by Colin Tudge
Theory predicts that when only one foundress colonizes a particular fruit, the ratio of males should be low: one in twenty rather than one in two. But the more foundresses there are, the more we would expect the ratio of males to increase. The point is that each female strives to pass on as high a proportion of her own genes as possible. If all the larvae within any particular fruit are her own offspring, then all her daughters are bound to be mated by her own sons (if they are mated at all). The shortcomings of incest and inbreeding are apparently outweighed by the advantage that the mother thereby passes on her genes both via her sons and via her daughters. So she needs only enough sons to ensure that her daughters are all fertilized—and one son per twenty daughters seems enough. It is good, of course, to focus on daughters, because they are the ones that lay the eggs that supply the grandchildren generation.
But if there is more than one foundress per fruit, then the young males find themselves with rivals who are not simply their brothers (who would be genetically very similar) but come from a different lineage (albeit of the same species). In such circumstances, we might suppose that it could pay a female to produce sons exclusively—provided those sons are big and tough enough to mate all the daughters of all the other foundresses. The theory shows, however, that it never pays to produce more sons than daughters. A 50:50 ratio of sons and daughters is the maximum. Again, natural history supports the theory. Dr. Herre and his colleagues have shown that as the number of foundresses per fruit rises to about six, so the proportion of males rises to around 50 percent.
But here comes another twist. The males have one function only: to mate with the females. Apart from that, they are a dead loss—both from the wasp’s point of view and from the fig’s. After all, the fig has to sacrifice a seed for every young wasp that is born. The youngsters that matter to the fig are the females, which fly off to pollinate other figs. As far as the fig is concerned, the fewer males, the better. This, in turn, implies that figs should encourage wasps to enter their syconia one at a time: that they should evolve some limitation on access (and there are many comparable examples in nature). As things are, small syconia are much less likely to attract multiple foundresses than are large syconia—so we would expect natural selection to favor small syconia. In reality, while some fig species do have small syconia, others have larger ones. So why does natural selection ever favor big syconia? This question will be raised twice more as this narrative unfolds, in two quite different contexts. Whichever way you look at it, big syconia seem like bad news. Yet there is an answer, which will be provided later in this chapter. Patience, gentle reader.
As if the game between figs and wasps were not convoluted enough, there enters now a third set of players: parasitic nematode worms.
ENTER THE NEMATODES
It has been suggested that every species of creature on earth above a certain size has its own specialized nematode parasite; if this were so, it would mean that the total number of species on earth is equal to the number of non-nematodes times two. Whether this is so or not, it does seem that every species of pollinator wasp does have its very own species of nematode parasite. All the nematode parasites of Panamanian fig wasps belong to the same genus: Parasitodiplogaster. Since STRI, where Dr. Herre works, is based in Panama, this is the genus he and his colleagues have studied most.
The life cycle of Parasitodiplogaster nematodes is superimposed on that of the wasps they attack. Not all figs are infested with nematodes, but in those that are, the nematodes will have reached the immature, dispersal stage by the time the young female wasps are emerging from their flowers. The worms then enter the wasp’s body cavity and begin to consume it from within. Their efforts are not immediately fatal, however, and so their host carries them on to another syconium. When the infested wasp finally dies, generally after laying her eggs in the next syconium, up to twenty or even more adult nematodes crawl from her body, mate, and lay their eggs. The young nematodes hatch before the young wasps emerge—and so they are ready to invade the young wasps and begin the cycle afresh.
In general, the relationship between parasite and host is as delicate as that between partners in a mutualistic relationship. The aim of the parasite is to grow and reproduce, and for this it must feed upon its host. If it feeds too vigorously, it is liable to kill the host. If it is too decorous in its approach, it loses out to rival parasites who are more vigorous and so breed more quickly. In general, then, it pays parasites to be as vigorous—“virulent”—as possible, but without overdoing it.
Now a further twist. Theory predicts that if nematodes infest wasps that occupy fruits on their own—one wasp per syconium—they should be less virulent. After all, if they are too virulent, and kill their host wasps, they have no chance at all of being transmitted to a new fruit to lay eggs of their own. But if the nematodes attack wasps that invade fruits more than one at a time, they can afford to be more virulent. It doesn’t matter too much if some of the young host wasps are killed off, since there are liable to be others that are not killed, and will carry the nematodes to pastures new. The Smithsonian scientists found that this prediction stands up. Wasps that invade fruits singly generally manage to fly off to new fruits even when they are infested with nematodes. But in fruits that entertain more than one foundress, a proportion of infested foundresses perish before they leave the syconium of their birth.
Nematodes are clearly bad news for the wasps; and particularly virulent nematodes are bad for the figs, too. After all, the fig has to sacrifice one of its would-be seeds for every wasp that is produced, and the sacrifice is wasted if the wasp then dies from nematode attack. Again, it seems that figs would be better off producing syconia that attract only one foundress. Again, small-sized syconia seem advantageous—because, in general, the bigger the syconium, the more foundresses it is liable to attract. So the question is prompted again: why do some figs continue to produce large syconia?
There is more.
COOL FIGS AND HOT FIGS
Although figs surely have no love for gall wasps, they do go to great lengths to protect the vital pollinator wasps. In particular—as again revealed by the Smithsonian studies—they maintain a temperature within the syconia that allows the young wasps within to develop.
As a preliminary observation, the scientists showed that when the temperature is only 5° to 10°C (9° to 18°F) 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 the researchers measured the temperature inside syconia—and found that they stayed more or less near the ambient temperature: still comfortable for the young wasps developing within them. Even on the fiercest days, the temperature within small syconia never rose above 32°C (90°F), 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. 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 (14°F). When the outside temperature was at 29°C (84°F, 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 c
ool—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 favored 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 consume at least as many acorns as they scatter. When trees produce fleshy fruits, animals may simply eat the pulp and then either spit out the seeds (as monkeys may often be seen to do with machine-gun efficiency) or else allow the seeds 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, and 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 color 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 2.5 acres 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; there are twenty or more fruits per square meter 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 less than two and a half ounces). 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. However, 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 types of 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 animals: 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 midsized spotted cats of tropical America. But the almendro also contrives to satiate the agoutis—to produce more seeds 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 wipeout for the particular year.
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 animals: 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 as of 2004 there were some saplings, since such ocelots as there were had 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 on 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 trees 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? When the students finally run out of steam he reveals the answer: “Ants!”
How can it be? It is easy to see how ants might help plant a tree. They could carry the seeds to their nests if the seeds are small enough. Those of Chukrasia are only a couple of millimeters 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 Balaklava.
On the sites where the trees now stand, there once were small beds of the white-flowered Tabernaemontana 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—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.