too. So the surviving seeds germinated s— one or two within each small bed. And so, within the working life of Dr Biswas, they have sprung up – ‘Before my eyes!’ he says, with a huge smile.
But for one of the most intricate stories of seed dispersal we must return to the figs.
WHY SOME FIGS HAVE BIG FRUITS DESPITE EVERYTHING: THE MYSTERY SOLVED
The syconia of figs qualify as bona fide fruits when the seeds within are mature and ready for scattering. Many animals come to prey upon them. Many, like monkeys, may do some dispersing at the same time, but on the whole are destructive. The figs’ main allies at this stage of its life, dispersing its seeds without taking more than their fair share, are various birds, and fruit-eating bats.
Each species of fig produces either red fruit, to attract birds, or green fruit, to attract bats. Fruit-eating birds hunt by day and rely on vision, and bright red does the trick. Among the birds, manakins are the main specialist fruit-eaters, while tanagers, tyrant flycatchers and woodpeckers are opportunist feeders, taking what’s on offer but happy to eat other things as well. Bats hunt by night, and for them plain green will do. In fact, fruit-eating bats are less active on nights of the full moon when there is more light, than on dark nights. On moonlit nights they are picked off by owls: a gothic encounter indeed. The birds that dispense figs are all of roughly the same size and so, accordingly, are the red fruits that have evolved to attract them. The fruit-eating bats are of various sizes. So, correspondingly, are the fruits they eat. Bats, unlike birds, carry fruit away from the tree to eat it at leisure elsewhere, in some more private roost. Perhaps this too is a defence against predators. Otherwise owls (or civets, or leopards) might simply hang around the fruit trees in wait.
So here at last, or so it seems, comes the answer to the puzzle – why figs bother to produce big fruits, which seem to cause them so much trouble. Big bats fly further than small bats. So on average, big fruits are dispersed more widely than small fruits. Dispersal, in tropical forest, needs to be as wide as possible. Big fruits seem to lose out at every turn but in the end, they are worth it.
This, at least in outline, is the fig story so far. Several morals are attached to it. The point that Allen Herre emphasizes himself, is how hard it is, in biology, to relate theory to what happens in the field. The basic interplay of figs and wasps is complicated enough; but then the complications multiply and multiply again as you stir in the cryptic wasps that look like pollinators but in fact are parasites, and the nematodes, whose virulence depends on the number of foundresses, and so on. However much we know about nature, we can never know enough. Science is wonderful – the studies that have led to the present understanding of fig-wasps are breathtaking: a brilliant amalgam of natural history, persistence, imagination and intellect – and yet the more that’s known, the more it seems there is to know.
Already it is clear, though, that if we do anything to interrupt the lives of the wasps – are too free with insecticide, for instance – then we will kill off the figs, or at least ensure that the present generation is the last. The fruits of figs are essential provender not only for bats and birds, but for a host of other creatures too. In Panama, figs of various kinds are in fruit all through the year while most other fruits are far more seasonal. There are times when figs are all there is. Take away the figs, and half the fauna could be in serious trouble. The whole ecosystem balances on a pin point – and we could tip it into oblivion without thinking; or indeed, we could let it slip through our fingers even if we were trying very hard to save it. On the other hand, precarious though it seems, figs and wasps have maintained their relationship in one form or another without interruption for more than 40 million years. There is robustness in the system. If only we can work with it, it might pull through yet.
Finally, given that so many trees rely so heavily on animal pollinators and dispersers, we might ask what happens to them if their allies disappear. One highly intriguing answer comes from the island of Mauritius, in the Indian Ocean.
THE DODO AND THE TAMBALACOQUE: A SAD TALE WITH A FAIRLY HAPPY ENDING
On the island of Mauritius lives Calvaria major, known as the tambal-acoque; one of the vast tropical family Sapotaceae. But in 1977 Dr Stanley Temple of the University of Wisconsin reported in the journal Science2 that the only tambalacoque trees left on Mauritius were all over 300 years old. There were no young ones. Since the tambalacoque lives exclusively on Mauritius, these ancients were the only ones left in the world. Yet the tambalacoque used to be common – common enough to be used for lumber. The remaining trees were fertile and were clearly pollinated, for each year they produced plenty of seed. So what was going wrong?
Perhaps, Dr Temple suggested, the tambalacoque had relied for dispersal upon the dodo, which was extinct by 1681, barely 200 years after European sailors first landed on Mauritius. For tambalacoques produce very big seeds – about 5 centimetres across – surrounded by an enormously hard and woody husk, up to 1.5 mm thick: too thick, apparently, to allow the young seedling to emerge unless the walls are first weakened. The tree, Dr Temple said, evolved such a stony seed to cope with the dodo.
The dodos ate the fruit of the
tambalacoque. They digested the pulpy exterior, and the big wooden pip passed to the gizzard – the extension of the gut which birds pack with stones and use to crush seeds. Tambalacoques evolved seed-coats that were thicker and thicker, in response to the dodo gizzard’s enormous crushing strength. Eventually they became so thick that the seeds could not germinate at all unless they had first been eaten by a dodo. Of course, the seeds would fail if they were crushed in its gizzard. But if the pips were merely abraded, or ‘scarified’, they would germinate much better than if not: indeed, they needed the scarification. Here, then, was another example of co-evolution. Dr Temple tested his theory by feeding tambalacoque seeds to turkeys, which are not related to dodos but are ecologically equivalent. Wild turkeys eat hickory nuts. The turkeys crushed some of the tambalacoque seeds – seven out of seventeen –but after six days or so they gave up on the other ten, and either coughed them up or passed them through their guts. Those ten seeds, duly abraded, did germinate.
As we have already seen, many other seeds benefit from some pre-treatment from animals in one way or another. In India, teak seeds are sometimes prepared for sowing by laying them out on the forest floor where the termites can get to them. They germinate better after the insects have nibbled some of the seed-walls away (though it’s important not to leave the seeds out too long). All in all, the tale of the dodo and the tambalacoque has all the elements of a classic.
Indeed the story has only one shortcoming. It does not seem to be true. Areas of forest in Mauritius have now been fenced, and cleared of the pigs, deer and monkeys that meddlesome Europeans have introduced to the island over the past three centuries – and lo, in the cleared areas, young tambalacoques have been springing forth. Evidently, it wasn’t the presence of dodos they required, but an absence of imported herbivores. This is excellent news for the tambalacoque. But it is pity indeed to kill off such an excellent story.