Vicious Viscosity

Many of the smaller invertebrate or invertebrate-like organisms in reef aquaria are well known to the aquarists maintaining those aquaria, but many of the factors influencing these organisms are a consequence of their small size and are difficult for aquarists to comprehend. "Strange" things happen in water when organisms are either very small or possess very little mass. As I have mentioned many times in this column, as aquarists we tend to interpret the world from our own perspective. There is absolutely nothing wrong with this, but in doing so, we must continually perform "reality checks" and realize that our perspective may not always provide an appropriate explanation of what is happening. In this particular case potential misinterpretations are due to size. Humans are among the largest animals on Earth; surely there are larger animals, but just as certainly, well more than 99.9% of all animals or animal-like organisms are smaller. And many of them are VERY much smaller. This size difference does have some profound consequences. Down to about the size of small aquarium fishes, or perhaps small bristle worms, most of the things that we take for granted about the world still work in ways that are familiar. But for very small organisms, well… it is like going through the looking glass after Alice: things can become very bizarre.

With regard to aquarium organisms, what appears to be strange is a result of the organisms' living in water. Water, like air, is a fluid medium. The properties of fluids relative to organisms depend upon the molecular properties of fluid's constituents, and the sizes and shapes of the organisms. We humans are used to air as one fluid medium with certain properties and to water with another altogether different set of properties. Yet, there are similarities between these media, and we can move through both of them relatively easily. This ease of movement depends largely on our mass. Once we start to move, our mass ensures that we build up momentum, or inertia, which allows us to move though the medium fairly easily.

When an organism's mass is low relative to the medium's viscosity, however, movement may become very difficult, indeed. As an example, if a human tries to walk in a wind blowing at about 100 miles per hour, his mass relative to the forces generated by the air's movement becomes small, and it becomes quite difficult for him to control his motion. Frictional effects, particularly drag, increase and instead of being able to move into the wind, he may find himself being blown along by it. Water is a much more viscous medium than air, so similar viscosity effects become apparent at much lower fluid velocities in water than in air. A scuba diver who is not carrying any excess equipment can swim against a water current flowing at between 1 and 2 miles (about 1.6 to 3.2 km) per hour without much difficulty. On the other hand, if the diver is carrying a lot of equipment, such as cameras and research gear, his effective frontal area increases, and so does the water's resistance to something moving through it. This resistance increases with the square of the frontal area, so doubling the frontal area increases the resistance by a factor of four. This means that for a scuba diver carrying bulky equipment, swimming even just enough to maintain a steady and stable position in water moving at 1 mile (1.6 km) per hour may be difficult. Relatively large scale oceanic water movements generated by tides or winds can travel at velocities well in excess of 5 miles (8 km) per hour, and at these velocities a diver becomes simply another piece of debris blowing along in the currents.

Allow me to share with you one of the shorter, but exciting, moments of my research career. One of the research sites that I used for my doctoral dissertation was the lower intertidal region of beach on the eastern side of the channel called "Point Washington Narrows" near Bremerton, Washington. Tidal currents in this channel exceed 10 miles (16 km) per hour. I once got a wonderfully wild and crazy (i.e., very stupid) idea to see what was happening in my study area while it was submerged during maximum flood tide. I strung lines across the bottom, and thought I would be able to 1) orient myself using the lines, which were labeled; and 2) hold on and make observations of the animals, some venomous snails I was studying. I did a lot of my research diving solo, and this time was no different so, fortunately, I didn't have to worry about a buddy. The water current in the area dissipates at either end of the narrows, a channel about a mile (1.6 km) long, so that even if the current became too extreme, I figured I could ride it out and be in relatively safe waters. I waited for the current to reach its maximum, donned my dry suit and entered the water. The results were ludicrous. I was flushed so rapidly through the area that I never even had a chance to grab onto the ropes I had strung over the bottom. Additionally, visibility in that water was relatively poor. By the time I could see the lines, I was past them and couldn't grab them. In retrospect, this was probably a very good thing. Had I been able to grab one and hang on, I would have been flapping like a torn flag in a gale. I did see my study site… it was about 530 feet (160 m) long. I passed over the entire site in less than six minutes, and believe me, in the murky, cold water of that December day in 1974, that was a real cheap thrill! However, it did give me a really good appreciation for the problems of being small in a viscous medium. Ah, to be young and dumb(er) again…

The point of this recollection is not just to illustrate the idiocy of youth, but to note that most marine organisms experience similar effects at much lower velocities. This is because they have a much lower mass so, relative to their sizes, water is much more viscous. This viscosity is due primarily to the dielectric properties of water molecules, which tend to cause water molecules to attract other water molecules. In effect, water molecules "stick" to one another. This "stickiness" of water has a great deal to do with both the movement of small organisms in it and its movement through small channels such as the interstitial pores of a deep sand bed, or the spaces inside an animal where it is moving as blood. Water's properties have a great deal to do with the design and functionality of organisms, both on the outside and on the inside.

Movement

Figure 1. Pseudopodia are generally too small to see with the unaided eye. However, the sessile red foraminiferan Homotrema rubrum, which is common in aquaria, catches particulate organic material on pseudopodia that it extends out into the water. These are visible as fine, threadlike extensions at the ends of the foram's branches.

As far as organisms are concerned, probably the most basic functional property that viscosity affects is water movement, and their small size combined with water's odd properties go a long way toward explaining some of the basic biological attributes of tiny organisms. The most fundamental type of movement found in tiny animal-like organisms is done by extending their body's entire surface. This type of movement is seen to best advantage in organisms such as amoebae. Small organisms, on the size scale of amoebae, are generally less than about 0.1 mm (1/250 inch) in diameter. Often these organisms are not comprised of multiple cells, and because of this they are not animals, which by definition are multicellular. Such organisms belong to several different and unrelated lineages, but we often lump them together by calling them protozoans, a name that means "first animals," as at one time they were considered to be simple animals, possibly similar to the ancestors of "true" animals.

Protozoans tend to have a lot of peculiar bodily structures derived from the single cell that constitutes their body but, of course, they lack things such as muscles and skin and other cellular derivatives. All amoebae and their relatives; organisms such as true free-living Amoeba; many similar parasitic forms such as Entamoeba histolytica, which can cause dysentery in humans; and the foraminiferans common in marine environments and aquaria can move by extending blobby, hair-like, or even net-like extensions of their body's surface called "pseudopods," a name meaning "false feet." Pseudopods typically move because of some interesting properties of the organism's structure. The outer part, called the "ectoplasm" of the organism, just inside the exterior surface's covering, or cell membrane, is altered chemically and becomes more fluid. Internally, the fluid that constitutes the internal bodily "goo," or cytoplasm, is filled with all sorts of odd chemicals, including a network of long and interconnected proteins connecting all the various parts of these tiny organisms' internal structure. These proteins are altered, causing some of them to contract, which forces the cytoplasm out into the more fluid regions. This, in turn, forces the cell membrane outward into a long extension, "the pseudopod." Pseudopods are quite effective locomotory devices and are surprisingly mobile and agile. In laboratory exercises, students are often quite amazed to watch what appears to be a "sluggish" amoeba capture and eat far more rapidly moving protozoans or even small animals such as rotifers. It is apparent from watching the movement of pseudopods that they don't move through the water easily. It provides a lot of resistance, and instead of rapidly flowing outward, they ooze slowly through it, often taking seconds to move just a few micrometers. Additionally, water's viscosity can be seen to influence the locomotion of amoeboid organisms in another way. If the water is relatively still, amoebae may be seen moving vertically through the water column. They are not swimming as much as simply climbing up into the viscous water. To these organisms water is about as fluid as thick corn syrup is to us, and they can quite easily climb up into it.

Pseudopodial movement is found in most free-living unicellular organisms, with the exception of diatoms. It is found also within the bodies of most multicellular organisms because these organisms contain cells that move around freely within and through tissues. For example, corals and other cnidarians contain "interstitial cells." These are cells that are termed to be "undifferentiated," which simply means that they don't look like anything other than a generalized animal cell. In other words, they look like an amoeba. They act like one, too. They move from place to place within the coral and can perform all sorts of tasks, depending on the animal's need. They can help repair injuries or turn into an egg, or turn into any other type of specialized cell. Aquarists also have many cells in their bodies that move by the use of pseudopods. Probably the most abundant of these are white blood cells, especially macrophages, which look and act quite like amoebae.

Cilia

Although pseudopodial movement is ubiquitous, probably the most widespread and common locomotory "device" used by organisms is a microscopic beating filamentous structure referred to, variously, as an undulopodium, a cilium or a flagellum. The main structural difference between a cilium and flagellum is length; flagella are typically many times longer than cilia. The mouthful term, undulopodium, used in a few texts and references, is a term devised to encompass both cilia and flagella. These structures are microscopic and therefore invisible to the unaided eye. In fact, they are so small that their basic internal structural attributes are invisible even with the best light microscope. As a consequence of this, an understanding of ciliary structure and function had to await the development of the electron microscope, which can magnify structures to a much greater degree than can a light microscope. Although cilia and flagella have been known for several hundred years, their main structural components and mode of operation remained undiscovered until the latter half of the twentieth century.

A cilium or flagellum is an extension of a cell's surface. Although hair-like in proportion, it is not a hair in the sense of a mammalian hair. Mammalian hairs are non-living proteinaceous excretions of glands located in the skin, and are thousands of times larger than either cilia or flagella. The cellular surface extension that comprises the cilium or flagellum is very narrow and roughly circular in cross-section. These structures are typically many hundreds of times longer than wide. As they are extensions of the cellular surface, they are covered externally with a cell membrane continuous with the membrane covering the rest of the cell. Internally, both structures possess a rather consistent anatomy. They are comprised of nine tiny tubular molecules, called "microtubules," which are arranged in a helical pattern. In the center of this helix of nine microtubules are two more microtubules. This rather peculiar arrangement of 9+2 microtubules is remarkably consistent throughout organisms possessing cilia or flagella. The internal microtubular arrangement is the same in the flagellum of a green unicellular microalga such as Euglena (1), or in a dinoflagellate, or in a human sperm cell, or in an epithelial cell of a coral. This unity of structure is considered to be one of the fundamental unifying factors showing that all life is related.

To explain that everything has its cost, we often use the aphorism, "There is no free lunch." That truism is as valid with ciliary locomotion as it is with the more familiar muscular movement. It takes energy to make motion. Cilia or flagella move by the application of chemical energy, most often derived from the breakdown of an adenosine triphosphate molecule (ATP) to an adenosine diphosphate (ADP) molecule and a free phosphate ion. The release of that phosphate ion liberates chemical energy that is used to move the nine external microtubules relative to each other and relative to the internal pair. That movement causes the entire structure to bend and flex. The bend and flexion is done in a specific "twisting" pattern resulting in a relatively stiff "power-stroke" phase and a rather flaccid "recovery-stroke." If the power stroke is from a cilium, the water is generally moved downstream toward the tip of the cilium or the animal is moved in the opposite; remember Sir Isaac Newton's third law regarding direction of forces. If the power stroke is from a flagellum, the resultant thrust vector is much more difficult to predict, and may be either direction along the flagellum or even lateral to the axis of movement. During the power stroke, the hair-like structure pushes against the water molecules and acts to move either the water or the organism. The only reasons a cilium or flagellum actually can function are because of the water's cohesiveness and the small size of the organism using it. When we view the movement of a cilium or flagellum, it often appears as if a fine thread is moving in fluid water; intuitively, we know that such a movement would generate very little thrust. Actually, the ciliary or flagellary action is more like an oar sculling through water to push a boat and, on the scale of a microscopic organism with very little inertia, the force generated by a cilium or flagellum is quite sufficient for movement.

Nevertheless, the thrust developed from one flagellum or cilium is relatively small, but so are the organisms they move. On a relative scale of body lengths per second, many flagellated organisms with a single flagellum can move rapidly over relatively great distances and, of course, all of the readers of this column are the result of just such a race run by many small flagellated spermatozoa. While most organisms tend to bear flagella in more-or-less small groups, generally from 1 to 10 per microscopic organism, there are exceptions to this, and some flagellated protozoans found in termite and wood-roach guts may be covered in thousands of flagella (See this diagram and image of Trichonympha, a flagellate found in the guts of termites).

Cilia, on the other hand, are more typically found in huge numbers. Many small mobile organisms such as ciliated protozoans, the numerous free-living flatworms, acoelomorphs (the so-called "acoel flatworms" such as the "oh, so familiar" red planarian, Convolutriloba retrogemma which is not even a typical flatworm, let alone a planarian), and ribbon worms are completely covered with them. Additionally, discrete bands of cilia are often found on larvae and are quite capable of moving them rapidly and over great distances. Small, ciliary swimming organisms are exceptionally common in the world's oceans, and are often the foods of many suspension-feeding organisms such as stony corals, soft corals or other filter feeders.

Ciliary locomotion on surfaces results in the characteristic "gliding" movement typical of many small aquarium animals, seen to best advantage on aquarium walls. In these cases, the animal is moved by its cilia in a manner quite like that of a microscopic ciliated protozoan. It may be a bit surprising, but many larger animals also utilize cilia for locomotion. Among animals living on the ocean's bottom, it is likely that the most massive animals to move by ciliary means are many large snails that move using a ciliated foot. These snails move with a gliding motion created by the ciliated epidermis covering their foot. In aquaria, the most common snails to move in this manner are probably the meat-eating scavengers in the genus Nassarius.

Most mobile and sessile marine animals that lack an exoskeleton possess cilia on their epidermis. These cilia move water over the epidermis and continually bathe the animal's surface in clean sea water. Such an arrangement is found on animals as varied as corals and sea stars and is probably the most effective way of maintaining the cellular surface in good condition. The water movement so generated acts to facilitate diffusion of materials both into and out of cells. Such self-generated water movement is particularly important to sessile animals such as corals. In many normal marine environments, the water flow near the substrate is almost nil due to the water's viscosity and the development of a water layer called the benthic boundary which gets created close to all surfaces in areas with smooth or laminar water flow. Boundary layer effects may be seen in air as well; the equivalent to the underwater benthic boundary layer is found over the surface of a moving fan blade. Even though the blade may be moving a lot of air, the air directly over the blade's surface is stagnant, and dust, which can easily be blown off the blade, will settle on it, even as it is moving. Similarly, laminar water current flowing over an organism will not move water in the benthic boundary layer that surrounds the organism and without some means to generate such currents, even on a small scale, organisms would suffer problems in breathing and waste transfer.

Conclusion

An understanding of the basic cellular means of locomotion, whether or not they move the organisms or water around or even function within organisms, is fundamental to the understanding of the "biology" of all organisms. On the basest level cilia or flagella move small organisms. They also move water around larger organisms, assisting in respiration and waste removal. On top of this, they are also found within many organisms moving fluids from one portion of the body to another. For example, in echinoderms such as sea stars and their relatives, cilia move the body fluids around and act as the motive force for internal circulation. Although these animals don't have a circulatory system with a muscular heart, fluids move within circulatory channels under the coordinated and cumulative action of millions of beating cilia.

Ciliary and flagellar locomotion are the fundamental means of rapid locomotion by small organisms, and were undoubtedly the means used by the first small mobile animals, animals apparently quite like acoelomorphs (1, 2, 3) in size and structure. However, this type of locomotion is limited by the size and, to some extent, the shape of the organism. For animals to get big and to be successful, other means of movement were necessary. Next month, I will discuss locomotion by muscular means and how the development of discrete muscular layers first allowed effective crawling and then rapid swimming.

Figure 5. Although acoelomorphs look like flatworms or ciliated protozoans, they are not closely related to either group, but instead appear to be a remnant of the ancestral stock of all bilateral animals. This small, 0.05 mm (1/500 inch) long, acoelomorph has eaten a diatom, which is visible in its body. All acoelomorphs move using cilia.

References:

Barrington, E. J. W. 1979. Invertebrate Structure and Function. 2^nd Ed. John Wiley & Sons. New York, NY. xiv+765pp.

Kozloff, E. N. 1990. Invertebrates. Saunders College Publishing. Philadelphia. xiv+866 pp.

Ruppert, E. E, R. S. Fox, and R. D. Barnes. 2003. Invertebrate Zoology, A Functional Evolutionary Approach. 7^th Ed. Brooks/Cole-Thomson Learning. Belmont, CA. xvii +963 pp.+ I1-I 26pp.

Vogel, S. 1994. Life in Moving Fluids. 2^nd Ed. Princeton University Press. Princeton, NJ. xii+467pp.