Illustration: Brian Bookwalter
From the massive Blue whale to the tiniest plant viroids, size extremes have long fascinated mankind. This is not a trivial pursuit, for size can yield important insights into the physical constraints that govern an organism's evolution, as well as the particular mechanisms that impose a limit at either end of the scale.
Some size limits apply broadly to entire classes such as mammals, while others apply more narrowly to a single species because of its particular ecological niche. Species limitations tend to be imposed by the selected mode of feeding or locomotion, with insects being the most widely studied group in this respect. Recent research is answering various longstanding questions about animal size, such as why insects cannot be too small, and perhaps why mammals cannot get any larger than the Blue whale.
BEATING THE MIDDLE MAN One group whose size is confined within tight boundaries is the xylem-feeding insects such as the cicadas. They extract, through a syringe-like snout, a weak nutrient solution through the xylem vessels located in the plant's roots. "It is rather a bizarre way of feeding, as xylem vessels carry almost pure water. It's one of the most nutrient-poor food sources plants can provide herbivorous insects," says Vojtech Novotny of the Parataxonomist Training Centre in Papua New Guinea.1
These insects need to ingest 400 to 800 times their body weight of xylem fluid per day for sufficient nourishment. In addition, they must expend considerable energy, because xylem fluid, unlike the sap-containing phloem that aphids consume, is under negative pressure that must be overcome by suction. The crucial point is that metabolic rate increases with decreasing body size, requiring more food per unit mass. Also, friction causes the resistance to suction imposed by the walls of the feeding proboscis to increase (as a ratio to body mass) as the diameter of the proboscis decreases. These factors together impose a minimum size limit that is larger than for a typical insect. For this reason, says Novotny, xylem-feeding insects such as cicadas are big, whereas phloem-feeding insects such as aphids, which need only tap the vessel to turn on the flow, can be very small.
Illustration: Brian Bookwalter
Yet constraints that apply to insects in general also confine xylem-feeding insects at the top end of the size range. Two theories attempt to explain why insects, such as the hawk moth, are limited in maximum size to around 15 cm in body length, 20 cm in wingspan, and 70 g in weight. Both explanations could play a part in constraining insect size evolution, says Michael Dickinson, professor of integrative biology at the University of California, Berkeley.
First, insects have evolved a method of distributing oxygen to the muscles that differs from vertebrates, including other flyers such as birds and bats. Instead of binding oxygen to hemoglobin in blood, insects carry it directly through internal air pipes. "For a small animal it's much more efficient," says Dickinson. "It's like beating the middle man." The final link in the distribution chain, taking oxygen into muscle cells, relies on gas diffusion from high to low concentration, and the efficiency of this declines rapidly at distances beyond a decisive point. "There seems to be a critical size beyond which you can't get enough oxygen into the tissue," says Dickinson.
The other, subtler constraint stems from the aerodynamics of insect flight, which differs from all birds except hummingbirds. Most bird flight can be explained, like airplane flight, on the presumption that airflow is smooth and regular. A vertical pressure gradient across the wing generates uplift. The bird wing is designed and elevated in such a way that the airflow has to travel further above the wing, causing the pressure to drop. Beneath the wing the pressure is higher, and so an upward force is created.
Illustration: Brian Bookwalter
For insects, this conventional aerodynamic force alone cannot provide the uplift, partly because it doesn't explain how insects can hover. A pioneer of insect flight study, R. McNeill Alexander, notes that unlike birds, insects flap their wings unsteadily, constantly changing direction and speed, causing their wings to rotate with each variation. Various detailed explanations exist about this process, but the common consensus is that with these rotations, insects create additional uplift by creating vortices that change pressure in the vicinity of their wings and bodies. In a sense, the wings act like a suction pump, creating regions of low pressure above the insect and corresponding uplift. The key to sustaining these pressure changes (and therefore keeping the insect airborne) is viscosity, defined as a substance's resistance to shear force, or the power that causes a substance's layers to slide, often atop one another. Air has a low viscosity, and so as an insect becomes larger, the air pressure differences caused by the flapping wings tend to dissipate too quickly between flaps to sustain uplift, imposing a maximum size limit.
An obvious objection to both explanations for maximum insect size can be made in the Paris Natural History Museum, which houses a fossil with a two-foot wingspan, the giant dragonfly from the Carboniferous Period. The generally accepted explanation of this apparent contradiction is that the atmosphere was substantially richer in oxygen then, allowing diffusion to be effective at greater distances, says evolutionary biologist Blair Hedges, Pennsylvania State University. But how could the dragonfly soar above the apparent dynamic size limit for current insect flight? This dragonfly may have evolved bird-like flight relying solely on conventional aerodynamics.
Viscosity also imposes a minimum limit on a flying insect's size, says Dickinson. At small sizes, the ratio between inertial mass and viscosity, known as the Reynolds number, becomes so small that wing flapping becomes hard to sustain. "That is why the very tiniest insects flap in a very unconventional way," says Dickinson.
Viscosity imposes a minimum size limit on another insect class, the water skimmers, and also water-skimming spiders, but for a different reason. At small sizes, the resistance to movement imposed by the water's viscosity becomes more significant, making it harder for the legs to generate the tiny vertical whorls or vortices beneath the water's surface to move the insect forward. "That would suggest that they have to be bigger than 1 mm, which does correspond roughly with minimum size observed," says mathematician John Bush, Massachusetts Institute of Technology, who with colleagues has studied water-skimmer locomotion.2 These creatures have a maximum size limit because they rely on surface tension to walk on water. If they became too heavy, their legs would break through the water surface and they would sink.
Illustration: Brian Bookwalter
PUMPING CALCIUM IN THE AIR In vertebrates, different rules govern size. Until a few years ago, it was thought that vertebrates had no general maximum size limit. The evidence suggested that Cope's rule--which states that animals generally will evolve to ever greater size--holds for mammals: The Blue whale is the largest animal in natural history.
In the case of flying birds, though, a rough maximum size limit is applied by the high energy required by a big animal for sustained flight, which is why swans and other large flying birds spend but a small portion of their time in the air. With increasing size, they become less dependent on flying to find food or escape from predators, to the point where birds such as the ostrich stay on the ground.
The minimum size of birds is limited by the vertebrate mechanism of muscle contraction, which depends on pumping calcium out of the muscle cell, says Dickinson. The smaller the bird, the faster the wing-flapping (which can approach speeds of 400 times per second). At this point, timely pumping of the calcium becomes difficult, leaving insufficient power for wing flapping. "If you look at really fast vertebrate muscles, such as the tail of a rattlesnake, or the eye muscle, there is precious little left except for the calcium pump," says Dickinson. "They're really wimpy."
The hummingbird, however, has managed to take vertebrate wing flapping to a new limit. "The wing of a hummingbird has lost a joint; it operates more like a face plate beating back and forth, like an insect does," says Dickinson. Unique among vertebrates, hummingbirds have jumped through an evolutionary hoop to fly like insects, able to create local vortices to hover in still air. They compete not with other birds but with hawk moths, which they resemble in both size and flight dynamics, and whose high-energy diet they share.
SIZING UP THE NONFLYERS For other nonflying vertebrates, different factors impose minimum size. For mammals, reptiles, and amphibians, as body mass decreases, the ratio of surface area to volume increases and causes greater loss of heat and water. Fish, which in warm waters experience neither of these problems, do not come much smaller. Another explanation is that a central nervous system cannot function below a certain size, but Hedges brushes aside this thought. Certain bilaterally symmetrical multicellular animals, such as tardigrades, which are related to arthropods, have limbs and nervous systems and are microscopic.
This points to another explanation, advanced by Geoffrey West and others3: For mammals, the minimum limit is imposed by the dynamics of vertebrate pulse-driven blood circulation; this breaks down at a body mass of around 3 g, which happens to be the mass of the smallest mammal, the shrew. In a mammal's circulatory system, blood is driven by pulses into branching vessels that become progressively narrower. As the vessels divide further downstream into tiny capillaries that feed the cells, the pulses of blood become so heavily dissipated by resistance that they disappear completely; energy waves can no longer propagate. Circulation in an animal smaller than the shrew would consist of only tiny capillaries; at this scale even the aorta would be of capillary size. Pumping blood from the heart would become highly inefficient because the energy pulses would be dissipated immediately. An animal this small would have to evolve a different way of distributing oxygen and nutrients. West suggests that his theory for mammals would apply equally, with appropriate changes in parameters, to all vertebrates.
More recently, West has suggested that his theory also imposes a maximum size on vertebrates. Although mammals do seem to have scaled up during their evolutionary history in line with Cope's law, West argues that this cannot continue, according to his model; in principle, the upper limit would apply to all vertebrates, with appropriate changes in the model's parameters.
The key point of West's theory states that the number of blood capillaries scales with increasing organism size only as 3/4M (where M equals mass), while the number of cells in the body scales almost exactly as M. This means that as the organism becomes bigger, the ratio between the number of cells and the capillaries feeding them increases. As West notes, this increase cannot continue indefinitely, because the cells need to be serviced by blood, and this becomes harder as the capillary network is more sparse in large animals. "Diffusion of oxygen and other nutrients from capillaries to cells can only support approximately four cells between adjacent capillaries, compared to about one for the smallest mammal," says West. Doing the scaling maths, this would suggest that the ratio between the masses of the largest and smallest mammals should be 10 million (107), says West. Indeed, calculations reveal that the ratio between the masses of the Blue whale and shrew is about 10 million, suggesting that mammals have already scaled to the limits of their evolutionary size range at both ends of the scale and that Cope's law will no longer hold. Says West: "This, again, is an argument that can be applied to other taxa."
Philip Hunter (firstname.lastname@example.org) is a freelance writer in London.
1. V. Novotny, M.R. Wilson, "Why are there no small species among xylem-sucking insects?" Evol Ecol, 11:419-37, 1997.
2. D.L. Hu et al., "The hydrodynamics of water strider locomotion," Nature, 424:663-6, Aug. 7, 2003.
3. G.B. West et al., "Allometric scaling of metabolic rate from molecules and mitochondria to cells and mammals," Proc Natl Acad Sci, 99 (suppl 1):2473-8, 2002.