## Info

Figure 8.13 The difference in oxygen partial pressure in water and in a poorly designed and a well-designed plastron bubble. [After Crisp and Thorpe (1948)]

---thin plastron

■ thick plastron possible over the entire outer surface of the bubble. This ensures that oxygen flows into the bubble over its entire surface. The flat distribution of ApO2 simply expresses this steady level of difference graphically.

Now let us modify the bubble in a way that would seem to make sense according to Fick's law: make the bubble thinner (reduce x). If oxygen moved through the bubble in only one dimension (from the surface of the bubble to the beetle's skin), thinning it should enhance the flow of oxygen, making it a better gill. A thinner bubble actually makes for a poorer plastron gill, however. To see why, look at the distribution of ApO2 in a plastron bubble one-tenth as thick as the normal Aphelocheirus plastron (Fig. 8.13, dashed curve). While the ApO2 is quite steep near the spiracle, it is much shallower at the bubble's margins. This occurs because thinning the bubble impedes the flow of oxygen in the second dimension, that is from the margins of the bubble to the spiracle (Fig. 8.12). As a result, oxygen flowing into the bubble accumulates at its margins, and this reduces the ApO2 that can develop there. Consequently, little oxygen enters the bubble along its margins because the concentration gradients that could drive a flux there are small. Put simply, the bubble's margins are "useless machinery," like the fins on those 1950s cars. Take it away, and the performance changes little.

These design principles are in fact encapsulated into a neat formula:

ApO2 oc ^JiO^s2/Dh where h is the thickness of the bubble, iO2 is oxygen's invasion coefficient, s is the distance to the spiracle, and D is oxygen's diffusion coefficient in air. "Good design" is evidenced by making the thickness of the bubble large compared to the distance from the spiracle. Practically, the ratio on the right side of this equation should be less than 1, although the smaller it is, the better the plastron gill will perform.

Let us now return to the problem of the Agriotypus ribbon. This structure, which seemed such a poor candidate for a plastron gill when considered in terms of a simple one-dimensional flow, actually becomes the epitome of good design when it is analyzed with due appreciation for its complexity. Although the ribbon is long (5 cm), it is also fairly wide (2-3 mm), which means that diffusion of oxygen along it is not significantly impeded. Indeed, a calculation of the change of ApO2 along the length of the ribbon shows it drops by only about 1 pascal from the tip to the cocoon. Thus, the entire ribbon can draw oxygen from the water with equal facility along its entire length.

If this is such a good design, why then is it not applied more often? In fact it may be used more often than we might think. For example, many insect eggs sport long projections from their egg cases. Often, these are used to attach the egg to some surface, but not always—in some eggs, the stalks are air-filled and project directly to the spiracles of the developing larva. In one of the more interesting cases, eggs of a blood parasite use a stalk to extract oxygen directly from a host's blood, essentially co-opting the respiratory machinery of its host to support its own gas exchange.

"Anti-Gills" in the Bubble Nests of Spittlebugs Finally, we turn to an interesting example of a bubble gill that lets an aquatic insect live in the air: the bubble nests of spittlebugs. Spittlebugs are the nymphal stages of a group of insects, the Cercopidae, that are included among the insect family Homoptera. Among the more familiar Homoptera are the leafhoppers, aphids, and cicadas. Spittlebugs are especially common on mead-owland crops like grass and lucerne (alfalfa), and most people who have spent any time walking around such habitats in the spring will have seen their nests: wads of white, bubbly "spittle" attached to stalks or stems (Fig. 8.14).

The spittle itself has some interesting folklore attached to it. Probably the strangest idea is the oldest, proposed by Isidorus in the sixth century, who believed the spittle to be the spit of cuckoos. Indeed, a common name for spittle nests in Europe is some variant of "cuckoo-spit." Among the slaves held in North America, spittle nests were thought to be constructed

Figure 8.14 Photograph of a spittle nest.

by horseflies, perhaps reflecting some African folklore concerning their origins (and a story closer to the truth than the legends of their European masters). The great eighteenth-century naturalist John Ray got it right, though, by identifying the spittlebug as the source of the spittle. Surprisingly, how the bug produces the spittle, or even which end of the bug it comes from, the mouth or the anus, was not really settled until the early twentieth century (it's the anus, by the way).

Many homopterans are parasites of plants' vascular tissues that live by tapping into a stem or leaf and sucking out the fluid within. Among the vascular plants, there are two types of vascular tissue, phloem and xy-lem, each of which transport different types of fluid in the plant. Phloem usually carries in it a dilute mixture of water and sugars produced by photosynthe-sis—when maple sap flows at the end of winter, it is being transported by phloem from the roots, where it was stored the previous summer, to the branches, where it can fuel growth of a new leaf crop. Xylem, on the other hand, carries in it a very dilute solution of salts and amino acids and virtually no sugar. The homopteran parasites of plant vascular tissue likewise fall into two broad categories. On the one hand, the "smart" phloem feeders, mostly aphids, tap into a nice rich sap of sugars and amino acids. On the other hand, the "stupid" xylem feeders tap into the nutritionally impoverished sap in the xylem. Spittlebugs are "stupid" xylem parasites.

The spittle nest is produced from xylem sap mixed with secretions from glands in the bug's anus and from intestinal glands commonly found in insects, the Malpighian tubules. The spittle starts as a liquid drop extruded from the anus, which is taken up by the hind legs and folded so that it incorporates a bubble of air. The bubble is then passed forward into a tubular fold of the body wall along the bottom of the insect, called the ventral tube. The insect's spiracles open up into the ventral tube. The insect continually secretes raw spittle, and the repeated formation of bubbles from raw spittle forms the froth, which is eventually forced out the front end of the ventral tube. The overflow covers the outside of the insect and the stem it sits on, forming the spittle nest.

The spittle nest, despite looking like an ordinary wad of foam, is actually a woven structure, like the bubble webs of Argyroneta. The fluid of the raw spittle, which ends up as the bubble walls, includes lots of fibrous proteins, including short fibers of silk. Because the bubbles are impregnated with these silk fibers, they are very long-lived—the bubbles in a spittle nest will last for weeks, as long as the nest is not allowed to dry out. The large quantity of liquid produced—as much as thirty times the weight of the bug per hour—and its rich protein content makes the spittle nest a very energetically expensive structure. Some estimates place the energy investment in spittle production as high as 90 percent of the nymph's total energy budget. So, it is reasonable to suppose that the nest does something important for the animal. But what?

As many theories for the spittle nest's function have been proposed as there have been for its origin. Some of the more easily dismissed theories: it is a trap for insects (but spittlebugs eat only plant sap), it is an antimicrobial or anti-fungal shield (it actually is a quite good culture medium), it is a deterrent against preda tors (I can say from personal experience it doesn't taste bad). Current conventional wisdom, though, is that the spittle nest helps keep the insect from drying out. There is some justice to this claim: spittlebug nymphs do have thin skins, and they dry out quickly and die if they are removed from their spittle nests. Because spittlebugs probably were aquatic insects that secondarily returned to the air, it seems reasonable that the spittle nest might provide the bug an aquatic microenvironment, the same way amniotic fluid supposedly provides a "uterine pond" for a mammalian fetus.

Watch out for Occam's razor, though: the role of the spittle nest is actually not so simple. First, we have to ask: is there any possibility that spittlebugs will ever face a water deficit? The answer is probably not, since they feed from an extremely rich source of water, the xylem sap. How could they ever dry out while sitting in the middle of a veritable spittlebug Niagara? Indeed, the enormous production rate of spittle—thirty times the nymph's body weight per hour—is only possible because of the abundant supply of water provided through the xylem tissues of the plant host. So we are forced to ask another question: why should the spittlebug spend such enormous amounts of energy to construct a spittle nest to protect it against water loss when it has such an abundant supply of water to begin with?

The story gets even stranger. Spittle, being wet, obviously loses water by evaporation. The rate of evaporation is about 30 percent less per square centimeter of surface than it is from a plain water surface, a phenomenon that, again, fits into the supposed role of the spittle as protection against desiccation. Probably, the fibrous web of the bubble walls helps retard evaporation, in the same way a thin layer of oil on a pond reduces evaporation from it. But then you have to ask still another question: why should the nymph go to the trouble of blowing up its anal secretion with bubbles? If reducing water loss was the object, it would make more sense to just let the anal secretion ooze over the insect as a smooth sheet. By blowing the liquid up with bubbles, the insect increases the surface area from which water can evaporate. Indeed, spittle nests lose water at a total rate roughly 10 percent faster than the bug would if it simply let water, without all the added costly proteins, ooze over the smaller surface area of its body. So the spittle nest does not provide much protection against water loss, even supposing such protection is needed.

So, what is going on? It may be that the spittle nest is part of a plastron gill that has been carried up into air when spittlebugs made the transition from water back to land. For example, the ventral tube of spittle bugs is coated with a waxy cuticle that elaborates into a very finely reticulated network, similar in appearance and function to the plastron hairs of other aquatic insects. It seems a bit strange, though, that a plastron gill would be retained in the rich oxygen reservoir of the air. A plastron makes more sense, though, if it is intended to exchange some gas other than oxygen. Probably, that other gas is ammonia.

When any animal uses protein for energy, one of the inevitable by-products is ammonia. Ammonia is highly toxic, and animals that produce it must keep it at fairly low concentrations in the fluids of the body. For an animal that lives in fresh water, this is no problem. Ammonia diffuses across the body wall or gills and is diluted in the water of the environment. Indeed, as we saw in Chapter 7, the large flow of water through the bodies of freshwater animals helps keep ammonia concentrations low. In marine or terrestrial environments, however, animals face an ever-present danger that ammonia will build to unpleasantly high concentrations (Box 7A). This is an especially serious problem for terrestrial animals: unless the ammonia can be converted to something less toxic, like urea, it can only leave the body by volatilization—moving from solution into the gaseous phase.8 Ammonia is

8. You will remember from Box 7A that many terrestrial animals use alternative nitrogen-containing compounds, like urea or uric acid, to remove ammonia wastes from the body. Spittlebugs seem not to use this strategy—neither urea nor uric acid is detectable in spittle nests. The implication is that these animals lose ammonia as ammonia gas.

not easily volatilized, however, because of the way it reacts with water to form the weak base ammonium hydroxide:

NH3(g) « NH3(s) + H2O « NH4OH « NH4+ + OHGetting ammonia to evolve away from a solution as a gas involves somehow biasing the reaction to the left.

Spittlebugs face an unusually serious challenge in this regard. Their diet of xylem sap is virtually all amino acid. Thus, virtually everything they consume for energy produces ammonia as a waste product. Furthermore, spittlebugs, as far as is known, are not able to detoxify the ammonia to urea or uric acid, as other terrestrial animals commonly do. Consequently, one of their major physiological challenges is how to handle the high ammonia load that is, for them, an unavoidable cost of living.

It just may be that the spittle nest is the solution. Ammonia loss is facilitated by providing a large surface area for it to volatilize from. Blowing up the spittle nest may be the spittlebug's way of increasing the volatilization rate of ammonia, in just the same way that blowing up the nest increases its rates of evaporative water loss. Furthermore, by filling the liquid portion of the spittle with bubbles of air, it increases the diffusion rate of ammonia away from the bug, for the same reason that diffusion is so effective in the air-filled tracheoles of insects. Indeed, ammonia moves through a layer of bubbles about twice as fast as it does through a parcel of water with no bubbles. So it just may be that the spittle nest of spittlebugs serves as an accessory gas exchange organ—one that promotes the exchange of ammonia rather than oxygen.

. . . And on the pedestal these words appear: "My name is Ozymandias, king of kings: Look upon my works, ye Mighty, and despair!" Nothing beside remains. Round the decay Of the colossal wreck, boundless and bare The lone and level sands stretch faraway.

—PERCY BYSSHE SHELLEY, ozymandias chapter nine

### Manipulative Midges and Mites

The image captured in this epigraph—the arrogance of kings mockingly ground to rubble and dust—reflected the poet's radical (for the time) antipathy to monarchy and monarchs. Still, you have to give Ozymandias (known to us as Ramses II) some credit. It was, after all, his image and his words that sat there disintegrating in the sands, not those of some other fellow who lived four thousand years ago. Something about Ozymandias made him capable of leaving behind such a formidable monument.

What made Pharaoh's legacy an enduring one had nothing to do with his own physical prowess: it wasn't Ozymandias who carved out all those stones and hoisted them into place. Rather, the monuments were built because he had a talent for getting others to build them for him. Whether this talent derived from terror, persuasion, or inspiration, we really cannot say, but the magnitude of his legacy is undeniable.

The ability to appropriate the energy of others to build structures for you is not limited to human societies. In fact, many aphids, mites, flies, and wasps engage in this type of construction by proxy. These insects hijack the physiology of organisms much larger than they and force them to build structures that feed, shelter, and protect them. These structures are known collectively as plant galls, and it is to them that we shall turn in this chapter.

My thesis is that a particular type of gall, specifically leaf galls, are structures that a parasite tricks a tree into building for it. The gall is built for the "purpose" of altering the heat budgets of leaves afflicted by them. A parasite that instigates the construction of a gall in ef-

fect activates an adaptation normally employed by a leaf to cope with abnormal temperatures for its own benefit. To develop this idea, I shall first describe in general what galls are, with special attention to what leaf galls are and how they develop. I shall then explain how leaf temperature normally affects the energy budgets of leaves and how leaves use shape to control or otherwise manipulate their own temperatures. At that point, we will be ready to explore the consequences of galls for leaves' heat budgets and temperatures, and how these galls might affect the exchange of energy between leaves and their parasites.

### Growth and Development of Galls

Galls are a developmental anomaly found in a wide variety of plants and in nearly every type of plant tissue, including stems, leaf blades, leaf veins, and the vascular and woody tissues of trunks, roots, and buds. They are usually induced by an arthropod parasite, although fungal, bacterial, and viral infections also can induce them. Frequently, the gall grows so that the parasite is enclosed in it. In some cases, the gall houses only one stage in the parasite's life cycle, like the larva, but in others, such as in some galls induced by aphids, the gall is the animal's permanent home—it may even house entire societies or communities of aphids. Some galls have economic benefits for humans—in medieval times, certain galls of oaks, for example, were an important source of ink pigments. More often, galls are deleterious to the health of the plant, as evidenced by the common designation of galls as "plant cancers." Indeed, many trunk and stem galls of trees do show the type of uncontrolled growth that is typical of cancerous tumors in animals (Fig. 9.1). Plants afflicted with these tumors face problems similar to those suffered by animals with cancer: a diversion of energy toward the growing mass that saps energy away from the host, weakening it and eventually killing it.

Some galls, however, particularly those that affect leaves or buds, are highly organized structures, and characterizing them as "plant cancer" seems decidedly b

Figure 9.1 Two examples of "plant cancers," stem galls of oaks. a:The noxious oak gall, Neuroterus noxiosus. b:The gouty oak gall, Andricus punctatus. [From Felt (1940)]

inapt—I have selected a sampler of examples for Figure 9.2. Consider just one of these remarkable galls, the spruce cone gall. Cone galls arise at the leaf buds and bases of leaves of spruce (Picea spp.) and their relatives, hemlock (Tsuga spp.), and fir (Abies spp.). They are induced by a small fly, about a millimeter long, known as a gall midge, which lays its eggs at the bases of buds or leaves. Once the larvae hatch, the bud begins to grow abnormally into an anomalous woody structure with a shape very reminiscent of a spruce cone (Fig. 9.2a). The remarkable thing about these galls, of course, is their highly organized and most uncancer-like growth and development. It is as if the midge, in depositing its offspring at the base of the leaf bud, is commanding the tree (like Pharaoh to his slaves), "build a cone here!"

On the face of it, this is an extraordinary achievement. The formation of complex structures like spruce cones would seem to require a complex developmental program that controls rates and timing of growth and differentiation, as similar programs do in animals (Chapter 5). How does a gall midge make the tree build such a structure? Two possibilities come to mind. First, the midge may stimulate the plant's cells to begin simply activates software already written by the company and normally used by it to cut its checks.

### Plant Homeosis and Galls of Buds and Leaves

Cone galls, or other galls that likewise mimic normal plant structures, probably are induced by parasites acting as genetic hackers. This is surprisingly simple to do. Take, for example, galls that mimic structures derived from leaf buds. The leaf bud is a sort of foundation structure for a variety of specialized structures. Leaf buds can develop into (of course) leaves, but they also develop into flowers, or thorns, or hairs. A leaf bud's developmental fate can be mapped out as a series of contingent pathways. The early stages of development are the same whether the structure is destined to become a leaf or a flower. At some point, though, the developmental pathways for the different structures will diverge. Follow one pathway, and the bud develops into a leaf. Switch pathways at some point, and a flower might be the result.

The points of divergence in developmental programs, both in animals and plants, are controlled by so-called homeotic genes, which act essentially as genetic switch points. For example, one homeotic gene might initiate the developmental pathway for a leaf-derived structure like a thorn. Keep the gene switched off, and development will proceed toward leaves or flowers. Switch the gene on, and development will proceed toward a thorn. Another homeotic gene, later in the sequence, might control the point of divergence for leaves versus flowers. Keep the gene switched off, and development proceeds toward a leaf. Switch it on, and development proceeds toward a flower.

In normal development, homeotic genes are useful because they provide simple ways of controlling complex patterns of development. You don't need to regulate an entire complex program, all you need to do is regulate the switch that activates it. Having these developmental switches, however, makes the plant vulnerable to attack by organisms that have learned how

Figure 9.2 More highly organized galls develop in leaves and buds. a: The spruce cone gall, Adelges abietis. b:The cypress flower gall, Itonida anthici, showing a cluster of flower galls and one flower gall enlarged. c:The spiny witch-hazel gall, Hamamelistes spinosus. d: The pine bud gall, Contarinia coloradoensis, showing a cluster and a single gall enlarged. [From Felt (1940)]

Figure 9.2 More highly organized galls develop in leaves and buds. a: The spruce cone gall, Adelges abietis. b:The cypress flower gall, Itonida anthici, showing a cluster of flower galls and one flower gall enlarged. c:The spiny witch-hazel gall, Hamamelistes spinosus. d: The pine bud gall, Contarinia coloradoensis, showing a cluster and a single gall enlarged. [From Felt (1940)]

to grow and, as they grow, direct the cells' rates of growth and differentiation. If the midge can force the developing plant tissue to mimic the patterns and rates of growth that characterize the development of a normal cone, the gall will resemble a cone. On the other hand, the midge could hijack the developmental program already used by the plant to produce a cone;that is, it may activate the plant's own developmental programs inappropriately, the way a hacker might break into a company's computer system and make it write checks. In this case, the hacker does not write the code to make the victim's printer cut the checks—he or she upper epidermis palisade layer spongy mesophyll

- lower epidermis

Figure 9.3 Cross-section through the lamina of a leaf, indicating the four principal layers of cells. [From Bridgewater (1950)]

to switch the genes on themselves. This is probably what gall midges do: they initiate anomalous production of cones by switching on the homeotic gene that controls cone development. Once activated, the program runs whether doing so suits the needs of the plant or not, and a cone gall results.

Growth and Differentiation in Normal and Galled Leaves Gall inducers can also work the hard way—by intervening in and controlling the growth and differentiation of cells, rather than the homeotic switch points. These types of galls are common in growing or already mature leaves. Leaf galls commonly form relatively late in development, after the leaf bud is already developmentally committed to the formation of a leaf, rather than another structure like a flower. By controlling the leaf's normal patterns of growth, the gall-inducer can significantly alter the leaf's shape as it develops. To see how, you must first understand something about how leaves normally develop.

A mature leaf consists principally of two parts: the leaf ribs and associated vascular tissue, and the leaf lamina, the flat sheet of photosynthetic tissue that fills in between the vascular tissue. In a typical leaf, the lamina itself consists of four layers of cells (Fig. 9.3).

The upper epidermis and lower epidermis, located on the upper and lower surfaces of the leaf, are composed of cells that are typically flattened and tough. Below the upper epidermis is a layer of columnar palisade cells that together form the sheet-like palisade layer. Sandwiched between the palisade layer and lower epidermis are the loosely organized spongy cells, which form the spongy mesophyll. The cells in the spongy mesophyll are rather loosely packed so that oxygen and carbon dioxide can percolate through the layer.

A leaf begins as a small protuberance from the stem known as a foliar buttress (Fig. 9.4). Within the foliar buttress, two types of primordial tissues are evident. Running along the midrib of the buttress are the cells of the primordial vascular tissue, which will become the midribs and vascular tissues of the leaf. Flanking this are two bodies of marginal or lateral meristem, which will grow and differentiate into the leaf lamina.

The shape of a leaf is determined by the basic patterns of growth of these primordial tissues. The primordial vascular tissue grows by elongation along the long axis of the foliar buttress, while the lateral meristem grows outward from the stem. If unmodified, the result of these combined patterns of growth would be an elongate leaf, similar in shape to a tobacco

Figure 9.4 Cell types in the foliar buttress.

Figure 9.3 Cross-section through the lamina of a leaf, indicating the four principal layers of cells. [From Bridgewater (1950)]

leaf, consisting of a single midrib flanked by the leaf lamina.

Leaf shape can be modified in various ways by modifying these basic patterns of growth. One common modification is the branching of the primordial vascular tissue. For example, if the primordial vascular tissue elongates for a time, sends branches off to each side, and then continues to elongate, the leaf will take on the shape, say, of a maple leaf. Leaf shape can also be altered by modifying the growth of the lateral meristem relative to the vascular tissue. If vascular tissue and lateral meristem grow equally rapidly, for example, the leaf will have a simple outline—that is, its margin will not be cut with lobes, teeth, or other complicating shapes (Fig. 9.5a). But if vascular tissue grows relatively faster than the lamina, the leaf might have a lobed or toothed appearance, like a maple or oak leaf (Fig. 9.5b). If the initiation of growth of the lateral meristem is delayed with respect to the vascular tissue, the leaf might even develop as a compound leaf, with numerous leaflets arrayed along "stems" of vascular tissue, as is the case in leaves of ash or locust (Fig. 9.5c).

The internal structure of a leaf also depends upon characteristic patterns of growth and differentiation in the marginal meristem. Early on, the marginal meristem differentiates into two cell types. The marginal initial cells are arrayed along the top and bottom surfaces of the marginal meristem: these cells will eventually form the upper and lower epidermis of the leaf. The submarginal initial cells, sandwiched between the two layers of marginal initial cells, will form the palisade and spongy mesophyll layers. Normally, the marginal initial cells will go through several cycles of cell division and then cease dividing and continue to grow by lateral elongation. This pattern of growth both flattens the cells and extends the space between the two epidermal layers. This space is filled as the palisade cells and spongy mesophyll continue to divide and grow (Fig. 9.6, third line from top). Commonly, the spongy mesophyll cells cease dividing first, and the continued lateral elongation of the leaf causes these

opmental rates of the primordial vascular tissue and the marginal meristem. a: The development of the simple leaf. b: The development of a lobed leaf. c: The development of a compound leaf.

cells to separate from one another, opening up the air spaces of the spongy mesophyll (Fig. 9.6, bottom). The palisade cells continue to divide as long as the epidermal cells continue to elongate, and they consequently pack themselves into the compact palisade layer.

Many leaf galls arise through modifying these basic patterns of growth. For example, leaf-rolling is a common gall disease (Fig. 9.7a). As the name implies, the leaf grows into a curled-up cylinder rather than a flat blade as it normally does. Leaf rolling is a direct result of the parasite forcing a mismatch in the growth rates of the upper and lower epidermes. If the upper epidermis grows more slowly than normally, for example, the leaf lamina will roll upward. The mismatch in growth rates comes about in a number of ways, all of which disrupt the temporal synchronization of the growth of the marginal initial cells.

Leaf crinkling is another common example, but this time the mismatch is between the growth rates of the primordial vascular tissue and the marginal meristem (Fig. 9.7b). If the primordial vascular tissue prematurely stops growing, or if the leaf lamina continues to grow past the time it would normally stop, the lamina will buckle and crinkle along its surface. Both leaf rolling and leaf crinkling can come early in a leaf's development, in which case the entire leaf will roll or crinkle. In some gall diseases, the abnormal growth sets in later in leaf development, in which case the malformation is limited to the leaf's margin or focal points on the leaf blade.

Galls can also arise in mature leaves, as a result of the insect forcing a dedifferentiation of the leaf tissue; in effect, the insect causes a portion of the leaf's cells to revert to their primordial and undifferentiated states. Dedifferentiated cells are more prone to grow, and as upper epidermis ^ i__

palisade cell Q ' "N mesophyll cell Q J lower epidermis H

epidermal cells ^^^ ^^^ cease proliferating all other layers □□□□□□□□

proliferate palisade cells epidermal cells elongate proiiferate □□□□□□□□□□□□□□□□□□□□□□□□□□ mesophyll cells □□□□□□□□

cease proliferating epidermal cells elongate

Figure 9.7 Crinkling and curling of leaves induced by developmental anomalies. a: Leaf curling. b: Leaf crinkling. The dotted line indicates the level of the cross-sectional view shown above each top-down view of the leaf.

Figure 9.6 Sequence of development in the growth of the leaf lamina.

Figure 9.7 Crinkling and curling of leaves induced by developmental anomalies. a: Leaf curling. b: Leaf crinkling. The dotted line indicates the level of the cross-sectional view shown above each top-down view of the leaf.

they grow the gall-inducer directs their subsequent development. A simple example of this type of gall is the so-called bladder gall commonly found on the leaves of hackberry (Celtis spp.), induced by a gall midge (Fig. 9.8). The formation of a bladder gall begins with the parasite puncturing some of the palisade cells, injuring them so they and the surrounding cells begin to dedifferentiate and divide. The locally high rate of growth causes the leaf surface to buckle, producing a small pit. As the larva matures, the palisade cell layer and epidermis are then induced to dedifferentiate and grow, forming an upward-growing cup that surrounds and eventually encloses the larva. Such cups are not in any way a normal part of the leaf, but they are characteristic of the species of midge inducing it.

Needle galls, which afflict the leaves of the sugar a.

spongy mesophyll proliferates upper epidermis & palisade cells grow upward

Figure 9.8 Development of a bladder gall on the leaf of hackberry (Celtis) by the growth of a gall midge (Pachypsylla). a: Schematic development of the bladder gall. b: Cross-section through a Pachypsylla gall on a hackberry leaf. [From Wells (1964)]

maple, are formed in a similar way, but by a mite, not a midge. The mite dedifferentiates the epidermal tissues of the leaf, and the ensuing growth produces a thin column of epidermal tissue, which grows up around the mite, enclosing it. The thin needle-like column of tissue gives the gall its name.

### Leaf Temperature and Photosynthesis

Let us now shift gears a bit. Leaves, of course, are a plant's principal engines of energy acquisition. How well they perform this task affects all other aspects of a plant's biology. One would expect, therefore, that natural selection should refine leaves to work as well as possible. Natural selection can only do so much, however. Leaves function in a fickle physical environment—just consider the wild and difficult-to-predict fluctuations in so seemingly simple a thing as the air temperature. No matter how refined the functioning of a leaf is, natural selection's perfecting power will always be subverted by the chaotic variation of the physical environment in which the leaf exists. Often, this inescapable conflict is resolved by some compromise between efficient photosynthesis and variable leaf temperature.

The compromise is best understood by invoking a crass materialist analogy—the tree as an industrial corporation. A corporation works by taking money and doing something with it that adds value. The money put in is the investment, or capital, which is used to develop and operate the infrastructure that generates the added value. A corporation does best when it sustains the production of added value. This does not necessarily mean maximizing profit: sometimes it means diverting some of the added value away from profit and plowing it back into more investment. A healthy corporation is one that looks soberly at all the costs and returns that accrue to its operations and sustains the maximum sustainable difference between them. Generally, corporations that do so will fare better than those which simply seek to maximize profit.

Plants do something like this, but with energy, not money, as the currency. Plants take chemical energy (sugar) and use it to build infrastructure (leaves) whose purpose it is to capture the energy of light in chemical energy (photosynthesis). A plant does best when it sustains a maximum return on its investment, and temperature has a very important role in determining a plant's returns.

A plant cell, like any other cell, consumes energy both to maintain itself and to grow. Having a leaf commits a tree to meeting these metabolic costs, which are measured by how rapidly the leaf releases carbon di oxide. Similarly, benefits are measured by how rapidly the leaf consumes carbon dioxide, essentially, the rate at which the carbon in carbon dioxide is incorporated into sugar, also known as the gross photosynthesis (Fig. 9.9, top graph). A leaf returns added value on the investment in it if, in its lifetime, CO2 consumption exceeds CO2 production. In other words, the leaf succeeds if it has produced more sugar than it has consumed and its net photosynthesis (gross photosynthesis-metabolic cost) is maximized (Fig. 9.9, bottom graph).

It is important to realize that maximizing net photosynthesis does not necessarily mean maximizing gross photosynthesis. If we plot rates of CO2 consumption (by photosynthesis) or production (by metabolism) against leaf temperature, for example, we see a charac-

maximum gross photosynthesisl-

photosynthesis carbon flux maximum gross photosynthesisl-

photosynthesis

•'' metabolism

temperature

 net CO2