The Deadly Tomato

 

As I walked through the weeds between the early-successional trees in the field about which I earlier wrote, I noticed a Solanum dimidiatum weed (horsenettle). It was in the same genus as the potato, a close relative of the tomato. And it had what looked like little green tomatoes on it. This is the time of year when tomatoes are really good. But if you think these tomatoes might be delicious, think again. The entire plant is filled with toxins that are dangerous, even deadly, to most animals.

 

[Photo from Carolina Biological Supply Company] 

The horsenettle plant expends a lot of its energy creating these toxic compounds [what are they]. Expensive they may be, but they protect the plant from having its leaves eaten by most animals. But there is at least one group of animals that can eat the leaves as if they are not toxic at all. The sphinx moth (Sphingidae) caterpillars (hornworms) of the genus Manduca can eat them with little effect on their growth. I know this because I have measured the growth of hornworms when they ate ground-up horsenettle leaves and when they did not; their growth was the same. The toxins do not protect the horsenettles from hornworms, but in many cases, there are no hornworms about. The plant is taking a chance. It invests in imperfect, but usually good, protection.

You may wonder how to compare hornworms that eat horsenettle tissue and those that do not. To what do you compare the ones that do? This is an interesting story. You can purchase little hornworms, special vials to grow them in, and hornworm chow. They do not naturally eat this chow, but if you start them on it when very young, they will eat it and grow grossly big. It is sort of hornworm junk food. The control worms are the ones that eat only the chow; the experimental worms have horsenettle tissue mixed in with the chow.

Herbivores, and the defenses of plants against them, are a constantly moving evolutionary target. They hardly ever get it right, but they come close enough that there are lots of plants, and lots of herbivores, in the world. Any plant that invested too much in defense would grow slowly and die; but if it invested too little, it would disappear down the gullets of extinction. There is a balance of nature, but it is imperfect and shifting.

New Video: Darwin Eats Tree Leaves

In this video, Darwin jumps around in springtime exuberance and eats leaves of a water oak (Quercus nigra). He was inspired to do this by seeing a French video in which a naturalist ran around in the French woodlands and ate young leaves. He smiled really big and talked about how good they were, including oaks, willows, poplars, beeches, etc.

But the French videographer warned his viewers that they should do this only with very young leaves. Older leaves in European forests are full of toxic compounds which, although they will not kill you, at least taste bad. The leaves manufacture these compounds (for example tannins) to discourage animals, especially caterpillars, from eating them.

But it can be expensive for a leaf to defend itself. Every molecule of defensive chemical that the leaf makes has a construction cost in energy and raw materials. These costs could be used to make more leaf area, which is an investment in photosynthesis that will bring in more energy and raw materials. The ideal amount of defense spending for a leaf (or a nation) is zero, but this is not possible in a dangerous world. Therefore, leaves, like nations, economize their defense spending. Leaves make defensive chemicals only when they are needed.

Ever since the work of Paul Feeney fifty years ago, scientists have understood that, in European forests, many herbivorous insects die during the cold winters. Their populations build back up during the warm, wet summers. The forest trees, such as the oaks studied by Feeney, economize their defense spending by producing very few defensive compounds in the spring, then more and more as the summer goes on. In the early spring, therefore, the forest is almost like a big salad bowl, especially for the Frenchman I mentioned earlier. In the video, Darwin decides to eat a young water oak leaf in Oklahoma.

Darwin got a surprise. The leaf was bitter. Then he understood why. In Oklahoma, the winters are not very cold (February 2021 being a significant exception) and many insects can find little crevices to hide in. In Oklahoma in the spring, unlike in Europe, the insects can come out in full force. The young leaves are ready for them, having defended themselves with chemicals. Many of the insects die during the long, hot, dry summers in Oklahoma; that is, their populations die back in the summer, not so much in the winter.

This raises the possibility that tannin concentrations in Oklahoma oaks are high in the spring and lower in the summer. Of course, once the leaf produces tannins, why not just keep them all summer? But it is possible that the tannins can be degraded and the molecules used for something else. I tried to measure this in post oaks (Q. stellata), only to discover that I am not a very good chemist and failed to measure the tannin levels correctly.

I did try a different, creative approach to determining whether the early season oak leaves were more toxic than the late season leaves. I ground up leaves in liquid nitrogen and mixed them up into hornworm chow. You read that correctly. Hornworm chow. It turns out you can buy hornworm eggsand caterpillars, and even chow and growth vials, from Carolina Biological Supply. Wild hornworms usually eat tomato leaves, but these caterpillars eat chow, and, apparently, almost anything you mix into it, like leaf powder. The hornworms grew best on the chow. But they grew bigger and faster when they ate late-season oak leaf powder than early-season powder.

So my advice to Darwin is, if you want to eat tree leaves in the spring, go to Europe.

Tentworms in the Forest

Today, I took a walk in a forest near Tulsa. Spring came late this year for most of the United States. The buds of most of the woody plants have begun to open, but very few leaves have expanded. One kind of tree, the black cherry (Prunus serotina), has opened its leaves. And as soon as the leaves opened, they were eaten by tentworm caterpillars (Malacosoma americanum).

Mindlessly and cruelly efficient, that’s what it was. Dozens of hungry tentworm caterpillars hid inside of silk tents that they wove where branches diverged in wild cherry trees. While it looked soft, the silk was actually very tough. Though a bird would easily see the caterpillars through the translucent fabric, it would take a lot of messy work for the bird to tear through the fabric and eat them. At night, when the birds cannot see them, they slip out of their tents and eat the young leaves. It seemed like a perfect arrangement for the benefit of the caterpillars. Tents festooned cherry trees throughout the forest.

This was not merely an interesting observation. It was observations like this that spawned a whole branch of ecological research. Why is the world green? Given the astonishing ability of insects to multiply their numbers, why have they not eaten every leaf and sprig of grass on the planet? Outbreaks such as locust plagues prove that they could do so, given the opportunity. What stops them? The answer is, lots of things. The interaction between plants and the animals that eat them (collectively called herbivores) is dynamic and constantly shifting.

Despite what seemed like an easy feast, there were lots of chances for things that could go wrong for the caterpillars. Like most plants, the cherry tree produces toxins in its leaves that inhibit the growth of herbivores. The cherry leaves, like the leaves of all the other plants in the deciduous forest, are not a big salad bowl. Toxin production, however, is metabolically expensive. To make the toxins, the leaves must use energy and molecules that they would otherwise use for growth and food production. That is, if the leaves defend themselves more, they grow less.

Young leaves are often tender and have relatively few toxins. This appears to be the case with wild black cherry. If the tentworms are going to eat them, it is best to do so early in the spring. If the eggs hatch too late in the spring, the leaves may be tougher and more toxic. That is, the caterpillars must get their timing right. I looked around me and saw that the leaves of most of the trees were just emerging. Black cherry was one of the earliest trees to open its leaves.

But, aside from encountering leaves that may be harder to eat, what problems might the caterpillars encounter if they emerge too late? Black cherry trees produce nectar in their flowers (which open later in the spring), but also from “extrafloral nectaries,” structures on their reddish bark that produce nectar. Nectar inside a flower attracts pollinators, but what benefit might the cherry tree get from producing nectar on its bark? In numerous other species, extrafloral nectaries attract and feed ants. When the ants visit the cherry tree, they do not just eat nectar. If they encounter big packages of protein, such as tentworms, they will swarm over them and eat them. As the spring progresses, ants become more common and they search a larger and larger area. Late tentworms might find themselves under attack. They need to hide and pupate soon if they are to have a chance.

But the caterpillars must also not hatch too early. In a previous year in this same forest, I found dozens of tents filled with caterpillars, and no leaves for them to eat. The particular pattern of weather conditions that year had tricked the caterpillars into hatching too early. That year, many or most of the caterpillars probably starved. This event interrupted what might otherwise have been a year-by-year population explosion of tentworms.

Herbivores often specialize on certain species of plants whose toxins they have evolved to tolerate. Some herbivores, such as gypsy moths, seem able to eat almost any kind of tree leaf. But even they have their limits. They do not eat grasses, for example. These tentworms, however, seemed to eat only black cherry leaves. Perhaps this was because they were the leaves that were available at the right time. I decided to look more closely to decide if this might be the case.

The black cherry trees were almost, but not the only, early leaves. The invasive Bradford pear (Pyrus calleryana) is the tree that wakes up earliest in the springtime. Before the buds of any other woody plant open, the Bradford pear is in full white bloom. By the time the tent caterpillars swarmed over the wild cherry trees, the Bradford pear leaves were already out. Why were there no caterpillars eating their leaves? Perhaps the pear leaves had toxins that the tent caterpillars could not tolerate. This seemed unlikely, because the pears and the cherries are closely related species in the rose family. The same is true of the serviceberry leaves (Amelanchier canadensis). But I had nothing to go on. All I knew was that the wild cherries had caterpillars and the serviceberries and the invasive pears did not.

Or did they? One of the habits of a successful scientist, whether professional or amateur, is to keep looking closely, to not be satisfied with a quick glance. After seeing dozens of caterpillar tents on black cherry trees, I finally found one on a Bradford pear. The tent was small, and the caterpillars were short and skinny compared to those on the cherry trees. They had not eaten very much, and this meager diet would almost certainly cause them to starve before reaching adequate size for pupation. I also found one tent, similarly small and with scrawny caterpillars, on a red oak tree (Quercus rubra).

Tent caterpillars have been widely reported to prefer cherry trees, and this is certainly what I see every spring in this particular forest. But they have also been found on other kinds of trees; my observation of tentworms on a red oak was therefore unusual but not something to write home about. It is difficult, without extensive research, to know why the tentworms prefer cherry trees. Perhaps it is because the caterpillars often eat cherry leaves, and when the adults emerge to mate, they look for cherry trees as places to lay their eggs. This cycle of preference from one generation to another might maintain the association between tentworms and cherries. This, however, is not a very convincing explanation. As I saw on just a single day of exploration, the tentworms occasionally hatch on and try to eat other kinds of trees. It would not take long for the tentworms to spread to other tree species, if the leaves were just as suitable a food for them as are cherry leaves.

Still, if the tentworms begin their feast on the right kind of tree, not too early, and not too late, they would seem to have it pretty good. But the natural world is full of perils. Dozens of species of other insects attack or parasitize the eggs, caterpillars, or pupae. Though I cannot find a published confirmation of this, I suspect that some of the parasites may affect the nervous system of the caterpillars in such a way as to alter their behavior. There are parasitic worms that cause strange behavior in, for example, snails. In particular, the worm makes the snail climb out on a twig tip where a bird can eat it. I have seen a few tentworms, in the daytime, on the outside of their tents, where birds could easily find and eat them. Was it because parasitic worms influenced their behavior? Perhaps so. The caterpillars would occasionally twitch!

Finally, the effects of the tentworms on the cherry trees may not be as great as it would at first appear. I have seen hundreds of cherry trees infested and completely denuded by these caterpillars, but I have not seen any of them die. Since I did not mark the trees, I cannot be certain; but there are certainly not very many tentworm victims. Since the tentworms must finish their work as quickly as possible, well before the end of springtime, the cherry trees simply grow a new set of leaves once the caterpillars have pupated.

No matter what the cherry tree does, there is a cost. It could produce costly toxins early in the spring, thus defending itself from tentworms; or it could allow the leaves to be eaten, and grow them back. For reasons that at least I do not know, evolution has selected the latter option for the black cherry.

All this, from just looking closely at and thinking about something I saw while walking through the forest.