WATER QUALITY: Technical Information--"Aquatic biology: Some thoughts on its history, principles, and future needs" In Reply Refer To: April 15, 1980 EGS-Mail Stop 412 QUALITY OF WATER BRANCH TECHNICAL MEMORANDUM NO. 80.13 Subject: WATER QUALITY: Technical Information--"Aquatic biology: Some thoughts on its history, principles, and future needs" by Robert C. Averett, WRD, Lakewood, Colorado. Enclosed for your information is the subject paper, which was prepared by Bob Averett for use at the 1979 California District Conference. Bob's thoughts about the past, present, and future of aquatic biology should be useful in putting that area of hydrology into perspective as we continue to expand our water-quality programs. Please circulate the paper as widely as possible in all district and project offices. Thank you. R. J. Pickering 7 Enclosure WRD Distribution: A, B, FO-L, PO Key words: water quality, information, aquatic biology Superseded memoranda: none AQUATIC BIOLOGY: SOME THOUGHTS ON ITS HISTORY, PRINCIPLES, AND FUTURE NEEDS by Robert C. Averett INTRODUCTION The title of this paper would indicate that it is a position paper on research needs in aquatic biology. In part that indication is correct; in part it is in error. An individual has no license to prepare a position paper on such a broad important subject as aquatic biology. What is intended in the pages that follow is to elaborate a bit upon the history of aquatic biology, at least the recent history. Following the historical part is a discussion on the modern view of process biology in streams and lakes. Obviously, we only will be able to touch upon the highlights. Next is a discussion of advances in the field in the past several decades, an era of significant importance in aquatic biology. It relates how these advances are tied to the past and the future. Finally, I will give my viewpoints on some of the items that need further exploratory work; items that I believe will make aquatic biology a more useful science to mankind. I hope that this type of paper will be more useful as an instrument to stimulate thought and future research than as a guide to an understanding of how we do things. I ask the reader to keep in mind that the statements in this paper are, in most instances, my own interpretations. Another author might well see the past somewhat differently, and the future quite differently. I believe, however, that I have covered enough material to insure a strong enough link between the past and the future to put some reliability into both. Anyone with the simplest knowledge of the history of science will know that these are fast-changing times. We often attribute this fast pace to the 1960's. Not so; they were the "much studied times", when research money and those who used it were easily obtainable. The 1960's were a peak period for data gathering, as well as a period for some excellent interpretation of those data. For example, biochemistry is a field of science that flourished in the 1960's, and continues so today, primarily I believe, because of the momentum that began in the 1960's. Without question, most fields of science have moved ahead in recent years; some more rapidly than others, and some with a more scientific steadiness than others. I put aquatic chemistry in the latter category. Progress in aquatic chemistry has followed many of the best laid plans of experimental design--test, revise, test, revise, conclude, hypothesize, continue to disprove the hypothesis. Even so, while aquatic chemistry has made some excellent strides in recent years, its greatest thrust has been in analytical techniques. We are able to analyze for a great number of elements and compounds in water. Our understanding of what these analyses mean has not moved forward at anywhere near the same rate. In most disciplines of science, we have attempted in very recent years to model the processes involved. Modeling, to mathematically mimic the elements of a natural process, would of course provide the best of both worlds. We could have it both ways in that we could not only understand the processes involved, but we also could describe them mathematically. The computer spawned the era of modeling and it has added much to our understanding of the several branches of science. The manipulation of computer-spawned mathematical models often has made us reevaluate our thinking and learn much more about the processes involved in nature. Such is science in its simplest but most productive form. Where does aquatic biology fall within all of this fast-changing, much-studied, process-understanding, modeling myriad of things? Rather than give a positional answer--beginning, middle, or end, I prefer to discuss the past, followed by a brief essay on our understanding of aquatic ecosystems today, and then discuss the present, followed by some thoughts on the direction aquatic ecology should take to be a more useful science to mankind in the future. The future is the most fun to predict and, after all, it is the only place we are going with any assurance. But predicting the future always depends upon the progress and the direction of the past. Let us begin there. WHERE HAVE WE BEEN? I do not know where aquatic biology began. Man has always been interested in the aquatic flora and fauna about him, and early man certainly was aware of life in streams and lakes, for such life provided a source of food. In fact, many tribes of early man were welded to the stream bank or lake shore because of the source of food it supplies. We credit Carlos Linnaeus for first describing, in a logical manner, the numerous types of plants and animals on earth in his three books published in 1753, 1754 and 1758. Linnaeus was a classifier, a taxonomist, and as such was a descriptive scientist. His classification schemes and descriptions were more along the line of the naturalist of some 10-20 years ago, who knew certain things happened in a somewhat repeating manner, but never really understood why. This was scientific evidence without an experimental design. Immediately after the work of Linnaeus, aquatic biology, and biology in general, underwent some significant discoveries and changes. Anatomy (form and structure) was still the keystone of the science; it was easy to study. Physiology (function), however, was becoming a branch of the biological sciences in its own right. Biochemistry, which united physiology and chemistry, was a century or more away from the time of Linnaeus. It was almost two centuries away if you consider only the modern concepts and discoveries of biochemistry. I believe it was physiology that truly moved biology ahead as a science. While not appreciated nor understood as functional processes, many biological discoveries made at the change of the present century were physiologically orientated. It was, in fact, in the late 1800's and early l900's when aquatic biology came into its own. Agriculture, industry, and urbanization with the flush toilet altered the aquatic environment in many parts of the world. The environmental changes were stream bottom alterations, areas of depressed dissolved oxygen, the introduction of toxic materials, and combinations of the above. Aquatic life either disappeared or the species composition was altered greatly. The presence of some forms of aquatic life and the disappearance of others in streams receiving organic waste material were noticed and recorded by a number of investigators. The presence or absence of fish was particularly noticed, because fish were easy to observe and were of economic value. But effects on other aquatic organisms were recognized and studied as well, and we owe much of our present-day understanding of aquatic biology to these early-in-the-century investigators, especially Kolkwitz and Marrson 1908, 1909), who introduced the concept of classifying organisms based upon their location on organically polluted streams. While lake studies were somewhat common place in Europe, they were relatively new in the United States until about 1910. Birge and Juday, two lake limnologists from the University of Wisconsin, pioneered lake studies in the United States. Their work on heat budgets and photoplankton distribution in lakes remains as a monumental work of science to this day. While Birge and Juday are credited as the "fathers" of lake limnology, the work on recognizing lakes as ecosystems truly belongs to Forbes, who in 1887 wrote his classical paper "The Lake as a Microcosm" (see Forbes, 1925). Studies of aquatic biology at the turn of the century and shortly thereafter set the stage for what was to come. Two things seemed reasonable then as they do today: (l) that the presence of particular organisms should indicate particular environmental conditions (indicator organisms); and (2) it should be possible to determine the concentrations of particular chemical constituents that are lethal to aquatic organisms (toxic levels, and thus be able to use streams for the production of aquatic crops as well as for waste disposal. Our success in these two endeavors, even today, has not been outstanding. We simply have underestimated the complexity of the aquatic environment. More on this will be discussed later. In the late 1920's, 1930's, and 1940's, there was a somewhat sporadic research effort to view and measure the energy and material utilization by plants and animals. This research effort was not continuous throughout the three decades, and took place in institutions somewhat distant from one another. There seemed to be no pattern of concentrated effort. While research was pioneering in almost every detail, it also was, for the most part, very sound research based upon well-thought-out experimental designs. The works of Brody (1927) and Lindeman (1942) remain classics. This energy and material utilization or "pathway" research paved the way for the concepts and principles of biological production, a study phase that began in earnest in the 1960's and is still going strong today. More will be said later on energy, material, and production. First, let us look at streams and lakes as environments, and at some new knowledge on stream ecology. FRESHWATER ECOSYSTEMS When compared to the oceans, freshwaters are dilute with regard to dissolved materials. All, however, support some type of aquatic life. The type of life varies greatly and the amount of living tissue that is produced per unit time also varies greatly and depends upon a number of factors, some of which are poorly understood. Consider a stream that begins in the mountains, receives water from other streams as it moves downgradient, eventually enters a lowland river which eventually flows into another larger river, or flows into the sea. The uppermost reaches of the stream (first order) have steep gradients which result in a rather rapid movement of the water. The stream bottom is often bedrock, and usually the stream bank is crowded with terrestrial plants (grasses, shrubs, and trees). Some vegetation, often aquatic mosses (although there are few "typical" plants), will be found in the stream growing on the banks or bottom. Some attached algae (periphyton) also will be found, but that probably will be the extent of the aquatic plant life. If the stream bottom is examined, a distinct invertebrate fauna will be found. The fauna often will be of a type having strong holdfast organs and a streamlined body that assists them from being swept downgradient by the current. From a descriptive standpoint, we could stop our discussion here for we have described the stream reach with such terms as steep gradient, terrestrial shoreline vegetation, bedrock bottom or substrate, some aquatic plants (mosses and periphyton), and aquatic invertebrates with strong holdfast organs. The descriptive part is easy. The processes which make it possible for our stream to support this life, or for the life to live in the stream, is exceedingly complex. We might ask the questions, "Where do these invertebrates obtain their energy and material, why are there not more aquatic plants in the stream system, what role does the terrestrial vegetation play in the scheme of things, and how does this headwaters stream section affect life and chemical quality in downstream stream sections?" When we ask these questions we are beyond simple descriptive biology. We enter the field of process biology and we weld it to hydrology. We are relating stream processes to one another and making an effort to understand the entire ecosystem. Asking the above questions has been an active part of recent research in aquatic biology, and because of this research, we can now answer some of the questions. A primary reason that there are few aquatic plants, including algae in the headwater stream, is that the stream section is shaded and only a very low light level reaches the stream bottom. The light energy is captured by the higher terrestrial vegetation. Another reason for few plants is the lower water temperature which in turn lowers the rate of plant production. A third reason is the lower concentration of dissolved or available nutrients in the stream reach. If, however, we measure the animal component of our stream, we find more biomass than we can seemingly account for on a material and energy budget. How can this be? The answer is relatively simple in that animal production in the stream depends upon the terrestrial input of material and energy. Leaves, twigs, needles, and of course, dissolved materials leached from the soil supply the material and energy necessary to drive the stream ecosystem. We term inputs of Such "outside" material as allochthonous. Simply, the material is transported from one ecosystem to another. As the stream moves downgradient, it receives water from other streams and becomes a second, third, and so-on order stream. As the gradient lessens, the stream bottom changes, often resulting in a more diverse array of microhabitats for aquatic organisms. Alternating pools and riffles describe its profile. No longer is the stream bottom only bedrock. Now there is clay, sand, gravel, and boulders present, and each provides d habitat for various plants and animals. Water movement may still be rather rapid but there are numerous places where an organism can avoid the direct effects of the current. While there is still streamside vegetation, the stream is often wide enough to permit direct sunlight to pass through the water. As a result, primary production in the form of algae and even some rooted aquatic plants are found. In much of the year, in-place primary production by plants supplies the material and energy to drive the stream ecosystem. We call this in-place primary production of organic matter autochthonous material; that is, material synthesized in the stream. Because of the more varied habitat and increased organic production, this downgradient stream section will have a more varied fauna and higher rates of production. Remember too, that this stream reach obtains terrestrial material input (allochthonous material) from the headwater reach. In addition, this downgradient stream reach also receives allochthonous material from its surrounding basin. Further downstream we reach a lowland river, a sort of catch basin for all upstream material. Slower velocities and deep pools characterize the river. Primary production by algae and higher aquatic plans insures that the stream is autochthonous with regard to material production. In many instances (in the absence of man's influence), the stream section would be self-supporting. Man's influence usually has been to add more organic matter from outside sources, especially domestic wastewater. The fauna of this downstream reach often will be a mixture of flowing and standing water types. Many of the fauna types in the deeper stream stretches are found in lakes as well. Because this river reach acts as a depository for sediments, the bottom material is often unconsolidated, and burrowing organisms are commonplace. I have not mentioned fish in the above discussion, but they are important inhabitants of each reach described. They are extremely temperature dependent, but temperature alone does not completely influence their distribution or species composition. Fish production and biomass, however, in the absence of toxins, does increase in a downstream direction. The problem is that from an economic standpoint, the highest production rates may be of a species undesirable for man's use. I Lakes are standing bodies of water which may have multi- directional currents depending upon the wind direction and speed. As mentioned, lakes and large rivers have many habitants in common. Some areas of lakes that receive the Influence of winds may have micro-habitats similar to riffles in streams, and the fauna may be similar. Lakes act as depositories for earth and stream-borne materials and the bulk of their bottom material is unconsolidated. Thus, burrowing organisms are often most common in lakes. Many lakes undergo distinct spring and autumn circulation and summer stratification patterns. When stratified, the warmer surface water does not readily mix with the cooler bottom water. In lakes with high amounts of organic matter, bacterial respiration in the cooler bottom water may remove most, if not all, of the dissolved oxygen. When this occurs, a large part of the lake may be uninhabitable by higher organisms. Some burrowing organisms can survive under low dissolved-oxygen concentrations, but not under anoxic or depleted dissolved-oxygen conditions. Only anaerobic bacteria can remain alive under anoxic conditions. Most lake problems today revolve around enrichment by phosphorus and other nutrients and the attendant problem of excessive production of algae--algal blooms. Not too long ago, we considered both nitrogen and phosphorus as the culprit nutrients. We argued among ourselves as to which was the most important and why, and we made studies that often showed that the nitrogen concentration in a lake was proportionately lower than was the phosphorus concentration on the basis of expected cellular concentrations. Our calculations may have been correct, but our knowledge of blue- green algae physiology was primitive. We now know that blue-green algae, the group that causes most nuisance algal blooms, can fix nitrogen, much like legumes. Thus, phosphorus generally remains the main culprit nutrient for triggering excessive algal production. There are other nutrients that are required by algae, but phosphorus remains the most important for arresting algal production. The study of freshwater ecosystems is not as simple as any of the descriptions given above. I have only touched upon some of the more simple concepts that will aid, I hope, in viewing where we are now, and how we have come to be where we are. For further reading see Cummins (1974), Likens and Bormann (1974), and Vannote and others (1980). Let me add a thought here. In my opinion, the field of aquatic chemistry is in the position where analytical techniques far outstrip our ability to understand what the analyses mean. In aquatic biology, we have, I believe, better concepts of what is taking place than we have data to support the concepts. In some ways, aquatic chemistry and aquatic biology face opposite problems. It will be interesting to see where both sciences are in regard to this dilemma some 20-years hence. Whatever the results, let us hope that hard data replaces dogma. THE PRESENT--WHERE ARE WE? These are exciting and frustrating times in aquatic ecology. We have broken many of the old barriers that for so long dominated our thoughts. The past barriers to our thoughts, however, linger with us in too many instances, and they influence our present-day thinking. This is a part of life, progress, and science. Another problem that always must be faced in viewing science, especially the history of science, is determining where something began and where it ended. I stated earlier that I did not know when aquatic biology began. I do not even know where the present thrusts began, but many were post World War II. In the 1950's, we were confused and wondering if what we were doing then would have long-lasting usefulness, or if it was simply needs-of-the moment. We suspected the latter, but we were not strong enough in our knowledge or convictions to know if we had any reason to be correct. As it turns out, we were half correct and half wrong--a comfortable position even if you do not realize it. For example, the era of the 1950's was the era of the effects of organic waste on streams and stream ecosystems. Strange it would be at that time when we could not directly measure organic carbon. Today, we are able to make rather accurate measurements of organic carbon, but still do not have a clear idea of what the measurements mean. It was the era of the 1950's tied to the era of the 1900-1910 that truly tied together our knowledge of untreated domestic sewage on stream. We had "pinned down" the culprit, the flush toilet. In fact, that was our goal--the federal water pollution control goal- -to insist on secondary and tertiary treatment of domestic sewage. We won that one, because today most municipalities in the United States release a sewage effluent with a low biochemical oxygen demand; BOD, the household word of the 1950's. In the 1950's, we studied and mastered the operation of sewage oxidation ponds for small municipalities. The problem in all of this was biological, the cure in all of this was biological, and the end result in all of this--cleaner streams and enhanced biological production--was obviously biological. It would be foolish to end this phase of the present era with a positive statement that the problem of domestic wastewater is completely solved. It is not; but we can all hold our heads high in that truly significant progress was made in the late 1950's, 1960's, and 1970's. Most domestic sewage-problem areas that remain could be solved easily with todays technology. Problems related to aquatic biology did not end with the solution to the domestic wastewater problem. Other problems soon took their place. For one thing, we realized (again) that there were other sources of organic matter in streams that resulted in a high BOD. These were leaves, forest litter, and, in many parts of the northwest and north-central and southeastern parts of the country, pulp-mill wastes. With the latter we had a color, BOD, and a suspended organic solids problem on our hands, as well as a toxicity problem. I cannot prove it and it would not be worth the effort if I could, but I firmly believe the domestic waste and pulp-mill waste problems directed us into the exciting aquatic biological research that began in the middle 1960's, and is continuing today. This research consists of a mixture of laboratory and field research (nothing new here), a bit of verification between laboratory and field research (much new here), and an appreciation of the progress from other fields of science and how they impinge upon aquatic biology (again much new here). After all, there had been great advances in biochemistry. The Krebs or citric acid cycle was well known and verified, and modern bomb calorimeters were providing methods not only for understanding, but for measuring energy and material utilization. Methods for the measurement of toxicity were more refined; this again was a result of input from other sciences, especially trace-element chemistry. I should quickly add that biology is a synthetic science; that is, it depends heavily upon physics and chemistry for its understanding. Thus, advances in physics and chemistry usually have led to advances in biology. But, the sciences are very often complimentary; for example, the solubility product of cyanide was corrected as a result of biological toxicity tests, rather than chemical determinations. Even those concerned with the production of fish began to realize there was more to measure and understand than length and weight relations. Indeed, fish again became organisms of research concern, because they encompass the highest forms of life in aquatic systems. But fish and the organisms they feed upon have quite different nervous and circulatory systems. Parallel study emphasis was, therefore, placed on aquatic invertebrates. This was a good decision by many scientists, and placed study emphasis on a larger segment of the inhabitants of the aquatic ecosystem. Bacteria still were ignored somewhat, but their role in aquatic ecosystems was gaining attention. Studies of aquatic ecosystems using artificial or laboratory streams gained prominence in the 1960's and into the 1970's as well. Streams were constructed to mimic natural conditions as much as possible, but also to provide controls on flow volume, rate of flow speed, light, temperature, and so forth. Such "stream" studies provided a great amount of insight into the role of algae and periphyton production and distribution in ecosystems. A great deal was learned about plant-animal relations and interactions as well. Studies in animal behavior (effects of crowding, competition for food, and so forth), secondary production, predation, and population dynamics were enhanced by the use of artificial streams. Even so, artificial streams and the activities or events we attempted to measure by their use were quite simple compared to natural ecosystems. We simply do not know how to measure everything. But the impact on our understanding of stream ecosystems through the use of artificial streams has been tremendous and will be with us for decades to come. It would be untrue to leave the implication that modern research in aquatic biology has been only the result of artificial streams. A great deal of other types of research has been carried out as well. Some are concerned with natural systems and others are concerned with physiological studies under laboratory conditions. Most of this research, at least that which has significantly advanced our understanding of aquatic ecosystems, has been tied to the modern concepts of biochemistry and our ability to understand chemical speciation and determine ultra-low concentrations in natural waters. Essentially, this is where we are now. There are a number of excellent well-designed studies underway using natural streams and making measurements under natural conditions. These studies, coupled with past laboratory studies, have increased greatly our knowledge of energy and material needs and utilization by aquatic animals, and nutrient requirements and uptake by aquatic plants. Coupled to these studies is a much better knowledge and understanding of animal toxicity; but, still too little is known or appreciated concerning sub-lethal or stress effects. More on this will be discussed later. Lake studies have taken a quantum jump in recent years in the form of understanding nutrient requirements of algae, algal physiology, and in estimating water budgets. Much of our understanding of natural lake conditions is a result of the Canadian experimental lakes programs, headquartered in Winnipeg, Manitoba. Lake studies by United States scientists also have been imaginative and have provided much insight to lake ecosystems that was not available a decade ago. In spite of our progress in understanding lake ecosystems and nutrient requirements of algae, we have only few options for reversing enrichment. The most feasible way to control enrichment is to prevent it in the first place, an option that has been closed in many lakes. That is probably enough on where we are. Without question, the past 20 or so years has provided some excellent insight and progress in aquatic ecology. Much of the research was tied to principles of physics and chemistry, which has broadened the field of aquatic biology. Moreover, agencies which at one time were concerned only with a single product (fish, for example) have broadened their scope in looking at the ecosystem instead of their product of interest. Thus, much improved studies in fish physiology, toxicology, and behavior have occurred in recent years. The simple recognition that fish are but a part of the ecosystem was, itself, somewhat of a breakthrough in aquatic research. THE FUTURE--WHERE ARE WE GOING? I cannot predict the future any better than anyone else, and there is always the chance I cannot do as well as others. But, I think I have some feeling as to what needs to be done and what can be done with our present understanding of aquatic ecosystems. I am going to discuss each item separately, even though there are pitfalls in using this approach. 1. Energy and material utilization by aquatic animals is an area for future endeavors. This is not a new concept. It was first derived by Ivlev (1945). We can now measure most components of the energy and material equation for animals as: Qc = QW + Qs + Qd + Qa + Qg Where Qc ~ total energy and material consumed QW - total waste Qs ~ basal or standard energy and material utilization Qd ~ energy cost of food transport Qa = energy and material used in activity Qg = energy and material used for growth We know that on the right hand side of the equation, the first four components of energy and material must be satisfied before Qg (growth) can take place. The equation is, of course, incomplete, for it neglects energy and material utilization and losses related to reproduction, a vital component of population well being. Nevertheless, it points out how energy and material must be used to satisfy life processes before growth, a population requirement, can be met. Much more direct research needs to be done on animal energy and material utilization under different environmental conditions. If we are to predict stress, we must base our predictions and findings on quantative values and these must be related to some vital factor needed by the organisms in order to survive. The above equation offers some promise in this direction. 2. The relation between organic matter and aquatic plants and animals will be a continuing and vital aspect of future research. This was touched upon earlier, and has been an area of active research in recent years. We now have a great deal of useful information on the role of benthic invertebrates in reducing coarse organic matter to fine organic matter. We know too that many aquatic invertebrates are quite efficient at removing particulate organic matter and transforming it into living tissue. Aquatic biology is somewhat ahead of organic chemistry in defining sources and sinks of organic matter in aquatic systems. The two sciences should and must come closer together in the future. Organic chemistry and aquatic biology are working on the same ground at the present time, a fact that has never before been true. 3. The toxicity of substances to organisms, because of various man-caused inputs to stream and lake ecosystems, will continue to be an active area of study. Hopefully, however, new approaches will be undertaken to put more emphasis on the sublethal effects of introduced materials. We need to know much more about stress and sublethal concentrations of material; that is, those concentrations and conditions that do not cause death, but stress the components given earlier in the energy and material equation. More also needs to be done on the activity and form that particular constituents take under natural conditions and the relative toxicity these constituents will have while in a particular form or activity. 4. More work on population ecology from the standpoint of processes carried out by populations is needed. We need less emphasis on population taxonomy and more on processes; a sort of population physiological approach. I quickly add that my comments are not anti-taxonomy. Certainly, we must be able to give a name to the organisms we work with. But taxonomy without an understanding of the role of the organism in the aquatic ecosystem is of little value to understanding the processes involved. 5. Modeling of the distribution of organisms also is important. We are, I believe, at the point where we can model particular aspects of the aquatic ecosystem. One such aspect is the distribution and movement of some organisms, especially phytoplankton in lakes. Modeling should not overtake our understanding of processes. But if used carefully, modeling can well point the way towards needed process research. 6. Lake restoration is a research activity that certainly is in need of a much more imaginative approach. A great deal of money and time has been spent reworking old tried-and-failed techniques for lake restoration. I do not have an answer, nor even a good approach for lake restoration success. But, we need to collate under a single cover those techniques that do not work-and get on with the job of looking at those environmental components that can be controlled and hence will control algal production. These then are six areas where I think future aquatic biological research should be directed. Doubtless six more could be added and, in a few years hence, some removed. We have come a long way since Linneaus, and the future is brighter than ever. References Cited Brody, S. B., 1943, Bioenergetics and growth: New York, Hafner Publishing Co., 1023 p. Cummins, K. W., 1974, Structure and function of stream ecosystems: Bioscience, v. 24, p. 631-641. Forbes, S. A., 1925, The lake as a microcasm: Bulletin of Illinois Natural History Survey, p. 537-550. Ivlev, V. S., 1945, The biological productivity of waters (translated from the Russian): Journal Fisheries Research Board of Canada, v. 23, p. 17271729, 1966. Kolkwitz, R., and Marrson, M., 1908, Okologie der pflanzlichen Saprobien: Bericht der Deutchland Botanisch Gesellschaft, v. 26, p. 505-519. Kolwitz, R., and Marrson, M., 1909, Ecology of animal saprobia: International Review of Hydrobiology and Hydrogeography, v. 2, p. 126-152. Likens, G. E., and Bormann, F. H., 1974, Linkages between terrestrial and aquatic ecosystems: Bioscience, v. 24, p. 447-456. Lindeman, R. L., 1942, The trophic-dynamic aspects of ecology: Ecology, v. 23, p. 399-418. Linnaeus. Carlos, 1758, Systema naturae, Regnum animals, 10th edition: Tomus L. Salvii Holinae. Vannote, R. L., Minshall, G W., Cummins, K. W., Sedell, J. R., and Cushing, C. E., 1980, The river continium concept: Canadian Journal of Fisheries and Aquatic Sciences, v. 37, p. 130-137.