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Home , Detritivore, Grandfather clock, Saprophagy

Forests: Fresh Perspectives from Analysis

(Proceedingspf the 40th Annual Biology Colloquium I

Edited by Richard H. Waring

Oregon State University Press Corvallis, Oregon Library of Congress Cataloging in Publication Data Biology Colloquium, 40th, Oregon State University, 1979. Forests, fresh perspectives from ecosystem analysis.

1. Forest ecologyCongresses. I. \Varing, Richard H.II.Title. QH541 .5.F6B561979 574.5'2642 80-11883 iSBN 0-87071-179-2 © 1980 1w the Oregon State University Press Printed in the United States of America All rights reserved Preface

Over the last decade a new perspective sections within this volume. The first on how forest operate has section (chapters 1-3) revises classical emerged. Ecosystems appear much more flex- theories on structure, succession, ible than we once thought. Even the most and ecosystems. The section (chap- persistent is still evolving in composition. ters 4-8) examines in detail how forest Yet for all their diversity, very similar canopies, soil microbes, and root systems processes are seen as operating in all operate as almost independent subsystems. forests, providing a point for comparative The final section (chapters 9-12) focuses studies. A more balanced perspective on the impact of the different materials-- brings a greater appreciation of the in- logs and leaves, soil and sediments, water frequent but dominating events that shape and minerals--that move through forests and the course of ecosystem development. into stream ecosystems. Although each Through joint studies of forests and streams section is distinct in scope, they share a we see new roles for living and dead com- common link of matter and . ponents of both ecosystems. For permitting us the opportunity to For the 40th annual Biology Colloquim share these ideas, we are indebted to the held April 27-28 1979 at Oregon State late Ralph Shay, who originally suggested University, a select group of scientists the topic and helped arrange the colloquim. was invited to share this new perspective To him we dedicate this volume. on forest ecosystems with a wider audience. The colloquium papers are grouped into three Richard H. Waring

V - Contributing Authors

Daniel B. Botkin R. V. O'Neill Department of Biological Studies Environmental Division University of California Oak Ridge National Laboratory Santa Barbara, California Oak Ridge, Tennessee

George C. Carroll Dennis Parkinson Departnent of Biology Department of Biology University of Oregon University of Calgary Eugene, Oregon Calgary, Alberta

Kermit Cromack, Jr. D. E. Reichle Department of Forest Environmental Sciences Laboratory Oregon State University Oak Ridge National Laboratory Corvallis, Oregon Oak Ridge, Tennessee

Kenneth W. Cummins Dan Santantonio Department of Fisheries and Wildlife School of Forestry Oregon State University Oregon State University Corvallis, Oregon Corvallis, Oregon

Jerry F. Franklin Wayne T. Swank U. S. Forest Service Coweeta Hydrologic Laboratory Forest Science Laboratory U. S. Forest Service Corvallis, Oregon Franklin, North Carolina

W. F. Harris Fredrick J. Swanson Environmental Sciences Division Pacific Northwest Forest and Range Oak Ridge National Laboratory Experiment Station Oak Ridge, Tennessee Forestry Sciences Laboratory Corvallis, Oregon James A. MacMahon Department of Biology and Center Frank J. Triska Utah State University U.S. Geological Survey Logan, Utah Menlo Park, California

D. McGinty Jack B. Waide Department of Biology Environmental Sciences Division Huntingdon College Oak Ridge National Laboratory Montgomery, Alabama Oak Ridge, Tennessee

Richard H. Waring Department of Forest Science Oregon State University Corvallis, Oregon

vii Contents

Section I: Ecosystem Theory

A Grandfather down the Staircase: Stability and in Natural Bcosystems ...... Daniel B. Botkin

Dimensions of Ecosystem Theory ...... 11 R. V. O'Neill and D. E. Reichie

Ecosystems over Time: Succession and Other Types of Change ...... 27 James A. MacMahon

Section II: Terrestrial Ecosystems

Distinctive Features of the Northwestern Coniferous Forest: Development, Structure, and Function ...... 59 Jerry F. Franklin and Richard H. Waring

Forest Canopies: Complex and Independent Subsystems ...... 87 George C. Carroll

Aspects of the of Forest Ecosystems ...... 109 Dennis Parkinson

The Dynamic Belowground Ecosystem ...... 119 W. F. Harris, Dan Santantonio, and D. Mccinty

Vital Signs of Forest Ecosystems ...... 131 R. H. Waring

Section III: Watershed and Stream Ecosystems

Interpretation of Cycling Research in a Management Context: Evaluating Potential Effects of Alternative Management Strategies on SiteProductivity ...... 137 Wayne T. Swank and Jack B. Waide

Geomorphology and Ecosystems ...... 159 Frederick J. Swanson

The Role of Wood Debris in Forests and Streams ...... 171 Frank J. Triska and Kermit Cromack, Jr.

The Multiple Linkages of Forests to Streams ...... 191 Kenneth W. Cummins

ix A Grandfather Clock down the Staircase: Stability and Disturbance in Natural Ecosystems

Daniel B. Botkin

BASIC CONCEPTS book, Man and Nature, that "nature, left un- disturbed so fashions her territory as to In a small village in New Hampshire, an give it almost unchanging permanence of elderly lady in an old red brick house form, outline, and proportion, except when crammed with antiques that her parents shattered, by geologic convulsions; and in bought at the turn of the century. At the these comparatively rare cases of derange- top of the staircase stands a wonderful ment, she sets herself at once to repair the grandfather clock, whose had swung superficial damage, to restore as nearly as rhythmically to and fro for many practicable, the former aspect of her Several ago two grandchildren dis- dominion." We tend also to agree with covered the clock and, in the process of in- Marsh that an undisturbed wilderness forest, vestigating it with all the empirical skills the kind that he referred to as occurring in known to small children, managed to edge it "new countries," meaning those not yet sub- over to the staircase. With a push, they ject to civilization's heavy hand, is watched it tumble down the stairs with a characterized by a single, permanent equili- marvelous series of noises.With consider- brium condition the climax forest of able effort, friends and neighbos eventually twentieth century ecology. In Wildernesses, returned the clock to its former position, Marsh wrote, "the natural inclination of the but the disruption had been too great for its ground, the self-formed slopes and levels, internal mechanisms and it has stood silent are graded and lowered or elevated by frost since, outwardly intact, a sad image of and chemical forces and gravitation and the mechanical frailty. flow of water and vegetable deposit and the Nature's biota sometimes seem like that action of the winds until, by a general clock -- able to withstand small disturbances compensation of conflicting forces, a condi- but unable to survive major perturbations. tion of equilibrium has been reached which, In ecological systems, perturbation and without the action of man, would remain, stability seem to oppose one another. In with little fluctuations, for countless both scientific literature and in popular ages" (Marsh, 1864). discussions of the effects of civilization On the other hand, we also seem to on the environment, stability is referred agree with Lucretius, who in the first to as resisting disturbance and perturbation century B.C. wrote in De Rerum Natura that as a disruption of the stability of nature. all things are subject to mutability and We call an undisturbed forest stable and a change; that "time does change the nature of highly perturbed one unstable. the whole wide world; one state follows from Are ecosystems, in these terms, stable another; not one thing is like itself for-- or unstable? Is perturbation common and, ever, all things move, all things are in some sense, natural, necessary, or nature's wanderers, whom she gives no rest, desirable? Or is perturbation always the ebb follows flow." Lucretius used the ero- product of human interference in nature, and sion along riverbanks in forests as an bad something to be avoided in our example of the mutability of nature. Here management of natural ecosystems? the forests, Lucretius said so long ago, In regard to these questions, we seem are "shorn, gnawed by the current" to believe simultaneously in contradictory (Hunphries, 1968). views. On the one hand, we tend to agree We acknowledge, as did Lucretius, that with George Perkins Marsh, who wrote more nature is subject to change, that forests than one hundred years ago in his classic change: trees have mast years when, for H 2 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS reasons we do not now understand, a single (idealized) pendulum, which will oscillate species will produce an of seeds indefinitely with a constant frequency and ovor a large geographic area. amplitude; that of a dampened (idealized) Well, which is it? Is the truth as pendulum, which will oscillate with a con- Marsh saw it? Does Mother Nature set her- tinually decreasing amplitude around its self at once to repair superficial damage central point but never come to complete and restore the former aspects of her rest; and that of a real pendulum with dominion, creating an equilibrium that re- friction, which will oscillate for a while mains for countless ages? Or is the truth but eventually stop at its original rest with Lucretius, that the earth is both point. "our mother" and "our common grave," and This concept of stability underlies the that all things, even undisturbed forest classical twentieth century ideas of forest wildernesses, are always changing? succession. According to this classical These two ideas can be brought concept, an undisturbed forest is unchanging together they only appear to be contra- and a disturbed forest "recovers" to its dictory. The contradiction occurs because prior condition. The forest proceeds of the restricted way that we define through a well-defined series of stages and stability a definition we have used eventually reaches a fixed single state, the during the last 200 years. In this paper, climax, which is that permanent condition I will attempt to show that perturbation referred to by Marsh. and stability are linked together in truly Early twentieth century ecologists like natural ecosystem processes. What appears William S. Cooper believed in this idea of to be contradictory can be shown not to be, forest stability. In the first decade of but this requires a basic change in our this century, Cooper made a classic study conception of natural ecosystems as well as of forest succession on Isle Royale in Lake changes in our concept of stability. These Superior. He saw that island, little dis- basic changes may seem quite disturbing at turbed by Indian or European culture, as an first, hut as we pursue the topic they will excellent place to learn about the real seem quite natural. characteristics of forest ecosystems. After This discussion is not merely academic: a careful study of the forests of Isle it is crucial to our management of our Royale, Cooper concluded that: one forest natural biological resources. Our attitudes type, the boreal forest, was the island's toward stability and perturbation have in- natural condition. This forest, he wrote, fluenced our methods of managing our bio- is the "final and permanent vegetation logical surroundings, sometimes to their, stage, toward the establishment Of which all 'and to our, detriment. I will concentrate other societies are successive steps." on forest ecosystems, because forests arc He believed that regardless of the condition composed of long-lived organisms and should of the starting point he it hare rocky be more likely to demonstrate long- surrenit or open water bog, the final condi- constancy than most other ecosystems. How- tion, given enough time, would be the same ever, I believe the points that I make will single state. "Both observational and ex- be general. perimental studies have shown," Cooper In the twentieth century, the favorite wrote, "that the balsam-birch-white spruce metaphor among naturalists for the stability forest, in spite of appearances to the of a forest, or any ecosystem, is the contrary, is, taken as a whole, in equili- stability of a pendulum. This is the brium; that no changes of a successional stability of a strictly mechanical system, nature are taking place within it" (Cooper, a stability that I have referred to else- 1913) whore as "static stability" (Botkin and Accepting this idea of stability, we Sobel, 1975). In the 1920's Alfred Lotka tend to think of a Derturbation as destabi- stated this metaphor in his Elements of lizing a forest in two senses: first of all, Mathematical Biology (Lotka, 1956). The a mild perturbation removes the system Australian ecologist Graerne Caughley used (pendulum or forest) from its equilibrium the metaphor in a recent review on the point. Strictly speaking, this is not a effects on ecosystems of the introduction change in the stability of the system, of ungulates into new (Caughley, merely a change in the system's current 1970). According to this view, a stable state, hut we often confuse equilibrium system has two attributes: an equilibrium state with stability. Second, a large state, and the ability to return to this perturbation, as when the two small children equilibrium state following a disturbance. knocked a grandfather clock down the stair- Thus a pendulum, when "disturbed" with a case, throws the system far enough from the push, will oscillate. Theoretically, a equilibrium that a return to that original pendulum can -demonstrate three possible equilibrium is no longer possible. Even kinds of stability: that of a frictionless today, the idea still predominates that eco- D. B. BOTKIN 3

systems in general and forests in particular a forest or other natural ecosystem, we are characterized by this static stability. must be able to identify the equilibrium In the last decade, ecologists have state. Before the theory of continental divided static stability into different glaciation was well established, which was stages and found it useful to refer to these before our century, it was possible to different stages and their different believe with George Perkins Marsh that the attributes. For example, C.S. Holling, equilibrium condition of a forest could per- using this concept of stability, described sist for "countless ages." But by the the resistance and resilience of an eco- beginning of the twentieth century, it was system (Holling, 1974). The resistance is well recognized that severe changes in like mechanical inertia the ability of climate had occurred during the last two the pendulum to resist the forces that tend million years. Earlier in the century, it to cause it to leave its equilibrium. The was believed that there had been four major resilience is, loosely speaking, the periods of glaciation, that the changes rapidity and ease with which the system accompanying these periods had been most returns to its original equilibrium state. marked at high latitudes, with little or no Although these are new terms, they refer to effect at low latitudes, and that the and accept the static concept of eco- climate during the glaciations represented system stability. This static stability is relatively short, anomalous climatic readily defined mathematically, as has been episodes. done in physics for a long time, and can be Once the theory of continental glacia- found in many recent ecology texts and tion was accepted, it was clear that, at articles (May 1973; Jordan et al., 1972; least in temperate zones, the climate had Krebs, 1972). changed markedly over periods of thousands If this static definition of stability of years and these long-term climatic for ecosystems is correct, then the natural changes were accompanied by changes in the condition of am ecosystem like a forest kind of ecosystem at a particular location. must be one of "rest" a static equili- Earlier in this century, ecologists brium point. Furthermore, a forest that is attempted to resolve the problem of eco- changing is therefore not in its natural system stability and long-term climate state, and a manager whose job is to main- changes by talking about a climatic climax tain a forest in its natural condition would for an ecosystem a single state or con- seek to restore the forest to its equili- dition that would persist without change as briuin as quickly as possible. He would also long as the climate did not This attempt to remove the possibility of sub- constancy is usually described in terms of sequent perturbations in the . the species composition, the relative or Evaluation of the stability of a system absolute abundance of species, and the total must involve a definition of stability and a amount of organic matter in the ecosystem. variable of interest, whose stability is Throughout most of our century, it has measured according to the accepted defini- been generally believed that enough time has tion. In a simple system like a pendulum, elapsed since the end of the last glaciation the measure of interest is obvious. In an to allow most natural ecosystems to obtain ecosystem, however, the appropriate measure an equilibrium, and that the presettlement is not obvious. We tend to think that landscape in North America represented an nature will provide us with the appropriate equilibrium state of the vegetation com- measure, but ecological studies of stability munities. During the two decades our use a variety of measures including species knowledge of the of the Pleistocene composition, relative abundance of species, climate and ecosystems has increased greatly. total organic matter, and the rate of flux Forest history is particularly well known or the stored amount of specific chemical for the Northeastern forests of North elements. America, those that extend from Maine to To summarize, a system characterized Minnesota and from Ontario to the southern by static stability has a single equilibrium Appalachians in Georgia. What does the state and will return to that state along a evidence from such areas tell us about the well-defined pathway following disturbance. equilibrium conditions of a natural forest? Also, it has generally been argued that Consider a forest in Minnesota and a perturbation is'bad" and an equilibrium is manager whose job is to restore that forest "natural to its equilibrium condition. What vegeta- tion assemblage would he choose? The obvious answer appears to be to choose a A FOREST DOES NOT HAVE A forest similar to the natural, original pre- SINGLE EQUILIBRIUM STATE settlement vegetation of that area. Recent studies indicate that the In order to apply static stability to forests of this area have undergone major 4 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS changes in species composition since the ISO 140 00 60 40 last glaciation. For example, a study in Minnesota indicated that the last glaciation was followed by a tundra period, then by a spruce forest that was replaced about 9,200 years ago by a forest of jack and red . About 8,300 years ago paper birch and alder migrated into this forest, and about 7,000 years ago white pine entered. Afterward there was a return to spruce and jack pine. These changes reflected fluctuations in climate, periods of cooling and warming, and the differential migration of the species as they returned north following the melting of the continental ice sheet. The study indicates that, on a time scale of 1,000 years, major changes have taken place in the species composition of the forests (Craig, 1972; Swann, 1972). Which of these forests represents the natural state? If one's goal were to return northern Minnesota to its "uatural" condi- IJ Tundra and pork tundra tion, which of these forests would one E Boreol Coniferous forest choose? Each appears equally natural in the Boreal coniferous forest (montone) Hemlock- northern hardwood forest sense that each dominated the landscape for Temperate mixedforest a rather long period, approximately 1,000 BEJ Temperate mixed forest (montone) years, and each occupied a landscape at a E Proine, Steppe, and Savanna time when the influence of human beings was Dry Steppe nonexistent or slight. The range of choice Desert shrub: and grasses is great, representing kinds of vegetation Subtropical Scrub Tropical communities now distributed thousands of miles apart. Figure 1. Natural vegetation zones in North The desire to return a particular spot America today, much generalized (from in Minnesota to its natural state leaves us Flint, 1971) in a quandary, because as the glaciers receded and the climate changed, the vegeta- each forest type. For example, in Flint's tion communities also changed. Thus we do standard work on the Pleistocene not find constancy in the abundances of (Flint, 1971), the vegetation communities forest tree species over time at a partic- are pictured as having been pushed south, ular location, at least in mid-latitudes of but still intact (Figs. 1 and 2). Figure 1 North America. shows the modern distribution of vegetation A thousand years seems to be a long zones and Figure 2 shows the distribution time. One might argue that changes in that was assumed to have occurred during forest composition are slow and that an the ice . In Figure 2 we see a tundra equilibrium state might be obtained in border just below the edge of the ice, periods of less than 1,000 years. However, spruce forests south of the tundra, and one would expect that the effects of a temperate mixed species forests to the marked change in climate would influence an south of the spruce. If this were true, one ecosystem for at least a few generations. could then argue that the communities have Because the lifetimes of some of the tree had a comtinuous existence throughout the species in northern hardwood and coniferous Pleistocene, merely migrating back and forests are on the order of 400 years, an forth along the landscape in response to equilibrium state would not have had time the climate. Then the natural condition of to develop in northern Minnesota. What a particular locale would be the entire alternatives are left to us? biological community that was characteristic Throughout the first half of the of the existing climate and had followed twentieth century, it was generally believed that climate across the landscape in ages that glaciers caused a great displacement in The natural forest would be the one the location of vegetation communities, but past. that existed under a particular climate these communities remained intact and merely prior to the influence of human beings. migrated north and south with changes in the Under this interpretation, each community climate. The location of a community and has retained its integrity and has a climate- its migration across the landscape were determined equilibrium state. Its structure, believed to have the same relative abun- in terms of the relative abundance of its dances of species as are observed today in D.B. BOTKIN 5

constituent species, has remained constant. different directions, as illustrated in th Recent evidence suggests that this accompanying maps (Fig. 3). Hickory moved idea is false. Studies of pollen deposits toward the northeast from some refuge in from 26 sites scattered across the eastern the southern midwest or west, while chestnut and central United States allow us to piece moved eastward from a refuge east of the together the paths of migration of the major Carolinas, an area that now is covered by tree species as they returned north during the ocean but would have been dryland during the last 13,000 years as the North American the glaciation. In recent , just prior continental ice sheet melted (Davis, 1976). to the chestnut blight of the early The trees migrated at different rates, de- twentieth century, hickory and chestnut were pending on the size and mobility of their two of the major trees of the forests of the seeds. Light seeds, like those of poplar, mid-Atlantic states, and botanists classi- are readilyblown long distances by the fied the forests of this region as chestnut- wind, and these moved northward most oak-hickory, believing that, without dis- rapidly. Heavy seeds, like those of beech, turbance, these species would dominate the are moved by squirrels and other small mam- landscape indefinitely. mals, and these migrated much more slowly. According to their interpretation, this Not only did the different species move oak-chestnut-hickory forest would have re- northward at different rates, but the mained intact during the maximum extension species appear to have moved northward from of the continental glaciers, merely occupy- ing an area south of its location.

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Figure 2. Sketch map suggesting possible pattern of vegetation in eastern andcentral United States at the Late-Wisconsin glacial maximum. Although controlled at a few localities, the sketch is very speculative (from Flint, 1971). 6 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Migration of hickory. Migration of chestnut.

Figure 3. Migration of hickory and chestnut interpreted from pollen records (from Davis, 1976) following the last glaciation. Each line represents in thousands of years the first occurrence of the species. Figures show the direction and temporal sequence of migration.

Migration of hemlock. Migration of beech.

Figure 4. Migration of hemlock and beech interpreted from pollen records (from Davis, 1976) following the last glaciation. Each line represents in thousands of years the first occurrence of the species. Figures show the direction and temporal sequence of migration. D. B. BOTKIN 7

But Davis's study indicates that the forest A FOREST IS NOT CHARACTERIZED BY composition itself changed markedly. The A SINGLE DETERMINISTIC PATTERN pecies thot are most important in the OF RECOVERY :dern forest scattered in different directions, forming forest communities that When a pendulum is given a push and no longer exist. displaced from its equilibrium, it follows But there is still another possibility a strictly determined pathway hackand that would allow us to believe in the forth until, if it is subject to friction, existence of a single equilibrium state in it eventually stops at its original rest a forest. One could argue that, although point. The position and velocity of the the individual species separated for a part pendulum can be calculated precisely if the of the glacial period, they returned rapidly position, velocity, and frictional and gra- enough to the present location to form an vitational forces are known at any one time. interglacial forest that would be constant Can forests be characterized by similarly throughout its entire range for most of the exact patterns? interglacial period. However, the maps of Even if we admit that over a long time tree migration routes indicate markedly forests change in composition, does this different rates of return (Fig. 4). Hemlock mean that we must also abandon the idea of reached Massachusetts 9,000 years ago, static stability for a short time period? approximately 2,000 years before beech, Suppose we consider a time period short although now beech and hemlock are assumed enough so that the species that make up a to occur in similar climates, with the forest, including all of the forest's beech occurring on slightly warmer, better successional stages, do not change. It was drained soils and the hemlock in cooler, frequently argued earlier in this century moister valleys, streamsides, and ridges. that a particular forest type, that is a Beech is also found in much of the pre- particular assemblage of forest tree sent range of hemlock, but the process has species, would follow a strictly determined not yet reached an equilibrium. Hemlock one-way pattern of recovery following a dis- reached the upper peninsula of Michigan turbance. Clearly this is not true at very 5,000 years ago and moved westward slowly, small spatial and temporal scales. Whether reaching the western shores of Lake Superior a seed germinates and survives, whether a 1,000 years ago. Beech, on the other hand, tree grows well or poorly, whether it dies is still westward, with its pre- in any one year, depend in part on chance sent western boundary in the middle of events. The success of any one tree or Michigan's upper peninsula. population in a small area can be predicted We need not abandon the possibility only in terms of probabilities. What of that an equilibrium forest condition will be large temporal and spatial scales? reached during the present interglacial, and we could argue that such an equilibrium forest would be the true natural state of A Lesson From Bogs nature of this region. It might he that we are still seeing a recover" and, if the In his study of forest succession at interglacials are truly very long in com- Isle Royale, William S. Cooper argued that parison to the period of continental glacia- there was a single climatic climax that tion, a true equilibrium of the distribution would be reached, given enough time under a of the forest trees may yet be reached. constant climate, regardless of the starting However, studies of the migration rates point. He believed that both a bare rocky of trees during the present interglacial and ridgetop and the open water of a bog would during previous ones show that such a proceed, through different but equally floristic equilibrium is never reached at specific successional patterns, to the same the mid and high latitudes. Furthermore, final equilibrium forest. Moreover, he and according to Davis, "In this sense, the others argued that the pattern of succession interglacials are unstable interruptions in from each of these starting points was Pleistocene history'T (Davis, 1976). Soils exact: like a pendulum returning from dis- also show continuous development throughout turbance, one stage inevitably followed interglacial periods, indicating that inter- another. glacials are too short for attainment of a A recent study of one of these kinds of soil equilibrium and therefore of an eco- succession -- that of freshwater bogs system equilibrium. suggests that this is not true. The classi- cal successional pattern would be develop- ment from dominant green , phytoplank- ton, and submerged macrophytes on open water to a stage of floating leaved macrophytes, to a reedswamp, to fensand various 8 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS fen stages, and finally to dryland. Walker spite of this conclusion about natural for- (1970) recently analyzed the available pub- est ecosystems, a manager could still argue lished pollen records concerning changes in that it is always desi rable and puss ible to bogs in Britain. From these he identified maintain a forest in a fixed condition, and twelve different stages in hog development. to remove or suppress perturbations. This He made a transition table, listing each was the belief regarding forest fires stage and the percentage of times that one earlier in this century. stage led to each of the others. Although In the nineteenth and early twentieth one pattern that Walker called the 'central centuries, severe fires followed intensive tendency' predominated, a variety of patterns logging in eastern and central areas of the actually occurred. In 17 percent of the United States. For example, in Michigan, cases the transitions were reversed; that is, where 19 million acres of white pine were the succession went in the direction oppo- cut, the great amount of slash left on the site to what was assumed to be natural. ground and the careless treatment of logged- This study of bogs is particularly over areas led to extremely devastating important because, as Walker concluded, "in fires. These left the landscape in a condi- a system which has often been considered one tion from which recovery to a mature forest of the most unvarying in plant ecology, the would take a long time, if it were to occur variety of courses actually taken is re- at all. As a consequence of these devasta- markable." The evidence demands, he con- ting fires, many concluded that the proper cluded, that "predictions be made only in policy for forest management was to prevent terms of probabilities." fires in all cases. Of course, one could argue that the We know now that such a policy of fire lack of predictability is due merely to the suppression can lead to quite undesirable uncertainty of our understanding of the results in some cases. One of the most causal mechanisms, and we would be able to famous cases is the attempt to prevent fires make exact predictions if we studied enough. in the jack pine forests of central Michigan. This is a belief that nature Is actually Jack pine (Pinus banks iana), as every good deterministic, and only the limits of our naturalist of the east knows, is a fire- observational techniques prevent us from successional species. It has serotinous learning the exact processes. cones that open after a fire; it reproduces However, Walker also found that the well after burning, grows rapidly, lives a transitions from one bog state to another short time, and cannot compete with those depended in part on the level of the water species which tend to appear in a forest table, and since this in turn depends on after several decades. Jack pine is, in rainfall, which is a stochastic phenomenon, this sense, an early successional species. there is some inherent, underlying unpre- If fire is prevented, jack pine decreases in dictability or risk about this successional abundance and eventually disappears. process. Thus bog succession is stochastic, In central Michigan, jack pine was the not deterministic, in its inherent nature. home and of Kirtland's warbler Other recent studies suggest that (Dendrolca kirtlandi), and this species was forest succession is a stochastic proess. threatened with extinction because of the In some recent studies researchers ha' elimination of ck pine by fire suppression. attempted to investigate what kinds o Only the activit of a few conservationists stochastic processes best characterize Jiese led to the maintenance of jack pine stands patterns (Horn, 1976). A model based by allowing change to occur and to the of individual species persistence of Kirtland's warbler. Here is can, if stochastic events are included, pro- a case where change was required to allow vide realistic projections of the cent l the continuation uf what was desirable. tendency and the variation around this Change and stability, at least in terms of central tendency (Botkin et al., l973) the preservation or the persistence of The graph of the central tendency Kirtland's warblers and jack pine forests, be mistaken for the path of a determini were linked. system following static stability. To ae such a mistake would cause a forest manager difficulty. Disturbances are Required for Some Desired Forest Conditions

CHANGE IS NOT ALWAYS UNDESIRABLE The preservation of warbler required that jack pine forests in Michigan Forests are not characterized by e J be allowed to burn. Other evidence indi- attribute of static stability: a single cates that change may be necessary to equilibrium or a single, deterministic achieve certain desirable states for some pattern of recovery from perturbatione I. forests. For example, Heinselman (1973) D. B. BOTKIN 9 studied the history of fires in the Boundary It is tempting, therefore, to continue Waters Canoe Area in Minnesota, an area to use the idea of static stability, argu- hore presettlement landscape was character- ing that although it may not be quite right, However, ized by jack pine and red pine forests. His it is a good enough approximation. work indicates that the intentional suppres- we have seen that an insistence on main- sion of fire can produce two trends, both taining a forest in a single state can lead Then what can undesirable. In the first, "dry matter to undesirable consequences. accumulations, spruce budworm outbreaks, we do? blowdowns and other interactions related to We must first recognize that underlying the time since fire increases the probability our concern with the stability offorests that old stand will burn." The probability and all ecosystems is a concern with the of a fire increases with the amount of time probabilities that they will persist on the since the last fire. Furthermore, because landscape, and with a concern about the fuel accumulates on the forest floor, the impact of natural and human influences on severity of a fire increases with the such probabilities. Reconsider a forest of amount of time since the last fire (at jack pine. To persist it must change, but least in terms of the area burned). Second, the changes must be bounded. If the abun- the successful prevention of a fire leads to dance of mature jack pine becomes too low, a change in the forest composition: in the then the forest may not recover following Boundary Waters Canoe Area, jack and red a fire (that is, it may not be maintained pine decrease and are replaced by cedar. as a jack pine forest). If the abundance Thus, the intentional suppression of fire of jack pine becomes too great, the did not lead to a maintenance of what was accumulated fuel in dead limbs on live found in the presettlement forests. In trees and dead organic matter on the forest these forests, fire can be seen as an surface may lead to a fire so severe that intrinsic part of the system; change must recovery would be extremely slow. be viewed as part of this system. This suggests two concepts. One is that Other evidence suggests that short-term of a manager who allows the forest to vary so perturbations are crucial factors in main- that particular states come and go and recur; taining ecosystems in what are thought to be and the second is that the recurrence of their natural state. For example, the desirable states depends on the total amount Serengeti Plains in Tanzania are often cited of variation (the total number of possible as the last true wilderness of the big game states), and this total amount of variation : wilderness in the sense of a lack must be bounded. This suggests the concepts of human influence and a lack of disturbance. of ecosystem Rersistence within bounds and However, Talbot (pers. comm.), one of the the recurrence of specific ecosystem states most knowledgeable wildlife scientists about (Botkin and Sobel, 1975). the Serengeti, has investigated the history A manager's actions can affect the of fires there. He believes that the great range of variation (the number of possible majority of fires are caused by people and states), the rate of recurrence of particular that the fires are important in the main- states, and the average time that the eco- tenance of the great abundince of large system is in any of the possible states. A mammals. manager can compare different policies on These are a few of many examples that the basis of these concepts. He can compare suggest to us that change may be necessary the effects of different policies on the to create the desirable conditions in many bounds within which the forest persists, the ecosystems. Then what can be meant by average time spent in desirable states, and ecosystem stability? the time between the recurrence of desired states. With jack pine forests, he would find ALTERNATIVE CONCEPTS OF STABILITY that a policy of removing all fires would decrease the rate of recurrence of desirable If a forest does not have a single states in comparison to a policy that pro- stable equilibrium and does not recover moted relatively frequent and light fires. from disturbance along a deterministic The cases discussed in this paper con- pattern of successional stages, what is cern abundance and species composition of meaningful to say about stability? How can forest ecosystems. Similar arguments can we compare the relative stability of differ- be made for ecosystem processes, such as ent forests, or of the same forest type mineral cycling. Similar evidence about the under different management policies? With- linkage between change and stability, per- out static stability we are left in an un- sistence within bounds, and recurrence of comfortable position as managers or specific states can be applied to other eco- scientists. Nature no longer tells us when systems. Such a review obviously would a forest is stable or in a desirable state. require a much longer discussion. 10 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

CONCLUSIONS Craig, A. J. 1972. Pollen influx to laminated sediment: a pollen diagram Throughout the history of ecology, In- from northeastern Minnesota. Ecology cluding the most recent decades, ecologists 53:46-57. have tended to believe that the stability of natural ecosystems was metaphorically Davis, M. B. 1976. Pleistocene biography like the stability of a simple mechanical of temperate deciduous forests. Geo- system. This metaphor has been used in a science and Man 13:13-26. mathematically formal way in a great many discussions of ecosystem theory and manage- Flint, R. F. 1971. GlacIal and Quaternary ment. In this paper I have attempted to Geology. New York: John Wiley and show that this metaphor is incorrect and can Sons, Inc. lead to undesirable management policies. Clearly, if this view of stability is wrong Heinselman, M. L. 1973. Fire in the virgin in practice, it must be wrong for ecosystem forests of the Boundary Waters Canoe theory. An ecosystem, like a jack pine Area, Minnesota. J. Quat. Res. 3:329- forest, is more likely to persist on the 382. landscape with certain rates of disturbance Holling, C.S. 1974. Resilience and stabil- than with others, and it will disappear ity of ecological systems, In Annual altogether without perturbation. The Review of Ecology and Systematics, persistence of biota on the landscape is a Vol. 4, edited by R. F. Johnston, P. W. central concern of discussions of stability Frank, and C. W. Michener. Palo Alto, in ecology and is clearly central to many Calif.: Annual Reviews, Inc. ecological investigations. I have attempted to show that we must Horn, H. S. 1976. Succession, in Theoreti- abandon the concept of static stability in cal Ecology, edited by R. S. May, both theory and management of natural eco- pp. 187-204. : Blackwell. systems. There may be a variety of alter- native concepts, but I have suggested that Humphries, R. 1968. Translation of Do we replace the concept of static or mechan- Rerum Natura, by C. T. Lucretius. ical stability with two others: (1) the Bloomington: Indiana University Press. persistence of an ecosystem within bounds and (2) the recurrence of specific eco- Jordan, C. F., J. R. Kline, and 0. S. system states. With these concepts we can Sasscer. 1972. Relative stability of focus on our real concern: the probability mineral cycles in forest ecosystems, that ecosystems will persist on the earth's Amer. Natur. 106:237-253. surface. By recognizing the real nature of our concerns, we recognize that change and Krebs, C. J. 1972. Ecology. New York: stability are linked together, and that the Harper and Row. ideas of Lucretius and George Perkins Marsh can be brought together in a certain way. Lotka, A. J. 1956. Elements of Mathe- matical Biology, reprint. New York: Dover Publ., Inc. LITERATURE CITED May, R. M. 1973. Stability and Complexity Botkin, D. B., and M. J. Sobel. 1975. in Model Ecosystems. Princeton, N.J.: Stability in time-varying ecosystems, Princeton University Press. Amer. Nat. 109:625-646. Marsh, C. P. 1864. Man and Nature, reprint, Botkin, D. B., J. F. Janak, and J. R. Wallis, edited by D. Lowenthal, 1967. 1973. Some ecological consequences of Cambridge, Mass.: Belknap Press. a computer model of forest growth. J. Ecol. 60:849-872. Swain, A. M. 1972. A fire history of the Boundary Waters Canoe Area as recorded Caughley, G. 1970. Eruptions of ungulate in "Lake Sediment Naturalist." J. populations, with emphasis on Himalayan Natur. Hist. Soc. (Minnesota) 23:24-31. Thor in New Zealand. Ecology 51:53-72. Walker, D. 1970. Direction and rate in Cooper, W. S. 1913. The climax forest of some British postglacial hydrospheres. Isle Royale, Lake Superior, and its In Studies in the Vegetational Histor, development. Bot. Gaz. 55:1-44, 115- of the British Isles, edited by D. 140, 189-234. Walker and R. C. West. Cambridge: Cambridge University Press. Dimensions of Ecosystem Theoryl

R. V. O'Neill and D. E. Reichic

INTRODUCTION environmental constraints--and how eco- systems evolved homeostatic, self-regulatory The study of ecosystems, forests in mechanisms to optimize use and exchange of particular, had its origin with early natu- resources. ralists who classified the occurrence and Large, empirical data sets on mineral distribution of a wide variety of ecosystems cycles and energy flow did not appear until (Kerner, 1863; Schimper, 1903). At the turn the advent of the International Biological of the century, ecologists perceived the Program. For the first time it was possible dynamic nature of ecosystems--growth, re- to compare quantitatively different establishment, succession, and persistence strategies of ecosystem metabolism (Reichie were themes that provided a qualitative et al., 1973a; Wetzel and Rich, 1973; Odum framework for research (Cowles, 1901; and Jordan, 1970; Woodwell and Botkin, Clemens, 1904). In the late 1950's the use 1970; Reichle and Auerbach, 1972). The of radiotracers initiated analyses of the first comparative analyses of forest meta- fluxes of materials among functional com- bolism over a wide geographic scale appeared partments of ecosystems. In recent years in 1975 (Reichle, 1975; Reichle et al., systems analysis has begun to synthesize l975a) disparate principles of growth, persistence, This paper reviews and extends our and metabolism into a holistic theory of earlier attempts at ecosystem theory (O'Neill ecosystem function. et al., 1975; Reichle et al., l975c; O'Neill, Recognition of the functional, energetic l976a). We will (1) define the dimensions basis of ecosystem organization is commonly of a theoretic construct of ecosystems, credited to Lindernan (1942), who developed (2) propose some elements of an ecosystem the concept of the trophic-dynamic structure theory, and (3) where possible, compare the of ecosystems (Cook, 1977). This approach predictions of this theory with ecosystem quickly led to a new theoretic basis for data. examining the structure and interconnective- ness of aquatic and terrestrial ecosystems (Juday, 1940; Elton, 1946). The trophic AN APPROACH TO ECOSYSTEM THEORY approach to an understanding of ecosystem dynamics soon associated the flows of A theory is a logical construct within materials between components of the system which a class of phenomena can be predicted with overall ecosystem metabolism (Odum and and explained. By use of theory, available Odum, 1955; Odum, 1957; Smalley, 1960; Teal, data are synthesized and new research is 1962; Macfadyen, 1964). These studies focused with minimal predispositions and resulted in an understanding of the quanti- assumptions. Indeed, the ratio of experi- tative, functional relationships between ments explained plus new experiments producers, consumers, and in stimulated to assumptions determines the ecosystems. Unresolved were the inter- appeal of a theory. The dimensions of a dependencies of mineral poois, , and theory are defined by the phenomena it seeks

1Research supported jointly by the National Science Foundation'sEcosystem Studies Pro- gram under Interagency Agreement No. DEB 77-25781 and the Office ofHealth and Environmental Research, U.S. Department of Energy, under contract W-7405-eng-26with Union Carbide Corpora- tion. Environmental Sciences Division. Publication No. 1355, ORNL. 12 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS to explain. In the present case, we focus the term "stability" (Botkin and Sobel, on the observation that ecosystems persist, 1975), it is necessary to clarify our use i.e., in the face of environmental pertur- here. bations, the system maintains its functional It is seldom appreciated that the con- integrity. To understand what we mean by cept of stability depends upon definition of ecosystem theory, the terms "ecosystem" and the system of interest. A system is stable "persistence" must first be clarified. if it remains within some bounded "state" or returns toward some reference (e.g., equilibrium) "state" following perturbation. The Ecosystem Concept The concept of stability strongly depends upon the definition of this state. If the The ecosystem is a functional unit. It system's reference state is defined speci- is important to clarify this concept, fically (e.g., species composition + rela- because the term is used in other contexts tive numbers of each species + spatial in ecology (O'Neill, 1976b). For example, arrangement of species), then every eco- the monarch avoids the toxic system is inherently unstable and every effects of secondary plant substances by perturbation causes irrevocable changes. If concentrating them in body tissues. In addi- the reference state is defined in terms of tion to avoiding toxic effects, this mechan- total biomass, then the ecosystem may show ism renders the butterfly unpalatable to bounded behavior and be considered highly predators (Price, 1975). The physiological stable. Thus, an ecosystem may be either mechanism is inexplicable if the population stable or unstable, depending solely upon is viewed in isolation from its food supply, the definition of its reference state- its competitors, and its predators. An Different definitions of ecosystem explanation requires reference to the "eco- state are influenced by intrinsic values and system" in which the population occurs, but can lead to dilemmas in management of eco- primarily focuses on the population. logical systems. In one respect, society In contrast, our concept of an eco- needs the ecosystem for support. The system emphasizes general system properties, ecosystem's ability to absorb CO2, release such as total biomass, , and 02, and process wastes is unaffected as long nutrient cycling, and minimizes considera- as the overall properties of the system tion of taxa. The difference in viewpoint persist. For these functions, species can be clarified by considering the composition se has little relevance. In ecosystem as it undergoes succession (Odum, other value systems, the ecosystem is viewed 1969). Although populations change as as a support system for values species, e.g., succession proceeds, productivity is a pro- sports fish or wildlife. The dilemma arises perty of the system measurable through time. when the ecosystem responds to perturbation Succession is not a sequence of different by shifts in species composition. Such systems, but a single system which exchanges shifts result in the persistence of the eco- transient species and populations through system, but also may result in the elimina- time. tion of valued species. This concept of the ecosystem as a A classic example of such a dilemma functional unit has analogies in community concerns the construction of the Indian analysis. Root (1973) introduced the con- Point Power Plant on the Hudson River. The cept of a "" as a group of species that use of river water as a coolant should re- occupy "equivalent" niches in a community. sult in a stable response by the total eco- Members of a guild have the same trophic system (Van Winkle, 1975). There will still function in the community and are seldom, if be an intact living system in the river ever, found together. Each plant, or group following the perturbation, but this stable of plants, may harbor a member of the guild response may be achieved by a critical but the specific species will differ from species replacement. A highly valued sports plant to plant. Thus, the guild has pro- fish, the striped bass, which uses the perties that transcend its component Hudson River as a spawning ground, may be populations. replaced by less desirable species such as white perch. In this respect, the ecosystem is not stable as a support system for this The Concept of Persistence valued species, and many elements of society regard this as an unacceptable alteration. The phenomenon of primary interest is In the present discussion, persistence the ability of the ecosystem to maintain refers to total ecosystem properties (i.e., functional integrity when subjected to total biomass, productivity). The "state" environmental changes. In other words, the of the system is defined by these properties, ecosystem is stable in some sense of the and a system is considered persistent or word. Because of ambiguity in the use of stable if these properties remain within reasonable bounds following perturbation. R. V. O'NEILL & D.E. REICHLE 13

ELEMENTS OF AN ECOSYSTEM THEORY Few systems rely exclusively on a single strategy. Forest ecosystems include an A theory of ecosystem persistence must herbaceous layer capable of rapid growth and contain a definition of the state of the reproduction (Taylor, 1974). Forests also system and its relevant components. Since contain saplings in the subcanopy strata persistence is a dynamic property, we stress capable of rapid growth if a canopy opening the functional components of the system. At occurs. Lake ecosystems with a of least three components are needed to explain phytoplankton production also may contain a ecosystem persistence: producers, hetero- zone of rooted or floating macrophytes. trophs as rate regulators, and a large Thus, the persistence of an energy base in storage component with slow turnover a fluctuating environment relies on the (O'Neill et al., 1975; Reichle et al., 1975c; opportunism afforded by the mix in that eco- O'Neill, 1976a). system of "fast" and "slow" turnover popula- tions of . The mechanisms by which ecosystems Primary Producers: The Ecosystem establish a persistent energy base translate Energy Base into competitive interactions among primary producer populations. A given number of The fixation of solar energy is essen- populations, with limited light, , tial to all ecosystems. Autotrophic popula- and water, will interact and tend to pack tions provide the energy base which supports the niche to support the maximum pri- secondary trophic structure. To persist in mary production that can be sustained by an unpredictable environment, the system available resources. The ecosystem strategy must be capable of flexibility in its energy- is simply the result of the population capturing function. This flexibility may be processes. achieved by two alternative "strategies." Whichever strategy characterizes a One strategy is to maximize resistance, specific ecosystem, a stable energy base i.e., the system becomes imperturbable, requires high rates of material (or energy) which results from producer organisms with processing. Odum and Pinkerton (1955) very large bionass and slow turnover. In postulated that the ability of the ecosystem this case, response to short-term environ- to persist is directly related to its mental changes is minimal. Mature forests ability to process energy. The larger the illustrate this strategy. These systems ratio of energy fixed to standing crop, the are usually dominated by "K-selected" more resilient the ecosystem. The validity species. The resistance strategy requires of this relationship was tested (O'Neill, that energy fixed exceed total metabolic l976a) by comparing the rates of recovery needs, so that net energy is available for after a 10 percent reduction in the standing structural elaboration of large organisms. crop of autotrophs in models of six eco- The second energy-capturing strategy is systems. The deviations from equilibrium that of resilience, i.e., a system maxi- were summed over time (25-year simulations), mizes its ability to recover rapidly in and each deviation was divided by the stand- response to perturbations. To maximize ing crop at equilibrium. The square root of resilience, the system consists of small the sum was compared to the energy process- biomass units with rapid turnover. Pelagic ing capabilities of the system (Table 1). phytoplankton-based systems illustrate this An increased ability to process energy is strategy. Such systems are usually composed associated with a decreased index of of "r-selected" species. Resilience can be recovery. The comparison (Table 1) indicates achieved either by a collection of species that recovery from perturbation is related to which are resilient to perturbations or by a the capability of the ecosystem to process collectionof species, each of which is energy. This reinforces our emphasis on the relatively nonresilient, but together can energy base of the ecosystem as a critical respond to a wide range of perturbations. ingredient in ecosystem persistence. Heterogeneity in spatial pattern, species composition, and genetic information are common elements of both resistance and Storage Capability: Nutrient Recycling resilience strategies. For the resistance and Ecosystem Resistance strategy, the development of large biomass consumes time and energy and, therefore, is Despite strategies to maintain a stable risky if persistence depends on a small carbon base, environmental extremes may number of species. For the resilience disrupt the energy-capturing capability of strategy, heterogeneity is required to en- an ecosystem. Since ecosystems are per- sure a large number of producer species, so sistent, some alternative to the energy- that no single perturbation is likely to capture component must exist to provide a destroy the entire species array. reserve energy supply. This reservoir must 14 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ,AN1LYS1S

Table 1. Comparison of ability to recover from perturbacion (JO decrease in primary producers) with energy-processing capability.1

Index of 3 Ecosystem type Recovery2 Power Reference

2 Tundra 7.9 x 10 0.018 Whitfield, 1972 ,2 Tropical forest 1.4 x 0.92 Odum and Pigeon, 1970 ,2 Deciduous forest 1.3 x 1.22 Reichle et al., 1973a

Salt marsh 1.3 xio2 1.28 Teal, 1972

Spring 1.9 x ,O 8.69 Tilly, 1968

Pond 5.8 x 10 32.2 Emanuel and Muiholland, 1976

'From Odum and Pinkerton, 1955. The comparison wasmade with a simple (O'Neill, 1976a) quantifiedfor eachof the systems. 2Meanerror sum ofsquares of deviations from equilibrium,divided by equilibrium values and sum over all compartments(see O'Neill,1976a). 3Primary production/standingcrop of active tissue.

Table 2. Comparison ofbiomasscs ofdetritus-based andplant-based heterotrophic food webs in terrestrialecosystems.-

Plant based Forest system Country based Animals Microflora

Temperatedeciduous2 USA 0.640 34.60 270.0

Tropical rain3 Puerto Rico 34.4 79.8 0.2

Temperatedeciduous4 Belgium 205.0 300.0

5 Subalpine coniferous Japan 2.6 50.0 280.0

6 Tropical deciduous Zaire 1.0 74.29

Temperatedeciduous7 England 3.0 360.0 890.0 8 Broadleaf evergreen Japan 3.0 1,680.0

Temperatedeciduous9 Denmark 0.5 1,435.0

1A11 valuesare in units of kgha1. 8Shidei in Reichle et al., 1973b. 2Edwardset al., 1974. 9Thamdrup in Reichle et al., l973b. 30dum and Pigeon, 1970 (assuming 5 kcal/gm). 4Denaeyer and Duvigneaud in Reichie et al., l973b.

5.Kitazawa in. Reichle et al., 1973b. 6Malaisse in Reichle et al., l973h. 7Satchell in Reichle et al., l973b. R. V. O'NEILL & D.E. REICHLE 15

Table 3. Nitrogen fluxes in terrestrial forestecosystems.1

Ratio System Country Inputs Losses input/losses

-1 -1 kgha y

Temperatedeciduous2 USA 13 109.5 0.12

Temperatedeciduous3 Belgium 8.7 79 0.11

Tropicalrain4 Puerto Rico 46 160 0.29

Coniferous5 Sweden 8 58 0.14

Tropical dry6 India 51 133 0.38

Mediterranean evergreen oak7 France 1.47 72 0.02

Montaneconiferous8 USA 5.1 12.3 0.41

1lnputs include atmospheric inputs and nitrification minus denitrification. Losses indicate total N lost from vegetation through litterfall, mortality,consumption, root . 2Henderson and Harris, 1975. 3Denaeyer and Duvigneaud in Reichle et al., 1973b. 40dum and Pigeon, 1970. 5Anderson in Reichle et al., 1973b. 6Bandhu in Reichle et al., 1973b. 7Lossaint in Reichle et al., 1973b. 8Stark, 1973.

be large (perhaps compensating for its sub- see in the data for nitrogen shown in optimal quality) and mustxhfbit slow Table 3. If elements were not recycled, response times so short-term fluctuations in growth of new tissue would depend solely environmental conditions would have minimal upon the input of nutrients from outside effect. Most ecosystems have a pool of in- the system (i.e., atmospheric and weathering active organic matter with the required of parent materials). Therefore, production characteristics of large size and slow would be reduced (by a factor of 0.5 to 0.1) response. to the rate of incoming nitrogen. This pool of inactive organic matter If our storage hypothesis is correct, serves as an alternate energy base. In we would expect soil organic matter and wood fact, for many systems, organic matter sup- components to be more important as tempera- ports a larger community of ture and moisture conditions for growth be- than living plant materials (Table 2). The come more favorable. Under these conditions, advantages of stability in the food base growth would more likely be limited by appear to more than compensate for the dis- nutrient availability and there would be advantages of difficult energy extraction. greater advantage to developing the organic This large, slow component plays a pool for nutrient conservation. role more important than supplying energy A climate index combining temperature it is fundamental for effective nutrient and moisture can be derived to test this recycling. Large pools of organic mass pro- hypothesis. Potential evapotranspiration, vide capability to store nutrient elements; PE, is proportional to the sum of daily slow turnover maximizes the probability that mean temperatures over 10°C. Average elements will be retained within the system. growing temperature, C, multiplied The importance of nutrient recycling can be by the length of the growing season, L, 16 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

0PNL-DVG 76-14935 should approximate the summation. The 80 exact relationship is given by Budyko (1956) A TR0PC6L EVERGREEN = 0.18 G L. A TR0PCAL DECDU0US 70 v BROADLEOF EVERGREEN By dividing PE into the actual precipitation TEMPERATE DEC)DL0uS during the growing season, p, we arrive at C- BOREAL EVERGREEN an index of moisture stress. We combine this index with average annual temperature, uj 60 T, to derive a measure of climaticcondi- U) tions (O1Neill and DeAngelis, in press), U) a (higher values indicate morefavorable H A climatic conditions), LU 50 H (U U)

HLU , can be com- This climatic index, ir 40 pared with the ratio of biomass of active leaf tissue to reservoir size (bole and (3 z branch biomass plus soil organic matter) U) for 16 stands in the International U) Data Set (Reichie, in press). Testing this 30 hypothesis for forests depends heavily on LU> the Woodlands Data Set. This data set is H V C-) composed of 117 sites which were involved U) in coordinated efforts to measure the 20 structure and function of woodland eco- 0 systems as a part of the International Bio- logical Program. With the conclusion of the program, these data are becoming avail- able in synthesized form (see Table 4) and represent a unique for the analysis a of forest ecosystems. Values of iT are correlated with size of the hypothesized nutrient reservoir 0 10 15 20 25 30 (Fig. 1). Although it may be an artifact -5 0 5 of the small number of sites, the relation- CLMATIC NDEX (ii-) ship approximates a straight line. The boreal forests lie toward the origin and Figure 1. The ratio of inactive organic tropical systems at the upper right, with matter (branch and bole biomass plus soil temperate deciduous and broadleaved ever- top organic) to active leaf tissue as a green forests occupying intermediate posi- function of the climatic index, a. The tions. The comparison confirms the pre- index is calculated as average annual tem- diction that systems in more favorable perature times precipitation during the conditions accumulate organic matter to growing season divided by potential evapo- store and retain nutrients. transpiration calculated according to the approximation of Budyko (1956).

Rate Regulation: The Role of Heterotrophs and Addy, 1975) maintain ecosystem hetero- geneity. Wiegert and Owen (1971) and Lee The role of regulation of and Inman (1975) have also discussed the ecosystem processes is essential to the stabilizing influence of heterotrophs. The persistence of ecosystems. popu- role of heterotrophs in nutrient dynamics lations may exert more control than would be has recently been summarized by Kitchell indicated by the small amount of organic and others (1979). matter actually consumed (OtNeill, l976a). The role of heterotrophs as regulators While consumption in forest canopies may be is apparent from the proportion of total only a few percent of net ., ecosystem respiration represented by hetero- the impact on photosynthetic potential can trophlc activities. Heterotrophic respira- be more substantial (Reichle et al., l973b). tion may account for between 35 and 55 Episodic outbreaks of populations (Mattson percent of total ecosystem respiration (auto- R. V. O'NEILL & D.E. REICHLE 17

trophic plus heterotrophic respiration) ORNL-OWG 74 6677 (Reichie Ct al., 1975b). Thus, a sub- 0IL a tantial pirtion of maintenance respiration 0 0 eaergy of cosystems is accounted for in z heterotroph activity. While a-0 Sm Tu organisms may play a role in rate regulation E 2 - _.Po )- 10 Df Cs of producers, Table 2 indicates that hetero- 10 S trophic effects are greatest in 0 TI a processes. In a forest ecosystem, 95 per- 0I- a cent of total heterotrophic respiration is a contributed by decomposers (Reichie et al., aI- 1 io o' 10' 102 1975b). o- Decomposer organisms increase the rate ENERGY INPUT PER UNIT STANDING CROP of release of nutrients from organic matter above that of simple physiochemical pro- Figure 2. 1-leterotroph biomass as a function cesses. While this increase may be un- of net primary production per unit plant important for highly mobile elements, it is biomass. Data from O'Neill, 1976a. The critical for nutrients tightly bound in six points represent ecosystem types: organic tissue (e.g., nitrogen). Simple Tu: tundra; P0: pond; Sm: salt marsh; increase in release rates, however, is in- Df: deciduous forest; Cs: cone spring; sufficient for ecosystem utilization, since Tf: tropical forest. References to the the rate of release must be commensurate original articles are given in Table 1. with the ability of soil and roots to absorb the nutrients. If the release is too slow, the demands of plant growth are not met. If the release is too rapid, much of the nutrient could be lost from the system by leaching. Thus, the heterotroph community performs an important function in controll- ORNL-DWG 74-6678 ing the fluctuations in the rate of release. I 1I This concept of control is important to 0a- understanding the complexity of interactions a within the decomposer community, particular- 6) ly the interactions of microflora and saprophagous animals. a-0 The evolutionary mechanisms resulting 'Sm In - Tu in the nutrient control system can be easily 10 Pp envisioned. Mortality of plants provides 10 Df 0 - Cs an energy base which can be exploited by a 'TI populations. Those populations 0I- a which evolved , possibly to avoid uJ C- with , begin to inter- IC act with the microbial opportunists already present in the dead organic matter. The resulting interaction stabilizes nutrient t [HIW releases and results in more efficient 102 lO recycling. Controlled nutrient availability ENERGY INPUT (Cal) permits sustained plant productivity and continued inputs of dead organic matter. Figure 3. Heterotroph bioinass as a function The result is a gradual buildup of the of net primary production. A key to the stable organic matter food base. abbreviations is given in the legend to In contrast to the view presented here, Figure 2. References to the original data consumers have often been considered are given in Table 1. simply as consuming excess production and playing a minor role in the maintenance and persistence of the ecosystem. If such a view were correct, then the biomass of heterotrophs should be directly related to the productivity or energy input into the system, or else to the productivity rate or energy input per unit of autotrophic stand- ing crop. Figures 2 and 3 demonstrate that this relationship does not hold. -Ti Cr)Co70 is takenTable from4. Burgess (1979) . Forest characteristics taken from the International Biological Program, Woodl Means were calculated for stands more than 50 years old. ands Data Set (Reichle,Outliers 1979) were . eliminated from the calculation if Forest classification 70 fl they were more than 2 standard deviations from the mean. Needle-leaved BOREAL Deciduous Brood-leaved Deciduous TE1ERATE Needle-leaved Deciduous -onoCo Characteristics (Plantation)Evergreen (Natural)Evergreen (Beech) (Natural) Evergreen(Natural) (Plantation)Evergreen Evergreen(Natural) (Plantation C-,Co70 0 Number of sites 6.65 0.259 7.49 19 9.9 21.5 1 13.6 5 6.15 10.2 CI)no-ISZ LeafMean areaprecipitationtemperature index (°C) (mm) 913 514 7.6 1073 5.2 917 5.2 2630 6.0 1338 935 8.8 1806 6.7 70-n Basal area (m2 ha 1) 25.846.2 17.232.8 23.930.6 20.823.7 1247.9 1534.5 2168.8 19.437.3 -1CoC',C)no AbovegroundStand height biomass(m) (g m2) 24452 1128 13917 516 25123 121B 17352 918 19328 1368 11918 1249 21437 1159 16938 939 Co AbovegroundLeaf biomass productivity (go 2) (g m2 y) 23081 1371 12443 964 24686 334 16249 350 18558 770 11249 647 22496 932 16080 359 Co WoodRatio biomass bark/bolebranch/bole (g m2) biomass biomass 0.090.13 0.070.18 0.050.30 0.27 0.36 0.150.24 0.37 0.11 WoodRatio productivity branch/hole (gproductivity m2 y1) 699 0.22 135 0.11 777 0.34 359 0.50 983 743 0.23 382 0.57 580 LeafRoot biomasslitterfall (g m2) (go2 y') 6005 344 3810 230 3842 308 3799 342 385 3116 348 201 3794 359 ifcalculatedData Tablethey Set were4.(Reichle, for more stands than1979). more2 standard than 50 deviations years old. from the mean. Forest characteristics taken from the International Biological Program, Woodlands classification is taken from Burgess (2979) . Outliers were eliminated from the calcuLation Means were (Plantation)Deciduous Broad-leaved (Plantation)DeciduousTROPICAL Evergreen(Natural) MEDITERRANEANBroad-leaved Evergreen(Natural) Number of sites Characteristics 14 2 4 3 Mean precipitationtemperature (°C) (mm) 1158 27.5 1058 1851 26.5 908 12.9 BasalLeaf area area index (m2 ha') 29.4 9.2 26.3 29.8 8.9 41.3 4.3 AbovegroundStand height biomass(m) (g m 2) 15200 14.3 17200 13.8 43266 37.8 28753 17.1 AbovegroundLeaf biomass productivity (g m (g m2 y1) 2) 1631 834 1304 1549 694748 WoodRatio biomass branch/bole (g a2) biornass 14355 0.16 16494 0.41 37126 0.2] 27825 0.10 WoodRatio productivity bark/bole biornass (p a2 y1) 1009 747 0.19 01cD RootRatio bioaass branch/bole ( productivity 2) 3459 2908 0.44 90 Leaf litterfall (p a 2 y l) 639 496 654 217 PtO 01I- 20 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

If heterotrophs actively participate ORNL-DWG 76-14936 L,J in the functional dynamics of the system and play a role in rate regulation, we would expect that greater heterotrophic 08 biomass would be supported per unit of autotrophic biomass as the need for regula- tion increased. That is, as the potential 6 for rapid fluctuations in autotroph biomass increases, the need for rate regulation 4 also increases. O'Neill (l976a) found this 0

relationship by comparing different eco- UI F- 1-0 forests UI I systems ranging from tundra through I to pond ecosystems. This hypothesis can .0 also be tested with data summarized by Whittaker and Likens (1973). Figure 4 0 5 10 15 20 25 30 (from O'Neill and DeAngelis, in press) ECOSYSTEM TURNOVER TIME (years) clearly shows that as turnover times (total above-ground biomass/net primary production) Ratio of heterotroph to auto- increases, the heterotroph/autotroph ratio Figure 5. troph biomass as a function of total eco- decreases. Figure 5 shows that the expected rela- system turnover time with data from the Only four sites have tionship also exists for four of the Wood- Woodlands Data Set. sufficient information to permit inclusion lands Data Set sites (Table 4). These Calculations are based on analyses reinforce the concept that con- in the figure. aboveground biomass only. sumers play an active role in ecosystems, and the more rapid the turnover of the system, the greater the heterotroph biomass required to maintain and regulate energy Population Interactions and flow through the system. Ecosystem Dynamics

ORNLDWG 76-44931 Discussion of the dynamic properties of ecosystems leads to a consideration of how U, these properties are related to interactions U, H .0 --4 ±--- I among populations in the ecosystem. Linde- 25 G man (1942) showed that the energy-processing I S I structure of the ecosystem resulted in a a- IIiIiiILiTiT 0 layered trophic structure. Heatwole and H Levins (1972) have shown that this trophic - structure is more consistent than the taxo- I- nomic entities which compose the trophic 0 H- levels. Levins (1974) and others have lO0 shown that populations can be stable only in C,) .0 specific configurations. Fager (1968), 0 Evans and Murdock (1968), and Teraguchi and co-workers (1977) all found that species I a- may change in different systems, but a basic 0 underlying trophic structure appeared con- H 0 sistently. O'Neill and Giddings (in press) UI H argued that resource competition among H UI phytoplankton populations would result in I relatively constant total production, no lO 2 5 100 2 5 40' matter what the mix of species. These ECOSYSTEM TURNOVER TIME (years) studies lead to interesting questions about ecosystem properties and underlying popula- Figure 4. Ratio of heterotroph to auto- tion configurations. troph biomass as a function of total eco- Populations competing for a limited system turnover time. Data from Whittaker resource, such as light or nutrients, are and Likens, 1973. System turnover time is essentially functioning in a parallel con- calculated as total aboveground biomass figuration (Fig. 6). In this case, dis- plus litter divided by aboveground net pri- mary production. R. V. O'NEILL & D.E. REICHLE 21

turbance to a single population would free ORNL-DWG 77-4624 other populations from competition, enabling PARALLEL SERIES OR CYCLING them to use the available resource. Con- ..ider a system parameter such as total or total respiration which results from the summation of the activity of the individual populations. Since the limited resource constrains the entire system, the expected result of a disturbance to a single population is that the system parameter would remain relatively constant even though the populations changed. If populations operate in a cyclic configuration (Fig. 6), then each population must process a resource before it can be SYSTEM PARAMETER: utilized by other populations in the system. Such a configuration would be expected in ENERGY FLOW NUTRIENT CYCLING (e.g. TOTAL RESPIRATION )(e.g. NUTRIENT LEACHING nutrient cycling or in of complex substrates. In this case, a per- turbation in any part of the cycle will Figure 6. Thro possible configurations for affect the overall process. population interactions. The parallel con- Ecological systems can be expected to figuration corresponds to populations in contain both parallel and cyclic configura- the same , performing similar tions. Examination of Figure 6 suggests, ecosystem functions and interacting with however, that if the system is disturbed, each other primarily through a limited some parameters (e.g., rates of nutrient resource. The cyclic configuration might cycling) will be relatively sensitive. To correspond to populations involved in test this concept, unpublished data of cycling of a nutrient or breakdown of a Ausmus and E. C. O'Neill on CO2 efflux and complex organic compound. leaching of NO3, NH, and PO4 from soil core microcosms were analyzed. By compar- The third index of variability, K, was ing the variability in the time series of the number of times that successive values respiration and nutrient loss data, it was differed by more than 100 percent. Table 5 possible to test whether an ecosystem para- shows that, again, K was always smaller for meterwhich results from the summation of the respiration values. individual populations activity (CO2 efflux) Table 5 shows unambiguously that the is relatively constant compared to a para- CO2 efflux was more constant in the micro- meter based on successive processing of a cosm system than was nutrient loss. With a resource (N and P cycling). single exception, the difference was always Three indices were developed to deter- greater than a factor of 2 and frequently mine whether CO2 efflux was less variable greater than an order of magnitude. Thus, through tine than nutrient loss. The first the analysis confirms the hypothesis that index was the coefficient of variation a system property resulting from the sum of (standard deviation divided by the mean for the activities of populations (respiration) the entire time series). Table 5 shows that is less variable than a system property the coefficient of variation was smaller for which depends on the cyclic processing of a the respiration rates in all replicates. resource (N and P cycling). A second index,Z,is given by The potential lack of stability of cyclic configurations leads us to ask whether one can predict the sensitivity of n x. x. ecosystem processes based on their under- 100 I i+l z lying structure. A sensitive process proba- n mm (x., x. ) i=l I i+l bly would involve multiple populations interacting in a cyclic configuration. where is the ith observation, n is the Because cyclic interactions depend on con- tinuity of rate processes, a perturbation total number of observations, and mm ( ) indicates that the smaller of the two values may not be sufficient to eliminate a popu- lation, but it may be enough to move the and was taken as the divisor. Z measures the average percentage difference system into a new, unstable state. Con- between successive measurements. Table 5 trolling variables might determine the shows that F was always lower for the CO2 magnitudes of flows between populations and ef flux data. the timing and synchronization of the pro- cess. Such an ecosystem process might be more sensitive than individual populations. 22 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Table 5. Comparison of variabilitp in CO2 efflux and nutrient leaching for six replicate soil cores.1

Replicates

1 2 3 4 5 6

Coefficient of variation

CO2 0.24 0.25 0.27 0.24 0.27 0.26 NO3 0.68 0.58 0.69 0.63 0.97 0.72 NH3 2.86 2.62 0.54 1.30 0.88 0.55 PO4 2.37 1.94 1.50 1.36 1.95 2.42

CO2 30 250 20 13 21 19 NO3 876 291 106 1,404 148 113 NH3 15,325 1,626 159 501 258 64 PO4 3,850 1,391 1,200 425 1,250 2,500

K4

CO2 0 1 0 0 0 1

NO3 6 8 4 7 6 5

NH3 9 11 2 6 4 3

PO4 9 12 10 10 9 15

'Dataare presented for three indices of variability (CO2 efflux N = 38; NO3, NH3, PO4 N= 18. Standard deviation/mean. 3Average percent difference between successive measurements. See Equation 1. 4Number of time successive measurements differed by more than 100 percent.

Nutrient cycling involves a significant with associated herbaceous ground cover. number of populations operating in a cyclic The surface of the soil was contaminated by configuration. Consequently, increases in adding litter collected adjacent to a lead nutrient loss from the system might occur smelter. This litter contained high con- irrespective of which specific organisms or centrations of several heavy metals (Jackson processes are being affected. Indeed, and Watson, in press) that subsequently physiological changes in response to some leached into the intact soil. perturbation might affect the rates and After nine of monitoring, no timing of processes in the significant differences could be detected in without detectable changes in populations. the tree growth (Table 6). However, mean Shugart and others (1976) have suggested values for Ca concentration in soil leachate that a nutrient in soil solution (i.e., were significantly higher (p < 0.05) for calcium) would have excellent properties as treated microcosms. Similar sensitivity of a monitoring point for overall system con- the nutrient cycling parameters were also trol. seen in small soil core microcosms and in This hypothesis has been tested with field sampling in forests adjacent to the data from microcosm experiments (O'Neill lead smelter (O'Neill et al., 1977). et al., 1977). The experiment consisted of These studies do not demonstrate, of six boxes of an intact soil, each containing course, that sensitive population parameters a red maple sapling approximately 2 m high, R.V. O'NEILL & 0.E. REICHLE 23

Table 6. Population and system level parameters from microcosms of Emory silt loam soil containing Acer rubrum seedlings (values represent means ± S.E.)

Population System parameter parameter

Treatment Annual branch Ca concentration (Pb mg/cm2) growth (cm) in leachate (pg/mi)

347 ± 42.8 6.6 ± 0.4

12 346 ± 67.7 10.0 ± 0.8

do not exist. However, it is not apparent guilds in the sense of Root, 1973), environ- which populations should be chosen a priori mental changes simply shift competitive as indicators of stress. The experiments advantages. If the perturbation is local- demonstrate that nutrient cycling processes ized (e.g., forest fire), spatial hetero- are relatively sensitive and changes can be geneity ensures that some individuals will detected in these processes before signifi- escape. In these and other ways, redun- cant increases in mortality of the popula- dancy in the system prevents catastrophic tions are evident. consequences due to perturbations. There are also detectable patterns of distribution which must be considered. Heterogeneity as a Mechanism Thus, the spatial distribution (clumping) for System Persistence of prey affects the rate of feeding by a predator (Pielou, 1969). The effect of Heterogeneity, the final element of the patterning along a gradient on ecosystem theory, may appear in a variety of ways: stability has been investigated by Smith diversity of species, spatial heterogeneity, (in press). The patterning may not or genetic heterogeneity within populations. necessarily be spatial, since there are Such heterogeneity is apparent in the distinct patterns (i.e., "J-shaped" fre- natural system and the search for patterns quency distributions, Pielou, 1969) in the in this heterogeneity is a major field of distribution of species abundances within investigation for community ecologists. communities. There also appear to be In stating that heterogeneity is distinct patterns of interactions among essential for ecosystem persistence, we do populations (Teraguchi et al., 1977; Heat- not imply any simple relationship between wole and Levins, 1972) in the form of and stability. The com- underlying trophic relationships and guild plexity/stability question at the community patterns. Since these patterns are dis- level has been discussed, and it has been cernible within the system structure, we argued elsewhere (Van Voris et al., 1978) hypothesize that pattern plays some role in that there is no reason to believe that the the persistence of the total system. Con- relationship should hold at that level. sideration of patterns of heterogeneity as Increased stability with increased numbers a component of ecosystem stability is intui- of species has been difficult to demonstrate tively appealing to the ecologist but has experimentally, and theoretical studies received little attention at the ecosystem (May, 1973) indicate that stability should level of resolution. Many of our present be expected to decrease. On the other hand, environmental problems will require us to Van Voris and others (1978) present data view the ecosystem in a broader context, that suggest complexity may be related to i.e., as an element in a landscape or stability at the total ecosystem level. regional mosaic. Heterogeneity can be viewed in terms of redundancy in function and pattern. Redundancy is essential so that any single SUMMARY perturbation is unlikely to destroy all capability for performing a critical func- Various dimensions of ecosystem struc- tion. If the system contains multiple ture and behavior seem to develop from the species capable of similar functions (i.e., ubiquitous phenomena of system growth and 24 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Stroudsburg, Penn.: Dowden, persistence. While growth and persistence Marshall. attributes of ecosystems may appear to be Hutchinson and Ross, Inc. simplistic phenomena upon which to base a comprehensive ecosystem theory, these same Elton, C. 1946. Competition and structure attributes have been fundamental to the of ecological communities. J. Amer. theoretical development of other biological Ecol. 15:54-68. disciplines. We explored these attributes at a hierarchical level in a self-organizing Emanuel, W. R., and R. S. Mulholland. 1976. system and analyzed adaptive system strate- Linear periodic control with applica- gies which resulted. We have taken causa- tions to environmental systems. Tnt. tive relations previously developed (Reichle J. Control 24:807-820. et al., l975c), expounded upon their theo- retical implications, and tested these Evans, F. C., and W. W. Murdock. 1968. assumptions with data from a variety of Taxonomic composition, trophic struc- forest types. Our conclusions are not a ture, and seasonal occurrence in a theory in themselves, but an organization of grassland insect community. J. Anim. concepts contributing towards a unifying Ecol. 37:259-273. theory, along the lines promulgated by Bray 1968. The community of in- (1958). The inferences drawn rely heavily Fager, E. W. upon data from forested ecosystems ofthe in decaying oak wood. J. world and have yet to be validated against Anim. Ecol. 37:121-142. data from a much more diverse range of eco- system types. Not all of our interpretations Heatwole, H., and R. Levins. 1972. Trophic are logically tight, and other explanations structure stability and faunal change will provide fruitful grounds for further during recolonization. Ecology 53: speculation. 531-534.

Henderson, G. S., and W. F. Harris. 1975. LITERATURE CITED An ecosystem approach to the character- ization of the in a Ausmus, B. S., and M. Witkamp. 1973. deciduous forest watershed. Ii Forest Litter and soil microbial dynamics in Soils and Forest Land Management, a deciduous forest stand. EDFB/IBP- edited by B. Bernier and C. H. Winget. 73/10. Oak Ridge National Lab., Oak Quebec: Laval University Press. Ridge, Tenn. Jackson, D. R., and A. P. Watson. Disrup- Botkin, D. B., and M. J. Sobel. 1975. tion of nutrient pools and transport Stability in time-varying ecosystems. of heavy metals in a forested water- Amer. Nat. 109:625-646. shed near a lead smelter. J. Env. Qual. (in press). Bray, J. R. 1958. Notes toward an eco- logical theory. Ecology 39(4):770- Juday, D. 1940. The annual energy budget 776. of an inland lake. Ecology 21:438- 450. Budyko, M. I. 1956. The Heat Balance of the Earth's Surface, trans. by N. I. Kerner, A. 1863. Plant Life of the Danube Stepanova, 1958. U.S. Weather Bureau, Basin. Trans. by H. S. Conard, 1951, Washington, D. C. The Background of Plant Ecology. Ames: Iowa State University Press. Clements, F. E. 1904. The development and structure of vegetation. Bot. Surv. Kitchell, J. F., R. V. O'Neill, D. Webb, Nebr. 7:1-175. C. W. Gallepp, S. M. Bartell, J. F. Koonce, and B. S. Ausmus. 1979. Con- Cook, R. E. 1977. Raymond Lindeman and sumer regulation of nutrient cycling. the trophic-dynamic concept in eco- BioScience 29:28-34. logy. Science 198:222-226. Lee, J. J., and D. L. Inman. 1975. The Cowles, H. C. 1901. The physiographic ecological role of consumers an ecology of and vicinity. Bot. aggregated systems view. Ecology 56: Gaz. 31:73-108, 145-182. 1455-1458.

Edwards, N. T., f. F. Harris, and H. H. Levins, R. 1974. Qualitative analysis of Shugart. 1974. Carbon cycling in partially specified systems. Ann. N.Y. deciduous forest. In The Belowground Acad. Sci. 231:123-138. Ecosystem: A Synthesis of Plant- Associated Processes, edited by J. K. R. V. O'NEILL & D.E. REICHLE 25

Lindeman, R. L. 1942. The trophic-dynamic O'Neill, R. V., W. F. Harris, B.S. Ausmus, aspect of ecology. Ecology 23:399-418 and U. E. Reichle. 1975. A theoreti- cal basis for ecosystem analysis with Macfadyen, A. 1964. Energy flow in eco- particular reference to element cycling. systems and its exploitation by In Mineral Cycling in Southeastern Eco- In Grazing in Terrestrial and Marine systems, edited by F. G. Howell, J. B. Environments, edited by D.J. Crisp, Gentry, and M. H. Smith, pp. 28-40. pp. 3-20. Oxford: Blackwell. ERDA Symp. Series (CONF-7L+05l3).

Mattson, W. 3., and N. D. Addy. 1975. O'Neill, R. V., B. S. Ausmus, D. R. Jackson, Phytophagous insects as regulators of R. I. Van Hook, P. Van Voris, C. forest primary production. Science Washburne, and A. P. Watson. 1977. 190:515-522. Monitoring terrestrial ecosystems by analysis of nutrient export. Water, May, R. M. 1973. Stability and Complexity Air, and Soil Pollution 8:271-277. in Model Ecosystems. Princeton, N.J.: Princeton University Press. O'Neill, R. V., and D. L. DeAngelis. Com- parative analysis of forest ecosystems. Odum, E. P. 1969. The strategy of eco- In International Woodlands Synthesis system development. Science 164:262- Volume, edited by D. E. Reichle. 270. Cambridge University Press (in press).

Odum, H. T. 1957. Trophic structure and O'Neill, R. V., and J. M. Giddings. Popu- productivity of Silver Springs, Florida. lation interactions and ecosystem Ecol. Monogr. 27:55-112. function. In Systems Analysis of Eco- systems, edited by G. S. Innis and Odum, H. T., and E. P. Odum. 1955. Trophic R. V. O'Neill. Fairland, Md: Internat. structure and productivity of a wind- Coop. Publ. House (in press). ward coral reef community at Eniwetok Atoll. Ecol. Monogr. 25:291-320. Pielou, E. C. 1969. An Introduction to Mathematical Ecogy. New York: Odum, H. T., and C. F. Jordan. 1970. Meta- Wiley-Interscience. bolism and evapotranspiration of the lower forest in a giant plastic cylin- Price, P. W. 1975. Insect Ecology. New der. In A Tropical Rain Forest, York: John Wiley and Sons, Inc. edited by H. T. Oduin and R. F. Pigeon, pp. 1165-1190. USAEC, Division of Reichle, D. E. 1975. Advances in eco- Technical Information, Washington, D.C. system analyses. BioScience 25:257- 264. Odum, H. T., and R. F. Pigeon, eds. 1970. A Tropical Rain Forest. USAEC, Divi- Reichle, D. E., ed. International Wood- sion of Technical Information, lands Synthesis Volume. Cambridge Washington, D. C. University Press (in press).

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O'Neill, R. V. l976a. Ecosystem persistence Reichle, D. E., B. E. Dinger, N. T. Edwards, and heterotrophic regulation. Ecology W. F. Harris, and P. Sollins. l973a. 57:1244-1253. Carbon flow and storage in a forest ecosystem. In Carbon and the Bio- O'Neill, R. V. l976b. Paradigms of eco- sphere, Proc. 24th Brookhaven Sym. on system analysis. In Ecological Theory Biology (CONF-7205l0), edited by G.M. and Ecosystem Models, edited by S. A. Woodwell and E.V. Pecan, pp. 345-365. Levin, pp. 16-20. Office of Ecosystem Springfield, Va.: National Technical Studies, The Institute of Ecology. Information Service.

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Reichle, D. E., J. F. Franklin, and D. W. Tilly, L. J. 1968. The structure and Goodall. l975a. Productivity of World dynamics of Cone Spring. Ecol. Monogr. Ecosystems. Washington, D.C.: 38: 269-197. National Academy of Sciences. Van Voris, P., R. V. O'Neill, H. H. Shugart, Reichle, D. E., J. F. McBrayer, and B. S. and W. R. Emanuel. 1978. Functional Ausmus. l975b. Ecological energetics complexity and ecosystem stability. of decomposers in a deciduous forest. Oak Ridge National Lab. Rep. ORNL/TN- In Proc. 5th Internatl. Colloquia of 6199. Oak Ridge, Tenn. Soil Zoology, Prague, Czechoslovakia, October 1973. Van Winkle, W. 1975. The application of computers in an assessment of the Reichle, D. E., R. V. O'Neill, and W. F. environmental impact of power plants Harris. l975c. Principles of energy on an . In Proc. of and material exchange in ecosystems. Conf. on Computer Support of Environ- In Unifying Concepts in Ecology, mental Science and Analysis, pp. 85- edited by W. H. van Dobben and R. H. 108. Albuquerque: ERDA. Lowe-Connell, pp. 27-43. The Hague: Junk. Wetzel, R. G., and P. H. Rich. 1973. Car- bon in freshwater systems. In Carbon Root, R. B. 1973. Organization of plant- and the Biosphere, Proc. 24th Brook- associations in simple and haven Symp. on Biology (CONF-72O51O), diverse habitats: the fauna of edited by C. N. Woodwell and E. V. collards (Brassica oleracea). Ecol. Pecan, pp. 241-263. Springfield, Va. Monogr. 43:95-124. National Technical Information Service.

Schimper, A. F. W. 1903. Plant Geography Whitfield, D. W. A. 1972. Systems analysis. upon a Physiological Basis. Oxford, In Devon Island IBP Project, High U.K.: Clarendon Press. Arctic Ecosystem, edited by L. C. Bliss, pp. 392-409. Dept. of Botany, Shugart, H. H., D. E. Reichle, N. T. University of Alberta, Edmonton. Edwards, and J. R. Kercher. 1976. A model of calcium-cycling in an East Whittaker, R. H., and G. E. Likens. 1973. Tennessee Liriodendron forest: Model Carbon in the biota. In Carbon and the structure, parameters, and analysis in Biosphere, Proc. 24th Brookhaven Symp. the frequency domain. Ecology 57:99- on Biology (CONF-720510), edited by 109. G. N. Woodwell and E. Pecan, pp. 281- 300. Springfield, Va.: National Smith, 0. L. The influence of environmental Technical Information Service. gradients on ecosystem stability. Amer. Nat. (in press). Wiegert, R. G., and D. F. Owen. 1971. Trophic structure, available resources Stark, N. 1973. Nutrient Cycling in a and population density in terrestrial Jeffrey Pine Ecosystem. Institute for vs. aquatic ecosystems. J. Theoret. Microbiology, University of Montana, Biol. 30:69-81. Missoula. Witkamp, M. 1971. Soils as components of Taylor, F. G., Jr. 1974. Phenodynamics of ecosystems. Ann. Rev. Ecol. Syst. production in a mesic deciduous forest 2:85-110. In Phenology and Seasonality Modeling, edited by H. Lieth, pp. 237-254. New Woodwell, G. M., and D. B. Botkin. 1970. York: Springer-Verlag. Metabolism of terrestrial ecosystems by gas exchange techniques. In Teal, J. M. 1962. Energy flow in the salt Analysis of Temperate Forest Eco- marsh ecosystem of Georgia. Ecology systems, edited by D. E. Reichie, 43:614-624. pp. 73-85. New York: Springer-Verlag.

Teraguchi, S., M. Teraguchi, and R. Up- church. 1977. Structure and develop- ment of insect communities in an Ohio old-field. Environ. Entomol. 6:247- 257. Ecosystems over Time: Succession and Other Types of Change

James A. MacMahon

INTRODUCTION HISTORICAL OVERVIEW

Biologists discussing change in eco- Before the word "succession" had even systems or communities generally subdivide been applied to biological systems, many their discussion based on the time interval observers referred to changes of plant over which change takes place. Short-term species composition of plots of ground, changes are thought to involve both internal over time. Golley (1977) mentioned a very ecosystem dynamics and the effects of allo- early paper (King, 1685) which presented genic perturbations, both of which cause observations of successional change in an fluctuations in various ecosystem attri- Irish bog without reference to the general butes (Rabotnov, 1974). Ecosystem change concept or use of the specific term. over moderate intervals is termed succes- I do not attempt to totally review the sion, while long-term change is generally history of the concept of succession here, defined as community or ecosystem evolution. only to point out that the process was so For a more detailed presentation of the "obvious," especially where trees were kinds of ecosystem change over time, see involved, that ecological historians can Major (1974). interpret writings as far back as Theophras- Part of all change in the organization tus (300 B.C.) containing discussions of of the organisms occupying a plot of ground succession. Indeed, such empiricists as is caused by very similar and fundamental Thoreau (1860) used familiar interpretations processes, regardless of the time scale in- of succession in a discussion of volved. That is, the evolution of communi- occurring in the hardwood zones of New ties and ecosystems, England (see Spurr, 1952). and short-term ecosystem or community The formalization of the concept, by fluctuation are all similar processes, application of a term, may be attributed to differing only in the time scale of the Dureau de la Malle (1825). From 1870 on- observer's mental reference system. ward, European ecologists implied succession To approach these complex anastomosing in their observations of vegetation while and overlapping relationships I shall focus attempting to develop classifications on the part of the time scale which empha- (Warming, 1909) sizes succession. I will attempt to dis- In the United States the work of Cowles cuss succession in terms of its historical (1899) expressly emphasized that, given development as a concept, its universality, enough time, vegetation would converge and details of the types of successional through succession to the same species nix changes thought to occur, along with the within a broad geographic area. As causes of the observed changes. Finally, I Whittaker (1974) points out, this involves will compare succession with the other types the assumptions that the end result of the of ecosystem change mentioned above. convergence is (1) stable and self-maintain- My definition of ecological succession, ing,(2) the terminus of the convergence for simplicity, is merely the change in the process, and (3) the characteristic and pre- biocoenosis (sensu Hutchinson, 1978) of a vailing plant community in that geographic plot of the earth's surface over a moderate (assume climatic) area. time period, i.e., tens to a few hundreds The result of these early studies was of years. Unlike many, I assume no in- the presentation of a plethora of observa- herent order to the process and no closely tional studies to verify the successional defined time schedule. trends and the climaxes of various areas,

27 28 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

particularly those culminating in forested knowledge is actually inferred from analysis sites in North America. Clemens (1916, of spatial variation in vegetation, where 1928, 1936) codified successional observa- various plots supposedly represent different tion by developing a lexicon to describe stages in a chronosequence. Such an assump- variations in the process and endpoints of tion is obviously forced by the long-time succession. His system used an analogy interval required by many seres and the between the community and the individual short observation period of most investiga- organism, where succession was akin to the tors. That this short observation period ontogeny of the individual. This approach is a fact is humorously obvious from Horn's was rapidly assaulted (Gleason, 1926, 1927, (1971) definition of climax as ".. . that 1939; Whittaker, 1951, 1953, 1957, 1962). stage when no significant change occurs It is now fairly clear that despite numerous during the lifetimes of several research detailed data presentations, many workers grants." have misunderstood the philosophical position After the word "succession" was first from which Clements' arguments emanated applied, the "concept" developed as an (Johnson, 1979). For details of the early important part of a whole system of ecology history of the concept of succession in by Clements. Despite the philosophical ob- North America and an evaluation of the jections of workers like Gleason directed various philosophies expressed, see Cooper to the mechanism causing change, the cata- (1926). loging of examples of succession from many While in its extreme form the analogy situations was enthusiastically implemented. between an organism and an ecosystem has A gradual falling away from Clementsian disappeared from ecological thinking (cf. views followed, replaced by the "ecosystem" Morrison and Yarranton, 1974; Williams appraoch of Odum and Margalef. Currently et al., 1969), there have been recent there is unrest and a search for a mechan- attempts to review the- emergent properties ism(s) to explain the phenomenon of eco- (see Salt, 1979, for comment on the use of logical succession. Details of the eco- this term) of ecosystems over time system development scheme were challenged (Margalef, 1968; Odum, 1969). Currently, by Drury and Nisbet (1973), whose work re- more workers are considering succession as newed interest in succession. Contemporary the outcome of interactions of individual workers have masses of detailed data (e.g., species with the environment, including the Bormann and Likens, 1979) that can be used biota (Connell, 1972; Connell and Slatyer, to address successional questions. These 1977; Drury and Nisbet, 1973; Grime, 1977; data have permitted new models, both mathe- Horn, 1974, 1975, 1976; Pickett, 1976; Van matical and verbal in nature, to be Hulst, 1978). Thus, the concept of a gen- developed. Despite these developments, eral convergence to a single species mix, succession continues to defy careful classi- over successional time, is often rejected; fication into a meaningful system, underlain for example, see the detailed study by by known cause and effect relationships. Matthews (1979a) of 636 sites of known age. Throughout the rest of this paper I While these are more robust approaches, they will discuss various levels of successional hardly differ from the ideas of Gleason relations, from the world pattern of where (1917, 1926, 1927, 1939), except in detail succession may or may not occur, to changes and mathematical sophistication. in single plots over short time periods Part of the intellectual underpinnings (tens of years). The history of some of older succession theory paralleled the aspects of successional theory, particularly development of the theory of evolution. since Odum (1969), was consciously omitted Initially biologists were inundated by in the terse treatment above and will emerge variety without seeing pattern. Then, when in these subsequent considerations. geologists developed earth science general- ities, the light went on for biologists and they followed the earth science lead. In- WORLD PATTERN OF SUCCESSION stead of a Lyell-Darwin combination as in evolution, ecology has its Davis-Cowles! Even though many authors catalogued Clements . Davis over a period of supposed successional changes in their years discussed the "Geographical Cycle" favorite vegetation type, some ecosystem (Davis, 1899, 1909), an idea which appealed types seemed, on the surface, to be devoid to a geologist-turned-ecologist like Cowles, of successional changes. Succession was who applied this perspective to changes in most obvious on sites where the climax con- sand dune vegetation. tained trees--whether this was in a temper- Since succession occurs over time ate or tropical climate. On the other intervals of moderate , it has sel- hand, succession seemed less obvious in cer- dom been observed directly (Drury and tain vegetation types, most notably deserts Nisbet, 1973). Rather, most successional and tundra (Muller, 1940, 1952). Since suc- J. A. MacMAHON 29

cession is usually characterized as a change plots the position of different ecosystem through time of species composition and types, separating those characterized by community structure of a site (see Pickett, "differentiated" and "ndifferentiated" suc- 1976), then the obviousness of succession cession (Fig. 1). He further subdivides must relate to the difference in percent the undifferentiated succession on the basis composition of species of initial and climax of his inferences about the specific reasons stages of disturbed plots or by differences for the lack of succession (Fig. 1). The in ecosystem structure. A common structural four he recognizes are: Aclimaxes, which feature used to emphasize change in eco- contain dominants having generation times systems is physiognomy or lifeform. This which are short compared to environmental approach is implicit in the use of attri- change and which are in "incessant" com- butes to measure successional change such munity fluctuation; Cycloclimaxes, where as stratification, size, and growth changes; "generations are timed to annual environ- see Oduin (1969). mental fluctuations"; Cataclimaxes, which The recognition of differences in the may or may not show succession, but where obviousness of succession in different eco- "generations correspond to irregular inter- systems is most common in terrestrial vals between destructions"; and Super- systems, where the majority of succession climaxes, where "generations are long rela- studies have been conducted. The same vari- tive to environmental fluctuation" and ation in the assessment of whether or not where a dominant's self-replacement is more succession occurs has also been applied to or less continuous, but the environmental aquatic communities (Blum, 1956; Wautier, modifications are small. These names 1951). The most detailed assessment of the designating climax "types" are not meant to obviousness of succession seems to be be formal terminology. Whittaker's (1974), wherein he specifically

"EU CLIMAXES" z HIGH FOREST 0 WOODLAND C) LL SAVANNA 0 FORESTFIRE\ J "CATACLI MAXES" z TUSSOCK w GRASSLANDS 2 ANNUAL- DIFFEREN T144 TED 0 UNDIFFERENTIATED > SHRUBDESERT' SUCCESSIONS z /1 \"CYCLOCLIMAXES" w TUNDRA ANNUAL LITTORAL, CORAL REEF \ DESERT U) PLANKTON "SUPERCLIMAXES" U) \ PERIPHYTON 0 AII BNTHOS ARCTICDESERT/ m LIFE CYCLES / ENVIRONMENTAL FLUCTUATION

Figure 1. Whittaker's (1974) scheme relating characteristics of climaxes and successions to one another and other community characteristics.Effectiveness of the distinction of climax from non-climax, and utility of the climax concept, increase obliquely upward to the right (redrawn by permission). 30 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

While considering the lack of apparent On the other hand, the combination of succession in some ecosystems, I asked the extreme values of an environmental factor following question: "What property of and the unpredictable variation obviously tundra and desert environments, two biomes taxes the adaptive suites of most organisms. where succession is often not conspicuous, In the context of succession then, I sug- is similar and might potentially be related gest that the only species that can survive in a cause and effect manner to succession in extreme environments are the ones that of plant species?" are already there. Thus, disturbance of a An obvious answer is that biomes are climax area opens up a plot of ground, but frequently differentiated on two-dimensional the only viable colonists are members of graphs, using mean annual temperature and the same species mix; the result is auto- mean annual rainfall as the axes (Fig. 2). succession (Muller, 1952). Thus, low While I realize that three or more axes of desert and tundra precipitation plus the environmental factors give better resolution extreme variability of precipitation may (Holdridge, 1967) and have even field eval- greatly limit the number of species capable uated such systems (MacMahon and Wieboldt, of adapting to these conditions. 1978), increases in resolution through in- Specifically I suggest that, as a creasing dimensionality are not required. worldwide pattern, low annual precipitation, Since tundra and desert differ so vastly in but more importantly its unpredictable vari- temperature, their similar low moisture ation, limits the species pool and their regimes is one apparent common feature. effects on the environment so that succes- As mean annual rainfall decreases, the sion is "telescoped" (Whittaker, 1974). I variance around that mean increases (Goudie believe that succession occurs in these and Wilkinson, 1977). We can conceive of areas and that the mechanism is the same, evolutionary adaptation of organisms to but that the results of the process are not extreme values of environmental factors obvious to casual observation. (e.g., low annual precipitation) if these Even in ecosystems where classical suc- extreme values occur in predictable ways. cession seems not to occur, minor species

1GRASSLAND DESERT TROPICAL FOREST 3 - U 11.1 0 /

i/ ( FOREST 4I- U a- :ROUS FOREST U I- 4-J 2 2 4 2 4 U

100 200 300 400 MEAN ANNUAL PRECIPITATION (cm)

Figure 2. Depiction of the differentiation of biomes on the bases of temperature and rainfall (redrawn from Hammond, 1972). J..4. MacMAHON 31

changes may take place following some types biome designation by referring to published of disturbance. For some desert examples, vegetation descriptions. see Beatley (1976), Shields and Wells (1962), The mean annual precipitation data Wells (1961), and the reviews of desert suc- were used to calculate variance. Addition- cession by MacMahon (1979), MacMahon and ally, log transformed values of mean annual Schimpf (1980), and MacMahon and Wagner (in precipitation (+ 1 mm to remove zero values) press), but these should not be mistaken for were used to calculate variance, which rep- directional changes in desert species corn- resents a measure of intrinsic variability postion (e.g., Shreve and Hinckley, 1937). (Lewontin, 1966). All sites, with their To test the precipitation predictability arbitrary biome designations, were plotted hypothesis, Smithsonian world weather on graphs of variance versus mean annual records (Clayton, 1944; Clayton and Clayton, rainfall (Fig. 4). Since there are no 1947) were used to calculate mean annual differences in log transformed or nontrans- precipitation and temperature for a variety formed data, I present only one data set. of localities, as well as to calculate the The shape of the curve, the lack of data coefficient of variation of mean annual scatter, and clarity of the breakpoint are precipitation. All localities were plotted striking. More striking is that the biome on the background of a hypothetical, two- types (desert and tundra) implied to lack axis world biome graph (Fig. 3). From the obvious succession group together on the position of that weather station on the ascending arm of the graph. Those biomes biome graph, a biome name was assigned to exhibiting conspicuous succession fall on each locality. Half of the weather stations the horizontal arm. used were checked for appropriateness of the

C-) 0 U

U 0 U H

0 1Q00 2000 3000 4000 5000 PRECIPITATION (mm)

Figure 3. Plot of weather data (taken from Clayton, 1944; Clayton and Clayton, 1947) from various world localities on an overlay of biome limits (adpated from Whittaker, 1975, P. 167). D = desert; F = deciduous forest; T = tropical rain forest; G = grassland; C coniferous forest; A = tundra. 32 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

I suggest that this separation, based (Peterson, 1978), as do some relatively more on unpredictability of the annual precipita- mesic desert sites. I predict that the tion, is in fact the cause and effect arrangement of such sites on Figure 4 would relationship explaining the conspicuousness place those of most conspicuous succession of succession. Thus, there are limits to closer to the origin and those of least the number of species, plants in this case, conspicuous succession farther up on the that can withstand the combination of low ascending arm of precipitation variance. and unpredictable water, and that these The overlap of the precipitation variance species, in the general sense, succeed them- of some tundra Sites with other biome types selves. The environment is never suffi- implies that some tundra sites should show ciently moderated by the effects of organ- equally conspicuous species changes--not isms to permit a new biota, adapted to the necessarily physiognomically obvious. changed environment, to become established. Additionally, the areal extent of distur- Conversely, in favorable invariate environ- bance and the presence of certain toxic ments (equable) more species can "make it" compounds may also alter successional dynam- and temporal turnover of species, each ics and enhance autosuccession. At the adapted to narrow subsets of the changing level of a global pattern, precipitation environment, is to be expected. Thus, represents a surprisingly good fit and succession of species will be more obvious. offers a first approximation of how conspic- The unpredictability and lack of pre- uous succession might be expected to be. cipitation are not the only factors deter- Succession is likely to be most ob- mining the conspicuousness of succession. vious where sites have environments with For tundra sites, temperature extremes may two characteristics. First, the difference also limit succession in some areas. Some between early and late succession environ- tundra sites show successional trends ments, in this sense the abiotic factors,

0.50

0.40

F- 0 0 o(9 0.30 -J

0LL 0.20 z

> 0.10

T IRIIIJ 0 1Q00 2000 3000 4000 5000 PRECIPITATION (mm)

Figure 4. A plot of the variance, the log of mean annual precipitation versus mean annual precipitation. See Figure 3 for data and biome designations. J. A. MacMAHON 33

must be great. Secondly, all of the en- located on the prairie-forest bor- vironments along the sere must be benign der (Illinois), arrived at dia- for organisms. These two conditions pre- metrically opposed views. These sent ideal conditions for species turnover. were substantially retained by Acceptable environments permit or even both men, in spite of subsequent foster high species diversity and a high extensive experience in diverse degree of change (early to late succession) areas. Is there an imprinting selects Out a continuously changing mix of phenomenon in ecologists?" species over the time axis. (McIntosh, 1975) Thus, deserts or tundra, with their harsh environments, are so dominated by This is a particularly important con- abiotic factors that the "reaction" effects sideration because many of the "synthetic" of the biota on the environments are minor attempts to predict trends in specific and relatively little environmental change attributes of seral ecosystems are undoubt- occurs. Add to this the limited number of edly attempts drawing on a body of litera- adapted species and succession is not ture biased toward temperate forest areas. conspicuous. In contrast, the tropical Of the attempts at a synthesis directed situation is such that the environmental to changes in communities over successional differences between a clearing and a closed time, by far the most widely quoted work is canopy are great, yet the differences are a seminual paper by E. P. Odum (1969). contained within the context of an equable Collating results from his own experiences environment so that the species turnover and drawing on the information of Margalef rate is great and rapid. This same relation, (l963a, 1963b, 1968), Odum postulated the steepness of the environmental gradient changes in 24 ecosystems attributes which from openings to canopy coverage, has been might be expected during succession from proposed as a factor accounting for enhanced the "developmental" to "mature" stages species diversity in tropical ecosystems (Table 1). (Ricklefs, 1977). Many workers have failed to recognize that Odum, in fact, was attempting to demon- strate a parallel between a "model for eco- CHANGES IN SPECIFIC PLOTS system development" and "development of DURING SUCCESSION human society itself." I shall not discuss those parallels here; rather, on the basis The biotic changes which occur on any of recent data, I will attempt to assess plot of ground during succession have been some of Odum's ecosystem predictions and, the topic of literally hundreds of scientific perhaps more importantly, show problems articles since the turn of the century. with some predictions in terms of their Workers have documented changes occurring verifiability. during primary succession (e.g., on granite It is instructive to reread Odum's outcrops -- Burbank and Platt, 1964), but exact words, describing his view of suc- more commonly those changes associated with cession at the time he wrote the paper. secondary succession are detailed. Of par- ticular significance in the American litera- "Ecological succession may be de- ture are the studies of two seres, one com- fined in terms of the following mencing with a fallow field (old field) three parameters (i) It is an order- which progresses to a forest-dominated ly process of community development climax, the other a prairie sere. I infer that is reasonably directional and, that such changes involve ecosystems therefore, predictable. (ii) It (MacMahon et al., 1978). results from modification of the Much of the history of the concept of physical environment by the com- succession, and perhaps even the basis of munity; that is, succession is some divergent interpretations of the pro- community-controlled even though cesses involved, may be attributable to the the physical environment deter- ecology of the ecologists, rather than to mines the pattern, the rate of the processes themselves (Sears, 1956; change, and often sets limits as McIntosh, 1975). The vast difference be- to how far development can go. tween Clements and Gleason may represent (iii) It culminates in a stabil- such an experimental bias: ized ecosystem in which maximum biomass (or high information con- "It is tempting to speculate tent) and symbiotic function be- how Clements' views may have been tween organisms are maintained formed by his location, early in per unit of available energy flow. his career, near the center of the In a word, the 'strategy' of suc- grassland (Nebraska), while Gleason, cession as a short-term process is 34 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Table 1. A tabular model of ecological SucceSSion:expected trends in the development of ecosystems.1

Developmental Ecosystem attributes stages Mature stages

Community energetics

1. Gross production/coimnunity Greater or less Approaches 1 respiration (P/R ratio) than 1 2. Gross production/standing crop High Low biomass (P/B ratio) 3. Biomass supported unit energy Low High flow (B/E ratio) 4. Net community production (yield) High Low 5. Food chains Linear, predom- Weblike, predom- inantly grazing inantly detritus

Community structure

6. Total organic matter Small Large 7. Inorganic nutrients Extrabiotic Intrabiotic 8. Species diversity--variety component Low High 9. Species diversity--equitability Low High component 10. Biochemical diversity Low High 11. Stratification and spatial Poorly organized Well organized heterogeneity (pattern diversity)

Life history

12. Niche specialization Broad Narrow 13. Size of organism Small Large 14. Life cycles Short, simple Long, complex

Nutrient cycling

15. Mineral cycles Open Closed 16. Nutrient exchange rate, between Rapid Slow organisms and environment 17. Role of detritus in nutrient Unimportant Important regeneration

Selection pressure

18. Growth form For rapid growth For feedback control ("r- selection!) ("K-select ion") 19. Production Quantity Quality

Overall homeostasis

20. Internal symbiosis Undeveloped Developed 21. Nutrient conservation Poor Good 22. Stability (resistance to external Poor Good perturbations) 23. Entropy High Low 24. Information Low High

1Taken from Odum, 1969, by permission. J. A. MacMAHON 35

basically the same as the 'strate- Community Energetics gy' of long-term evolutionary development of the biosphere-- Odum divided his 24 ecosystem attri- namely, increased control of, or butes into six somewhat related groups homeostasis with, the physical (Table 1). The first group Community environment in the sense of energetics -- seems easy to test. While our achieving maximum protection from analyses are not complete, the general re- its perturbations. sults suggest that we accept Odum's predic- tion for animals, at least the vertebrates, superorganism leanings are clear in and reject them for the plants (Fig. 5). the above statement. This specific case of conflicting tendencies, One or another of Odum's postulates i.e., whether to accept or reject the hypo- have been criticized for specific taxa by theses, will be used to elucidate a problem various workers. General reviews of the of Odum's, as well as many other authors', model suggest that many of the predicted ecosystem-wide hypotheses. ecosystem trends are the result of the Since most vertebrates are relatively "passage of time rather than of internal small and not embedded in the substrate, control" (Connell and Slatyer, 1977). See they are tractable research subjects and general critiques in Drury and Nisbet have been used for numerous laboratory and (1973), Colinvaux (1973), Horn (1974), and field studies of their metabolism and move- Mellinger and McNaughton (1975). A myriad ments. Thus, for bioenergetics topics we of studies have demonstrated excellent can make good approximations of values agreement with many of Odum's predictions necessary to calculate production/respira- for some components of some ecosystems, but tion, production/biomass, biomass/growth herein lies part of the confusion concerning ratios, and even yield. In fact, for most the robustness of Odum's postulates. There vertebrates we can guess tissue caloric is precious little data including both content or resting metabolism for an unknown plants and animals from one sere or even a species more accurately than we can measure broad taxocene considered over a variety of field population densities for common seres which is directed to testing the species. Aboveground plant parts are like- model. This is even true of the extremely wise relatively amenable to study because careful and significant Hubbard Brook eco- they are sessile and generally accessible. system studies (Bormann and Likens, 1979), The belowground component is much less which challenge Odum mainly on the basis of tractable and generally represents anywhere plant data. A partial exception is the from one-sixth (trees) to nine times (some work of Hurd and others (1971). desert shrubs) the biomass of the above- A group of workers at Utah State Uni- ground parts. Additionally, we have few versity has been attempting over the last respiration data for the whole tree on any five years to meld animal and plant data species. from a subalpine forest sere in northern The size, habitat, and numerical abun- Utah to address Odum's postulates in a co- dance of causes a problem ordinated way, using a site which shows the because many of them are soil forms that are classic species replacement chronosequence. difficult to sample and difficult to know in This is not the place to present all of the regard to critical aspects of their natural data generated from this program. However, --data which are required for some preliminary results, gleaned from my energetics analyses such as foods, feeding various colleagues, seem especially appro- rates, and reproductive rates. The result priate to the topic of this symposium. of these problems is that ecologists' I will discuss some of Odum's postu- assessment of successional community ener- lates, not so much to accept or reject them getics is biased toward aboveground plant at this time, but to comment on problems parts and vertebrates, especially birds and associated with an ecosystem approach to the mammals. This problem is demonstrated in postulates. The details of the sites our own work by the lag in filling in studied, the sere(s) involved in developing Figure 5 for invertebrates and some plant to Engelmann spruce forests in northern components. None of this is to overlook Utah, and the relation of northern Utah to many studies of invertebrates of various the subalpine Rocky Mountains are contained seres, including classics such as Shelford in Schimpf and others (1980, in press). (1912) or recent studies of adaptive syn- dromes of species as related to succession (Cates and Orians, 1975; Duffey, 1978; Hurd and others, 1971; and Otte, 1975). Even when dismissing all of the above data problems, the present results are still troublesome. The vertebrates (we have only 36 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

, e e ( ( -fl' Th e a a N a a - a N N a 'b ':- ( a a N N a a -' a b e' - 0 a 0N . . - ,,$_ - ,, o '- ATTRIBUTE:

Commun i ±y Energet i Cs R R N N N A A A A P/R Ra±ii approaches 1 N N N A A A A A P/B Ra±i decreases A A A B/E Ra±i increases A R R A A A A Yield decreases Commun ±y Structure R A A A R R R A Organicla±±er increases

Species Ji vers i R R R A A A A A A A Var increases R R P R R R R A R R R EquLability increases Life History R R R R R R A R Size ofJrganism increases Selection Pressure A R Growth Form r4K

Figure 5. A status report of an assessment of some of Odum's (1969) ecosystem attribute changes during succession. R = data suggest rejection of postulate; A = accept; N = not applicable; blank means data as yet are too incomplete to hazard an opinion.Notice that those categories across the top of the figure in parentheses are summaries of various groups to their left. For columns, B.G. = belowground; A.G. = aboveground; The abbreviations in the attribute column are: P = total photosynthesis; R total corn- munity respiration; B = biomass; E = energy flow, approximated here by growth.

birds and mammals on our plots), essentially How does one integrate the data obtain- without exception, follow the postulated ed from various diverse taxocenes to test trends of ecosystem energetics (Figs. 6 and the postulates? If the majority of species 7) as mentioned. But they represent a fit the supposed trends, shall the hypo- small portion of the total ecosystem com- theses be accepted? If so, Odum's postu- plement, and they Tlhandle,tt as a group, lates are correct for our site, i.e., most only a few percent and seldom more than 15 species, in this case, animals, follow the percent of the Net Annual Primary Production trends. Or does one accept or reject the (see Andersen et al., 1980, in press). On postulates on the basis of the energetically the other hand, trees continue to have P/R dominant organism, the plants, in which case (total photosynthesis/ecosystem respiration) we would reject the propositions? ratios greater than 1; yield does not de- While a modeling approach might be of value in this area of study, we must find crease in our oldest stands ( 300 years), nor in 1,000-year-old conifer stands in the less expensive and less data-demanding more favorable climate of the Pacific methods to assess the postulates, i.e., a Northwest of the United States (Waring and type of benchmark measure which would sug- Franklin, 1979; see also Franklin else- gest ecosystem-wide status. For most pro- where in this book). This is indirectly cesses these are not yet available, but shown for our site by the lack of an asymp- clearly some interesting, and perhaps sug- gestive, diagnostic measurements are now tote to the litter/duff accumulation data available (see Waring elsewhere in this sym- (Fig. 8) and continuously increasing (albeit posium for a summary of some creative uses at a lower rate) leaf production inUmatureT? of tree cores and their ecosystem-oriented spruce stands (Fig. 9). interpretation). U. A. MacMAHON 37

.02

0 03

02 P/B (kcal/g)

5 B/El 0 2.4

3

M A F S M F S

Figure 6. Changes in the mammalian component along a spruce-fir sere in northern Utah (M = meadow; A = aspen; F = fir; S = spruce; B = biomass). Total energy flow (E) = secondary production (P) plus respiration (R). Solid lines and circles represent 1976; broken lines and open circles, 1977 (taken from Andersen et al., 1980, in press).

Community Structure sonal problems, the year-to-year variations in many of these same attributes add addi- The postulates about community struc- tional complexity. ture (Table 1) have a mixed acceptance- All of the above comments can be made rejection record also. Again, addressing for what appear to be straightforward mea- particular taxocenes we caa calculate surements, such as total organic matter. species diversity metrics for variety or Clearly the dominance of trees in the equitability components. Here, we find "climax" provides more grams of organic additional problems. While we have cal- matter in later stages, and thus one accepts culated a diversity measure (H') that fol- Odum's postulates on the basis of accumula- lows predicted trends for mammals tion of the inedible plant parts, i.e., (Fig. 10), we had to make certain simplify- bole bionass. For other plants (Fig. l3A) ing assumptions. It is difficult to pick or animals (e.g., birds, Fig. 14), seasonal one population density (number per area) and and yearly changes in the system components one species density (species per area) value make calculation of "averages" difficult. to calculate an integrated seral stage di- While ecosystem-wide data for various versity. The problem rests with the taxocenes, collected intensively over time extreme seasonal flux in measures of diver- and space, are difficult to integrate into sity (e.g., insects, Fig. 11) or diversity single representative metrics, the data are components (e.g., insect richness, Fig. 12) valuable for considering some hypotheses. where taxocenes of seral stages do not For example, on our site 1976-1977 was a maintain the same position relative to one "drought" year ( a 90 cm maximum snowpack another. For example, in our study insect depth) as compared to either 1975-76 or and plant diversity of aspen as compared to 1977-78 (220 cm). During the drought year meadow seral stages switch seasonally as to bird species density (not species composi- which stages contain the higher diversity, tion) and integrated daily biomass (Fig. 14) or particular diversity components (Figs. remained more constant in fir and spruce 11, 12, and l3B). In addition to the - seral stages compared to meadow or aspen. 38 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

0.

U- 75000 D 0 50000

U- 25000 0 -U

0 0 00 200 300 TIME SINCE MEADOW (year5) C Figure 8. Total organic matter (kg/ha) in b. form of litter and duff contributed by 0.121 trees to spruce-fir successional stages in a spruce-fir sere in northern Utah. Triangles = aspen stage; squares = fir 0.09 plots; open circles = spruce plots (data provided by J. Henderson, G. Zimmerman, and S. Williams). 0.06

200 'S., 0.03

0 50 500 2.0 C. B/E 76 E C' m m

1.5 (I-) I- 0 m LU I000 L) 1.0

Ui 3

50

(-'I M A F S

Figure 7. Annual energetics relationships for the avian communities in each seral M A F S stage of a spruce-fir sere in northern Utah for 1968 through 1978 as calculated by a Figure 9. Production (g/m2) of herbaceous modification (Innis and Wiens, 1977) of the vegetation and tree leaves (aspen, sub- bird energetics model of Wiens and Innis alpine fir, and Engelrnann spruce) along a (1974). a. Total annual secondary pro- subalpine spruce-fir sere in northern Utah. duction divided by total annual respiration M = meadow stage; A = aspen; F = fir; S = b. Total annual production divided by spruce. Data are for 1977 field season. total annual biomass present. c. Total Triangles = tree leaves; open circles = annual biomasa present divided by total herbaceous vegetation (data from N. West, production plus respiration ("energy flow" G. Reese, and J. Henderson). of Odum, 1971). Note the general decrease in a and b and the general increase in c (data from Smith and MacMahon, mans, sub- mitted). See Figure 6 for abbreviations. J. A. MacMAHON 39

HE 50

40 Io -

O.5-

7 JUN JUL AUG SEP (1) 1977

Figure 12. Insect species (X no./m2) in the M A F S herbaceous vegetation layer throughout the 1977 sampling period. Trend lines fitted SERAL STAGE by eye: A = two aspen replicates (A) and (o ); M = meadow (. ); SF = conifers (0). Figure 10. Changes in diversity and rich- ness of herbivorous mammals between seral stages. General diversity is measured as 80 the Shannon-Wiener index, H'(closed MEADOW circles), with equitability measures as J' ASPEN (open circles). Richness is represented by '60 the heavy line. Data are for 1976 and 1977 (data from Andersen et a]., submitted). 40

1.5 20

H- CEF

0 50 100 150 200 1.0 DAYS SINCE SNOW MELTIN MEADOW M

>- H- SF 15 (1) 0 U) U) a 0. H- U) D10 D

0.0 JUN JUL AUG SEP 1977 H--

Figure 11. Mean Shannon diversity index O 0 50 100 150 200 H'/m2 for insects of the herbaceous vegeta- DAYS SINCE SNOW MELT IN MEADOW tion layer during the 1977 sampling period. Trend lines fitted by eye: A = two aspen replicates (A) and (o ); M = meadow ( ); Figure 13. Seasonal changes in the daily SF conifers (0 ). standing crop (A) and (B) of the herbaceous vegetation of four stages of a spruce-fir sere in northern Utah For 1977 (data provided by G. Reese and N. West). 40 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

0.061 MEADOW

0.04

S

0.04

0.04

[SWSIS

Figure 14. Daily amount of avian biomass(g/m2) present in each seralstage for 1976 through 1978 as calculated by a bird energetics model (Innis and Wiens, 1977) - The meadow is signi- ficantly different from the other stages in all years, and the meadows significantly different from both the fir and the spruce in 1977 and 1978 (Smith andMacMahon, in prep.).

The same was true for mammals. It is per- "stable" forest is changing its plant haps a better natural test of "climax' eco- species composition by significant percent-- system stability than some artificial per- ages yearly. For example, Holland (1978) turbations. Thus we might accept, on this found that while species density per quad- narrow criterion and for these specific rat remained the same in two hardwood for- taxa, Odum's postulate about increasing est study sites, there was a 20 percent and stability through the sere Other taxa, 14 percent species replacement or turnover other perturbation types, and other criteria over an eight-year period. Even over rela- of stability might lead to different conclu-- tively short periods, tree species are re- sions. Hurd and others (1971) found increas- placed, but the "forest" and the associated ing species diversity (approximating a seral illusion of stability remains. See for difference) but found that trophic levels example Forcier's (1975) climax microsuc- varied in their stability response to pertur- cession of Acer saccharum, Fagus grandi- bation, in this case a fertilizer augmentation folia, and Betula allegheniensis and Fox's Hypotheses about organic matter in- (1977) data on tree species alternation and creasing with time, when based on trees coexistence. Most species in an ecosystem (as are most succession studies), are un- are varying widely, season to season, year interesting. We should readily admit that to year, each responding, often independent- organic matter will increase if a plant is ly, to the vagaries of a somewhat unpre- long-lived, inedible, and continues to dictable world. It is clear to most grow. In fact, it is the organic matter ecologists that the vegetation we see may not persistence, in the form of standing trees, be adapted to the environnent we measure. that has deluded us into believing that the For example, current conditions may not per- climax is an equilibrium state. Part of mit reproduction, merely persistence of the "stability" is illusory. That is, the resilient adults until their death and re- 3. A. MacMAHON 41

placement by other species. Such persis- by Vitousek and Reiners (1975) and for tence, or as Gorham (1957) termed it, "bio- several of the postulates by Bormann and logical inertia," causes time lags in eco- Likens (1979) (see also Whittaker, 1975b). system change which confound ecologists' analyses. A confounding relationship is that between size and (see Other Trends Fig.1 in Bonner, 1965), i.e., larger species, animal or plant, have longer gen- In addition to postulates concerning eration times. Thus the largest, most ob- community structure and flows of matter and vious members of a biota take longer to energy, Odum also posits (Table 1) about develop and turn over, while the smaller, adaptive aspects of life histories, changes often more numerous, less abundant forms in selection pressures, and a catchall may be turning over yearly or even during termed "overall homeostasis." Since 1969 shorter time intervals (e.g., microbes). knowledge of "r" and "K" selection strate- The actual variation of species composition gies has burgeoned to the point where a shifts will be discussed later. simple two-ended continuum of selection The above discussion points out the strategies seems inappropriate either problem of addressing some of Odum's postu- empirically (Grime, 1977, 1979; Whittaker, lates; others are equally difficult to l975b; Wilbur et al., 1974), or even in the demonstrate. In many cases, it "all depends theoretical sense, as in the outcome of a on exactly what you mean.T' And what Is computer simulation (Whittaker and Goodman, "meant" varies from worker to worker. 1979). Similar caveats can be made to Examples of these problems of interpretation, some extent about other attribute changes. i.e., the lack of specificity in the ori- In addition to our reinterpretation ginal model, are given for nutrient cycles and expansion of the "r" and "K" life

1 00 FIR ASPEN SPRUCE-FIR

0 F- 10 E C) C) SW.' C) a- 0 0 C)

(0 o I 0.001 0 F- 1 z -C uJ I ME (0 C) 1-1 0.0001 w -i FIR 0_ -1

[SWSIII.I.1

I SPECIES SEQUENCE SPECIES SEQUENCE Figure 15. Dominance-diversity curves for herbaceous species along the subalpine sere. Figure 16. Dominance-diversity curves for Log of mean daily aboveground standing crop plant species along the subalpine ere. for each species is plotted against des- Log of proportion of total plot primary cending species sequence (data courtesy of production (tree leaves plus herbaceous G. Reese). shoots) for each species is plotted against descending species sequence (data courtesy of C. Reese, J. A. Henderson, and S. Williams). 42FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Table 2. A. Number of species within each successional stage of a subalpine spruce- fir sere, adapted for various types of dispersal. (Data from D. Schirapf).

B. Number of non-anemophilous species within each seral stage in four categories of flower color. (Data from a subalpine, spruce-fir sere in northern Utah, provided by B. Schimpf and R. Bayn).

A. Dispersal adaptation types Meadow Aspen Spruce-fir

Animal 4 6 5

Wind 6 6 8

Other 15 10 10

= 1.99, n.s.

B. Flower color Meadow Aspen Spruce-fir

Red, orange, or pink 6 2 0

Yellow 7 7 7

Blue or purple 4 3 1

White 6 6 12

= .05 < P < .10

history strategy concepts, some other very There are also interesting trends (per- interesting successional trends in life haps local, perhaps more general) in attri- history traits have been suggested. For butes of taxocenes within seral ecosystems. example, the rather standard species rank- Some authors have suggested a succession dominance curves are turning out to be in- from wind-dispersed to animal-dispersed teresting in the context of succession. plants (Dansereau and Lems, 1957). While Whittaker (1975a), Bazzaz (1975), McNaughton this may be true for other systems, we could and Wolf (1973), and May (1976) all point find no such trend in our data (Table 2A). out how such curves move to the right over On the other hand, we found a significant successional time. An example of this from increase in white flowers and a concomitant our own data shows the shift where domin- decrease in reds and blues along the sere ance is measured as standing crop (Fig. 15), (Table 2B). This correlation adds to the but less so when dominance is measured as growing body of data relating floral colors percentage of annual production (Fig. 16). to ecosystem characteristics (Daubenmire, Such trends seem generally true even though 1975; Moldenke, 1976; del Moral and Stand- various forest types, including tropical ley, 1979; Oster and Harper, 1978). wet forests, have different curves. The Recently, a general model relating difference among forest types, moving from plant strategies to vegetation processes less equable temperate montane forests to has been proposed and elaborated upon tropical wet forests, parallels the shift (Grime, 1977, 1979). In addition to many (see Fig. 8 in Hubbell, 1979). This quanti- other vegetation processes, this model des- tative difference does not negate the cribes the changes expected on a plot of qualitative similarity of dominance-diver- ground during succession. The crux of sity patterns in a variety of ecosystems. Grime's approach is that one can classify J. A. MacMAHON 43

the strategies of vascular plants on the average rates) early in succession may very basis of the "intensity of disturbance" of well be related to their lack of adaptation the environment and the "intensity of to stress. Thus, other forms are more ob- stress." Stress in this context ". .. con- vious until the trees are repressed in the sists of conditions that restrict produc- relatively more equable environments of tion... ," while disturbance ". .. is associ- later succession. When individual trees ated with the partial or total destruction occur as early successional species, they of plant biomass. . ." (Grime, 1977). Grime differ in many ways including morphogenesis sets up a two-by-two matrix, representing (Marks, 1975) from the same species in the two levels of each factor. Grime terms the climax. This is not inconsistent with low-stress, low-disturbance strategies Grime's approach, merely an addition of "competitive"; the low-disturbance, high- detail. While Grime formalizes the role of stress strategies "stress tolerant"; and stress, Woodwell (1970) clearly approaches the low-stress, high-disturbance strategies the relationships of woody plants to stress "ruderal." For the strategy of high stress gradients in a way that is compatible with and high disturbance, there appear to be no Grime's original model (1977), but is over- viable strategies. looked in that article and the subsequent Grime suggests that the three strategy book (1979). I will develop my approach to types are the result of selection pressures Grime's general model later in this paper. favoring these strategies. Using the short- It is clear that some predictable hand "C," "S," and "R" for the three axes changes in vegetation and animals occur on of a triangle, Grime (1977, 1979) shows in some plots of ground following disturbances. a series of graphs, the positions where his Our ability to predict exact species series data suggest various plant types should and proportions of each species through time cluster. Figure 17 depicts, in a summary is not good. In fact, I believe there are manner, where various types of plants might reasons to doubt that we will ever be able fit onto such triangular graphs. to do this very precisely. On the other Grime also suggests a possible path of hand, the biological characteristics of the vegetation succession under different condi- sequence of organisms must fit within the tions of potential productivity (Fig. l8B). constraints of the environment and the A plot of data from our studies (Fig. l8A) environmental changes occurring over suc- does not show clear-cut vectors. Rather, cessional time. Insofar as these changes our data suggest that early successional of environment are predictable and direc- stages ("M's" representing the meadow seral stage) show a broad suite of strategies represented by the vascular plants present, and that as succession proceeds there is a contraction of the spectrum of adaptive suites present. These data should not be I I,- \ taken as a critical test of Grime's model; 1/ however, they suggest some alternative in- \ô terpretations, consistent with existing r literature. A reasonable interpretation is that I_-s after moderate disturbance at many sites, the environment is acceptable for the estab- lishment of a variety of plants, represent- ing various adaptive suites. As time passes, and the environment changes as a // \ \ .... result of biotically mediated alterations, 1.1 / \ I 11 / liChen nual only a subset of the original spectrum of / ) brophytes )'.herbs adaptive suites are viable. Thus, there is 7... ) \ .... / an apparent contraction of the successful .. plant types occurring on a plot. A point STRESS similar to this was made by Drury and Nisbet (1973), who summarize data suggesting that many species, even climax forms, establish Figure 17.A nijdel, rrcdified from Grime early and are suppressed (not conspicuous) (1977, Fig. 3a-f), depicting the various until "climax" is approached. (See also the equilibria between competition, stress, and relay floristics vs. initial composition disturbance in vegetation.Axes are the arguments of Egler, 1954.) percentage of each strategy.Plant "life When trees are part of the climax, form" positions are approximated from their suppression (inability to establish or Grime's specific point data for a large ability to establish but grow only at below number of species. 44 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

A tional, so also will be the biological characteristics of the component organisms, without regard to their taxonomy. Details of this proposition (shown in Fig. 21) will be discussed later.

MECHANISM

The causes of succession, or the under- lying mechanisms related to the change of species composition of the biota, and/or physiognomy of a plot of ground, have been variously interpreted. Among ecologists, succession is variously thought to be allo- genic or autogenic in its controls, pre- dictable or unpredictable in its conse- quences, and an important scientific theory or a phenomenon of no value to generalized STRESS ecological thinking. Amazingly, Clements' (1916) idea that I-' the mechanism-producing success ion was com- posed of six processes has been accepted by some workers to the present time, despite much contrary data (Colinvaux, 1973; Connell, 1972; Drury and Nisbet, 1973; Egler, 1954; Gleason, 1917, 1939; Horn, 1974; McCormick, 1968; Niering and Goodwin, 1974). Clements' (see 1916, 1928 for details) view was that first an area was opened to invasion (nuda- tion process). If the substrate had not been occupied before, this was called pri- mary succession; previously occupied sub- strates underwent secondary succession. Once opened, an area was invaded by the propagules of species (migration process). He also clearly states the role of propa- gules remaining after the disturbance, entities I term "residuals." The migrants, being a somewhat random assortment of species proximate to the opened site, had to survive the conditions of that site, i.e., establish and grow (ecesis process). Re- Figure 18. A. An attempt to place species from a subalpine sere in northern Utah on a sulting from the successful establishment graph representing Grime's (1977) model of and growth was an increase in the size and plant strategies. Data for exact positions number of plants leading to competition for of species were derived from the literature various resources (competition process). and from a questionnaire addressed to local All of the activities of plants up to this plant biologists familiar with the flora in point, including , had effects on the question. Positions are difficult to assign environment, which changed various abiotic on a three-axis graph, so data represent a parameters (reaction process), which in turn best attempt. M = meadow stage species; favored a different set of migrants and so A = aspen; F = fir; S = spruce. Lines en- on, in a mechanistic repetition of the processes until the species admixture was close only herbaceous species since the three trees (aspen, subalpine fir, and able to maintain itself (stabilization pro- The six processes des- Engelmann spruce) cluster near the apex of cess) as a climax. cribed were grouped into three phases of the triangle. succession: initiation, continuation, and B. Grime suggested paths of vegetation succession under high (S1) to low (S3) termination (Table 3). Clements' approach is so pervaded by potential productivity. The figure is orderliness and laced with parts appealing modified from Grime's (1977) Figure 4a. to biological intuition that it remains The size of plant biomass at each stage of represented, in essence, by one of the three succession is indicated by the size of models of succession recently proposed by circles. Connell and Slatyer (1977). One model they J. A. MacMAHON 45

Table 3. Clements' (1916) three major proposed strategies based on a number of phases and six basic processes of characteristics including morphological fea- succession. tures, resource allocation, phenology, and response to stress. While Grime reasoned from empirical data gathered from plants, a

1. Initiation recent theoretical exploration by Whittaker and Goodman (1979) produced essentially the Nudation same three strategies. Grime represents succession as a vector across a triangle Migration whose axes are degrees of his three strate- gies (Fig. 18b). Other approaches to suc- Ecesis cession emphasize adaptive strategies in one sense or another (Auclair and Goff, Reaction 1971; Bormann and Likens, 1979; McNaughton, 1974; Newell and Trainer, 1978; Pickett, 2. Continuation 1976; Pielou, 1966; Shafi and Yarranton, 1973; Tramer, 1975; Van Hulst, 1978). Competition Recently, in a very lucid presentation of the data obtained during the 15 produc- 3. Termination tive years of research at Hubbard Brook, Bormann and Likens (1979) presented their Stabilization view of the bases of successional change after clearcutting a northeastern hardwood forest. Their emphases on the importance of various factors in determining the course of succession is not much different recognize is the facilitation model, which from mine. I will include some of their is essentially the Clementsian approach cast points in my discussion rather than present in the context of the ecosystem by Odum a separate analysis of their data. (1969). The second (tolerance model) If one allows some "wobble" in appli- holds that succession leads to a community cability, one can represent succession, composed of those species most efficient in using recent wisdom, in a manner not unlike exploiting resources, presumably each Clements. Such an admission is particular- specialized on different kinds or propor- ly hard for me because I have frequently tions of resources" (Connell and Slatyer, declared myself a staunch Gleasonian (e.g., 1977; Connell, 1975). Finally, the inhibi- MacMahon, 1976, 1978). For this discussion, tion model simply states that "...no species assume that I am tracking through time the necessarily has competitive superiority over fate of a plot of ground, including the another. Whichever colonizes the site first whole ecosystem (biotic and abiotic com- holds it against all comers" (Conneil and ponents). Generally, I will write only Slatyer, 1977). In essence, this is site aboOt changes in the biota, especially preemption by species which have long-lived plants, despite inclusion of the substrate individuals or other biological character- in the model (Fig. 20). istics leading to persistence. Figure 19 The model (Fig. 20) looks at the depicts the Connell-Slatyer model. states S0 of the plot through time. It Recently, Born (1971, 1974, 1975, 1976) nust alwar be assumed that cycling can has represented succession as a Markovian occur back through a process, say S3-S1, replacement process. Generally, his approach ançl when that occurs a new state exists, is to assume tree by tree replacement as a S1, which I will not formally indicate. probability function of the stand composi- See the caption for Figure 20 for details tion, using linear models but also finding of notation. interesting nonlinearities. Horn is not the Since a system must have initial condi- only one to use this general approach, tions I start, arbitrarily, at a point though others have sometimes not explicitly where a plot has substrate available for stated the use of nonlinearities in the colonization (Se). In successional terms, past (Botkin et al., 1972; Leak, 1970; this original state is the beginning of MacArthur, 1958; Shugart et al., 1973; either primary or secondary succession. Waggoner and Stephens, 1970) nor apparently There is no qualitative difference among in the future (Van Hulst, 1978). I will plots which are to undergo primary as return to Horn's approach later. opposed to secondary succession except that Additional contributions to mechanisms secondary succession plots may contain of succession have involved reasoning about residuals, i.e., plant or animal propagules the role of life history strategies by (seeds, spores, bulbs, cysts) remaining Grime (1977), as described above. Grime's from the predisturbance period. There are system emphasizes the identification of his 46 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

similar residual effects on the chemical pagules. Since there are differences in the and physical properties of once-inhabited amount of viable seeds in different vegeta- sites. It would be hard to differentiate tion types (Thompson, 1978), the relative plots on a mobile sand dune, which were importance of these precursors may vary never vegetated (undergoing primary suc- geographically and altitudinally. The cession) from those undergoing revegetation. importance of the residuals is such that Thus, to my mind the subdivision into pri- Egler (1954) specifically referred to them mary and secondary succession serves no as the "initial floristic composition." useful purpose, except to define extreme They formed a critical part of his discus- situations. sion of succession mechanics, incorporated The importance of the residuals cannot successively into papers by McCormick (1968) be overemphasized; their effects on the plot and Drury and Nisbet (1973), all of which might completely determine the vector of the purport to deal with the mechanisms of suc- subsequent successional changes. The number cession. Residuals were pointed out as of buried viable propagules can be quite especially important at Hubbard Brook high. In northern Saskatchewan, Archibold (Bormann and Likens, 1979). (1979) found 456 propagules per square As the residuals survive (valve in meter; 87 percent of these were seeds and 13 Fig. 20), endure the environment (environ- percent were remnant roots or rhizomes that mental driver, E in Fig. 20), including the produced aerial shoots. Tree species subsequent disturbance of the plot (distur- accounted for 42.9 percent of the total pro- bance driver in Fig. 20), and have their

A disturbance opens a relatively large space, releasing resources - - 1- 1 I Of those species that arrive Of those species that arrfve in the In the open space, only certain open space, any that are able to I B "early succession" species can survive there as adults can stab- lish themselves. establhsh themselves. ------w-.p1 :..__-'w , I Early occupants modify the envi- Early occupants modify the envi- Early Occupants modify the rornt so that It becomes less ronment so that It becomes less environment so that It becomes I suitable for subsequent rec1i- suitable for subsequent recriTTi- less suitable for Subsequent C. ment of "early succession" ment ofearly succession' of both early and species but more suitable for species but this modification late succession species. recruitment T'late succession" has little or no effect on Sub- species. sequent recruitment of 'late succession" species. I' ------.' 12

The growth to maturity of juven- Juveniles of later succession As long as Individuals of earlier iles of later succession species species that invade or are al- colonists persist undamaged and! Is facilitated by the environ- ready present grow to maturity or continue to regenerate D.mental modifications produced despite the continued presence vegetatively, they exclude or by the early succession species. of healthy individuals of early suppress subsequent colonists of In time, earlier species are succession species. In time, all species. eliminated, earlier species are eliminated.

1 12 - 3 y This sequence continues until This sequence continues until resident species no longer no species exists that can Ethefacilitate the invasion and invade and grow in the presence growth of other species. of the resident.

,I I-At this stage, further invasion and/or growth to maturity can occur only when a resident individual15 damaged or killed, releasing space. Whether the species composition of this CommEunity continues to chanle Fdepends upon the conditions evisting at that site and on the characteristiLs of the species available as ref1 AremPntc

1.. :'; Figure 19. Three rrodels of the mechanisms producing the sequence of species in succession. The dashed lines represent interruptions of the process, in decreasing frequency in the order w, x, y, and z (taken from Connell and Slayter, 1977, by permission). J. A. MacMAHON 47

opening where a single tree has fallen. Such species have localized reservoirs form- ing a landscape mosaic, where each "patch" goes to extinction as the site develops. ON. RIVER) SURVI This approach is explicit in a review of the R RESIDUALS C POOL adaptive nature of seed size and shape (Baker, 1972; Harper et al., 1970) and oil content (Levin, 1974) and in the general theoretical discussion of mosaic phenomena by Whittaker and Levin (1977). E, R ECESIS Given a longer time, the larger, less vague propagules of other species stand a statistical chance of eventually getting to the open plot. Thus, if a late succession- al species is not proximate to the plot, it may not occur on that site until late in succession because late succession species have less vagile propagules and greater dependence on vegetation reproduction. However, if a late successional species does occur proximate to the plot, it may very well be present in early successional Figure 20. A model of the change in the stages, though not obvious because of slow- status of the components of a plot of ground er growth rates or even because its growth over time. Boxes are states of the plot at is initially suppressed by other species. any instant. Diamonds are system drivers. It is through this very phenomenon that the The circle is an intermediate variable. size of a disturbed area can affect suc- Dashed arrows show information flows. cession. If 100,000 ha are burned, tree Letters next to control gates replace dotted seeds may have less chance to be in the lines from that point to the control for the middle of that area until the plot is very sake of graphic simplicity. old. On the other hand if a one-quarter hectare gap is created in a forest canopy, effect on the plot (Reaction (R) in Fig. trees are much more likely to reoccupy that 20), they are joined by a series of migrants site rapidly, "shortening succession." from the available biotic pool. The exact The specific nature of the species nature of the events during this early occupying the plot during these early peri- period of succession determine the ultimate ods can determine the subsequent course of successional vector. Which species get to plot changes. A case in point is the signi- a particular plot depends on a number of ficant effect that pin cherry (Prunus factors. Perhaps the two most significant pemnsylvanica) has on early successional are the distances various species are from nutrient dynamics. The pin cherry acceler- the plots and the relative vagility of each ates canopy closure and, by serendipity, species' propagules. A species distant this protects the soil from nutrient loss from a disturbed plot without good dispersal (Bormarin and Likens, 1979; Marks, 1974). potential is not likely to be a part of Finally, the stochastic phenomenon of early succession. Conversely, highly vagile the timing of disturbance can alter the and proximate species are likely to esta- migration process. Say that an environ- blish rapidly when a plot is available, mental disturbance occurred in the fall of assuming none of their environmental what happened to be a good cone crop year tolerance axes are violated on that plot. for spruce or fir. The success of these Notice in Figure 20 that the process of two species at more rapidly occupying a migration is itself affected by both the disturbed site might be greater with more environmental driver and the reaction inter- seeds available than if the disturbance had mediate variable. occurred in a low seed crop year, or even The prevalence of annuals or herbaceous earlier in the year before the crop was perennials in early succession of plots in mature, and other species could preempt the many different vegetation types is partly plot before the tree propagules were mature. related to their small, numerous, readily Such site preemption can involve alielo- dispersed seeds. Also, at least a few in- chemics and shading out (Turner and Quarter- dividuals occur around the countryside, man, 1975). providing seed sources uniformly across the Ecesis and biotic interactions work landscape. An obvious example is the pre- simultaneously, but they are separated here sence of dandelions in the most out-of-the- for emphasis. Ecesis, as Clements (1916) way places, e.g., in a spruce-fir forest 48 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

said is the ". . .adjustment of a plant to a number of existing models attempt to do this new home." That is, as in the case of a by using various quantitative methods. vascular plant seed, an organism that reaches Interestingly, the forester's stand yield a particular plot must be able to germinate models are a form of successional prediction and grow before it can greatly influence the model, usually limited to a few commercial plot. Generally this is a matter of endur- species. Most extant models consider hard- ing the physical environment, though biotic wood forest succession; exceptions are those factors such as the presence of a species' examining the wet sclerophyll forests of required symbiont are also requisites. Tasmania (Noble and Slatyer, 1978) and red- Simultaneous, and of increasing importance woods (Bosch, 1971; Namkoong and Roberds, through the time an individual grows, are 1974). Frequently such models deal with its interactions with other individuals. single stand predictions, although Shugart This interaction can take any of the many and others (1973) discuss larger regions. forms of a species-species interaction, The most detailed model appears to be that ranging from predator-prey interactions to of Ek and Monserud (1974) which includes . Clements' term, and major mixed age, mixed species assemblages as well emphasis for this process, was competition. as spatial variation. Some of the models Obviously, biotic interactions other than track tree-by-tree replacements as a func- competition are important. tion of Markovian processes (Horn, 1976; The net result is that a particular Waggoner and Stephens, 1970), while others species will occur on the disturbed plot use a continuous approach (Shugart et al., until such time as the nature of the plot 1973). One recent approach even considers violates one or more of its tolerance axes. multiple pathways of succession (Cattelino The plot itself is constantly changing-- et al., 1970). even if the biota is the same, seldom does Most of these models have fair predic- the physical milieu remain the same. There tive power for trees in specific forest is also a constant barrage of propagules types. What is proposed here is a general reaching the plot that may change the biotic framework that should work for various character of the associations. Of course, vegetations in a variety of geographic each of these migrants cycles through the areas. The model, as I envision it, does same test of persistence. not require convergence of vegetation during The process of reaction, in which the succession to a single end point. In fact, occupying species change the nature of the its structure was designed to permit great plots--classically to a state where they variability since I believe convergence is themselves cannot survive--may or may not be partially an illusion (see a detailed true. McCormick's (1968) experiment where example in Matthews, 1979). removal of annuals had little effect on An important aspect of this model is perennials suggests a lack of important the constant possibility of additional dis- reaction effects. At the other extreme, the turbance causing a recycling of the pro- importance of reaction was probably most cesses. Such disturbances, if they are of forcefully presented by Phillips (1934, moderate intensity and spatial extent, are 1935a,b) and is shown for classic sand dune important in maintaining diversity. This succession by Olson (1958). Undoubtedly, effect of disturbance has often been noted this is a case of "it all depends" reflect- (Loucks, 1970; Mellinger and McNaughton, ing the nature of the disturbance and the 1975) but recently has been the topic of particular species and environment involved. increased theoretical interest (Huston, This position is similar to the one arrived 1979; Whittaker and Levin, 1977). at by Van Hulst (1978), who emphasizes species adaptive strategies. The model I present uses Changes on Other Time Scales basic processes (Table 3) , but its intel- lectual base is clearly in the Gleasonian The time scale of succession depends tradition. Thus, processes are undoubtedly, on the particular site involved. It is with some alteration, as Clements outlined determined by the nature, intensity, and them, but they are really working on the extent of the disturbance, the specific biota in a highly individualistic way. The environment, and other factors. In any superorganism approach is not necessary nor case, the time axis involved is moderately even appropriate in my view, regardless of long, i.e., tens to a few hundreds of years. various eloquent protestations (Williams Superimposed on this process is a series of et al., 1969; Morrison and Yarranton, 1974). minor (micro) successions where seasonal My model does not include the mathe- changes occur in plant composition or matics to describe the form of the functions phenological aspectation. Some animals involved for particular vegetation. A closely track such plant changes (for d. A. MacMAHOM 49

example, see the microsuccession described His comments best fit regional patterns; a for insects by Price, 1975). Thus, if we small plot analysis would, I believe, in- extend out observation to animals and variably show significant dynamic changes in microbes, we literally find successions all but the most persistent and resilient within succession all at different time forms. Trees are often exactly such forms. scales (Levandowsky and White, 1977). Fre- Another scale of ecosystem-time change quently, this involves a group of coadapted covers hundreds to thousands of years and species--a group similar to what Root (1973) is what we refer to as ecosystem evolution. termed "component communities." Addition- Whittaker and Woodwell (1972) in a previous ally, some changes in species composition colloquium and more recently Whittaker occur over a very few years. Examples are (1977) and Whittaker and Levin (1977) point the cyclic replacement of hardwoods, out that all species evolve in the context apparently related to contrasting reproduc- of the community and that the community is tive strategies (Forcier, 1975), the cases the result of a history of species additions of alternation described for forests by Fox and subtractions (extinctions for that site) (1977), and even cases known for desert as well as gene pool changes for resident species such as cacti (Opuntia) and shrubs species, in the context of the total envi- (Larrea) (Yeaton, 1978). ronment. This is qualitatively no differ- Some species turnovers presently appear ent from the kind of model I have been dis- to be caused by chance (Holland, 1978). cussing. If a particular species can get Other causes of turnovers include the loss to a plot, survive, and reproduce there, of a particular species due to pathogens or it will persist as part of that eco- a critical environmental factor. Such system. If the species cannot survive on "disturbances" are currently thought to pro- that plot under those specific conditions, vide the landscape mosaics of patches of it must either go extinct on the plot or varying sizes, which contribute to the produce differently adapted individuals. diversity and stability of regional vegeta- Many associations we see repeated tion (Loucks, 1970; Pickett, 1976; Vitousek across the landscape today are composed of and Reiners, 1975; Whittaker and Levin, individual species which have formed associ- 1977). In some cases, replacement of the ations relatively recently, after being lost species is accomplished by the expan- parts of quite different ecosystems during sion of one or more existing species into the Pleistocene. Excellent examples of the "gap." The replacement of chestnut this come from the data of Davis (1969, (Castanea dentata) by oak (Quercus borealis) 1976, 1978) for forest tree species which after chestnut extirpation by chestnut now form the very associations used as the blight (Endothia parasitica) is an example data base for much of successional theory. (Karban, 1978) which typifies a one-for-one These species have become associated by a replacement, while on other sites several process similar to succession. In the past mesic species seem to replace chestnut their distributions were altered by various (Good, 1968; Mackey and Sevic, 1973, and events. Former associates had slightly references therein) different tolerances. As there was remixing All of these changes can be super- of species, different combinations could get imposed on the same model offered for suc- to particular areas and survive there in cession (Fig. 20). Thus, for some reason moderate perpetuity, and therefore currently a species is lost or at least its popula- form the "climax" vegetation type. None of tions are reduced. Its physical or biotic this denies that certain species assemblages environments may no longer be suitable. It are more stable, less vulnerable to change is replaced wholly or in part by a species than others (Robinson, manuscript). which, if it is a recent arrival, starts at As a form of summary I will use an the beginning of the model, i.e., can get adaptation (Fig. 21) of Grime's model (Figs. there and survive in that milieu. The 17 and 18). Every group of organisms species itself may alter the environment exists in the milieu composed of biotic and such that other species will be replaced, abiotic factors. It cannot exist in a sit- but the whole process may be cycled in a uation where any of its axes of biotic or roughly predictable fashion. Species al- abiotic tolerances are consistently vio- ready resident on the plot may simply in- lated. Each place on the surface of the crease in abundance. Regionally, the biotic earth, for any time interval, has a charac- components may appear to be in equilibrium teristic environment. This immediately yet changes, qualitatively the same as those places a constraint on what organisms could ascribed to succession, are taking place possibly survive there, regardless of their constantly on a smaller scale. As Gleason ability to get there. Figure 21A shows (1927) said, succession does not end, it such a hypothetical limit. Many organisms just becomes too slow to measure or observe. may end up on a site, some not capable of 50 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

ru

E. F.

Figure 21. A depiction of several aspects of an ecosystem over time, using the life history strategy approach of Grime (1977). Axes of triangles are the same as in Figure 17. The sequence A-D represents succession where each environment can only be occupied by species exhibiting certain life history strategies (A). Since many species with various life history strategies, including those which cannot persist in a given environment, can get there, a time exists where the spectrum of species life histories exceeds the environmental con- straints (B). The nonadapted species cannot persist (C) and through time the species may interact to further reduce the spectrum of viable life history alternatives (D).E and F show that over short times, various life history strategies may become established, as long as they do not exceed environmental limits (ecosystem fluctuation). G and H show a change in life history strategies which can exist, one type of ecosystem evolution. J. A. MacMAHON 51 of existing there. Figure 2lB show a hypo- (Diamond, 1975) which fit thetical group of such organisms (the well into the general model proposed here lighter line) imposed on th limits of the (Fig. 20), though in many cases they repre- hypothetical environment. Only those or- sent specific instances of what I term ganism who can get to a place and survive biotic interactions. there can continue to exist there. Thus the Let me conclude with an analogy. non-survivors are eliminated (Fig. 21C). In While speaking about the universe recently, some cases not all members of a species can Dr. Philip Morrison reminded me that in survive the competition, or other biotic physics there is a dichotomy between New- interactions, or even the results of the ton's deterministic and Gibbs' stochastic reaction process. Thus, over time perhaps a approach to the universe. smaller species mix persists in that plot We regularly predict with great pre- (Fig. 2lD). This is essentially succession cision the exact timing of the orbits of via the model (Fig. 20). That some sites some celestial bodies (a high degree of are so harsh that the same group of species apparent determinism). On the contrary, we are the only ones capable of replacing them- cannot predict the of a particular selves is an extreme case of the same pro- gas molecule in a room, even though the cess; it is just one where the original same rules of motion and gravity apply to environmental constraints are so severe, both because, in a sense, the molecule is succession seems not to occur. A global affected by every in the universe example of the possible cause and effect re- (stochasticity). Nonetheless, we can des- lationship between the unpredictability of cribe the average behavior of that species precipitation in low precipitation systems, of molecule in that particular room, under regardless of temperature, was presented those specific conditions. earlier. Succession and other ecosystem changes During short time intervals there can seem of the same type. On a regional basis be changes in species composition of plots we can predict with fair accuracy the aver- (Figs. 2lE and F). These changes, often age change in the biota under certain con- caused by minor biotic or abiotic changes in ditions, but it is difficult, nearly impos- the plot, are still within the overall sible, to predict the exact behavior of any physical environmental constraints. Cyclic one very small plot for a short time period, or even stochastic composition changes are and even harder for a longer time period frequently of this type. where very many unpredictable changes might Finally, the major climatic or other occur. abiotic variables may change over time As with entities in the universe, intervals, changing the very nature of a different species in a plot are reacting plot, and now new species mixes might be with their own characteristic "periods" selected for, or extant species may adapt. (Levandowsky and White, 1977). Addition- This is essentially one form of ecosystem ally, while there is determinism involved evolution. For all of these situations we in the system, the stochastic properties of can conceive of biotic changes also affect- such systems force us to offer "average" ing these ultimate plot characteristics; it answers--correct when we generalize, but is merely easier to visualize the abiotic often incorrect when we attempt to be too variables over time by use of weather specific. A goal of ecologists must be to records. learn where between these two extremes we All ecosystem composition changes are need to focus our estimates of potential qualitatively similar, and can be envision- ecosystem behavior, so that man, the eco- ed, mechanistically, as being driven by the system manipulator, can trust our science. same processes--equally well understood long ago by two intellectual opponents--Gleason and Clements. Such modern ecological ACKNOWLEDGMENTS theories as island (MacArthur and Wilson, 1967) can be considered as being The members of the succession project qualitatively similar to the old "conven- at Utah State University were most helpful tional wisdom" couched in a modern context. and unselfish in sharing their data with For example, the island distance from the me. These include: Douglas Andersen, Jan sources of a biota, its area, and the dis- Henderson, George Innis, David Schimpf, persal characteristics of various species Michael Schwartz, Kimberly Smith, Gary determine, in part, the "migration" phase. Reese, and Neil West. These early species establish a biota which Robert Whittaker and Neil West kindly may change the environment of the island, read and commented on an early draft of the a reaction process. This can include alter- manuscript. My alter consciences Doug ing the invadability of that island. Such Andersen, Dave Schimpf, and Kim Smith beat ideas have even been formalized into 52 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS their way through several manuscript drafts Burbanck, M. P., and R. B. Platt. 1964. Linda Finchum and Bette Peitersen helped Granite outcrop communities of the prepare all drafts. Bob Bayn executed all Piedmont Plateau in Georgia. Ecology figures and reduced data ad nauseum. Of 45:292-306. course, all of us could do this because the National Science Foundation provided the Cates, R. G., and G. H. Orians. 1975. Suc- necessary funds. cessional status and the palatability of plants to generalized herbivores. Ecology 56:410-418. LITERATURE CITED Cattelino, P. J., I. R. Noble, R. 0. Andersen, D. C., J. A. MacMahon, and M. L. Slatyer, and S. R. Kessell. 1979. Wolfe. 1980. Herbivorous mammals Predicting the multiple pathways of along a montane sere: community struc- plant succession. Environ. Management ture and energetics. J. Mann. (in 3:41-50. press). 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Yeaton, R. I. 1978. A cyclical relation- ship between Larrea tridentata and Opuntia leptocaulis in the northern Chihuahuan Desert. J. Ecol. 66:651- 656. Distinctive Features of theNorthwestern Coniferous Forest: Development, Structure, and Function

Jerry F. Franklin and Richard H. Waring

INTRODUCTION and the extent and importance of in terrestrial and stream eco- The coniferous forests of the Pacific systems is outlined by Triska and Cromack Northwest, those found on the slopes of the (this volume). The nitrogen cycle has been Cascade and Coastal ranges of Oregon, the source of one unexpected discovery Washington, northern California, and British after another. Ten years ago no clear idea Columbia, are known throughout the world. existed of nitrogen sources in these f or- This is the region renowned for Douglas-fir ests; fixation by nonleguminous woody plants (Pseudotsuga menziesii) stands and western such as red alder hasbeen widely known red cedar/western hemlock (Thuja plicata/ only since the mid-195O's. Textbooks hypo- Tsuga heterophylla) climaxes. Surely these thesized that free-living blue-green algae forests, observed by foresters and botanists might be a source of nitrogen inputs along since the time of von Humboldt and Douglas, with precipitation. In the last decade at are well understood and can hold few sur- least two major sources of nitrogen have rises. Indeed, when the Coniferous Forest been identified: (1) the crown and ground Biome Project of the U.S. International dwelling lichens with a blue-green algal Biological Program (US/IBP) started more symbiont and (2) microbial activity in some than 10 years ago, we thought we knew about types of organic matter such as coarse woody all we needed to know about the natural f or- debris (logs). Almost certainly the nitro- ests of this region. The U.S. Forest Ser- gem cycle will be the source of many further vice had already reduced their studies of surprises. older forests in order to concentrate on Our objective in this paper is to high- younger stands. Biome program designers light some findings on the structure and seriously debated the wisdom of studying function of these coniferous forests. We natural, older forests when major questions also hope to transmit some sense of the seemed to revolve around managed stands. progress and exicting directions of current During the last 10 years, however, we research and stimulate you to reexamine have made gigantic advances in our knowledge what you think you already know about these of these forest ecosystems.We have learned forests. We will cover: (1) biomass and how they are structured, their functional productivity; (2) factors responsible for behavior, and controlling factors. Research evergreen dominance and massiveness; (3) on these systems has evolved into tests of successionally oriented studies of age specific hypotheses as relevant questions structure and coarse woody debris; and (4) have become apparent. Many results pre- aspects of the old-growth systems. sented in this and other Colloquim papers Several topics highlighted in this are from these first- and second-generation paper are discussed more thoroughly else- ecosystem studies--i.e., biomes and sons where in this volume (see Waring, Triska, and daughters of biomes! and Cromack on coarse woody debris, Swanson Increasing knowledge has brought con- on erosion, Carroll on tree canopy eco- tinual surprises---counterintuitive finds systems, and Cummins on stream ecosystems). that make clear how little we really know about these coniferous forests. The high productivity and rapid turnover found below- ground in forests, for example, is outlined by Harris and Santantonio (this volume),

59 60 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

BIOMASS AND PRODUCTIVITY with maximal biomass values from other regions of the world (Table I). The analy- Over the last decade scientists have sis of a redwood (Sequoia semper- documented what we have always suspected virens) stand in Humboldt State Park in about northwestern forests--they contain the California provides the greatest accumula- largest biomass accumulations in the world tion ever recorded, with a basal area of and are very productive. Trees have been 343 m2/ha and a stem biomass of 3,461 ton/ha dissected and equations developed and (Fujimori, 1977). Addition of branch, leaf, applied, and the results have shattered and, particularly, root biomass would in- many theories about forest maxima which crease the estimate of standing crop to well were based upon studies of temperate forests in excess of 4,000 ton/ha--very close to in other regions of the world. Fujimori's (1972) earlier estimate of 4,525 ton/ha for a coast redwood grove. These figures are larger but are cons1stent Biomas 5 with the biomass of 3,200 ton/ha reported by Westman and Whittaker (1975) for three Biomass accumulates to record levels in redwood stands on alluvial flats. Super- large, long-lived species from dense coni- lative stands are not confined to coast ferous forests. Maximal values in the redwood, however (Table 1); maximum values Pacific Northwest contrast most strongly

Table 1. Maximal biomass values for three coniferous forest types in the Pacific Northwest and comparable data for different forest formations elsewhere in the world.

Formation, type, and Total stand location Stem volume Basal area hiomass

3 2 m /ha m /ha mt/ha Coniferous forests, Pacific Northwest

1 Sequoia sempervirenS 4 (> 1,000 years old) 10,817 338 3,461

Pseudotsugamenziesii-2 Tsuga heterophylla 4 (450 years old) 3,600 127 1,590

Abies procera2 4 (325 years old) 4,106 147 1,562

Evergreen hardwood3 (Quercus cinnamomum in Nepal) n.a. n.a. 575

1eciduous hardwood3 (Quercus prinus in USA) n.a. n.a. 422

Temperateronifer3 (Tsuga sieboldii in Japan) n.a. n.a. 730

C:iifer 1 antaton3 (CrypLomeria japonica in Japan) n.a. n.a. 1,200

1..Fujimori,. 197,.-, 2Fuji:oriet al.,l916. Art and Marks. 1971.

4Ste mass cnlv. J.F. FRANKLIN & R. H. WARING 61

for noble fir (Abies procera) and Douglas- Item Biomass fir are about half those for redwood, but (ton/ha) they still greatly exceed maxima for temperate and tropical forests in other Foliage 12.4 parts of the world. The contrast is further emphasized by the fact that biomass figures Aboveground in living plants 718.0 for the Pacific Northwest (Table 1) include stem biomass only, while those from other Total in living plants 870.0 regions are for total biomass. Current studies in the Pacific North- In logs and standing dead trees 215.0 west continue to gather evidence that large biomass accumulations are the rule rather Total ecosystem organic matter 1,249.0 than the exception. Average values con- trast as greatly with those for other regions as the maximal values (Table 2). The amount of biomass in living trees is High values are characteristic of young quite remarkable, given the apparent de- (100 to 150 years old) as well as old cadence of the stand as evidenced by the Douglas-fir stands and of subalpine forests large weight of dead trees and logs. (noble fir) as well as temperate forests. One noteworthy biomass component is Coastal stands of young-growth Sitka spruce foliage. Leaf biomass and surface area in (Picea sitchensis) and western hemlock the Pacific Northwest develop slowly, tak- (Tsuga heterophylla) tend to be particular- ing 30 years or more to reach a maximum ly high (Table 2). One of the more exten- (Long and Turner, 1975); in the eastern sive analyses available is for a 10-ha United States and other temperate regions watershed in the Cascade Mountains of of the world, equilibrium is achieved much western Oregon (Grier and Logan, 1978): earlier, reportedly in as little as 4 years (Marks and Bormann, 1972). Projected canopy surface areas in the Pacific North- west typically reach 10 m2/m2 and may reach as much as 20 m2/m2, which is very close to the theoretical maximum (Gholz, 1979). Table 2.Biomass values in representative stands of various types.

Aboveground Number of biomass 1 Type and age class stands Average Range

mt/ha

Douglas- fir 70 to r70 years 10 604 422-792

Douglas-fir/western hemlock 250 to 1,000 years 19 868 317-1,423

Sitka spruce/western hemlock 121 to 130 years 3 1,163 916-1,492

Noble fir 130 years 1 880

Temperate deciduous forest Mature 19 243 87-422

Tropical rain forest Mature 9 318 67-415

'Seeappendix for data sources for stands from the Pacific Northwest which include aboveground tree biomass only; source for temperate deciduous and tropicalrain forests is Art and Marks (1971) and includes shrubs and herbs. 62 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Leaf mass values are also very high, with sites. Mature or old-growth stands have an average of nearly 20 tons/ha (Table 3). lower net productivities (Table 4). These leaf mass and projected area values Annual net productivity can be very are much higher than those in temperate great on the best sites. Fujimori (1971) deciduous hardwood and evergreen hardwood reported a net production of 36.2 ton/ha in stands. Values for temperate conifer a 26-year-old coastal stand of western hem- stands in other parts of the world range lock. Young forests of coast redwood also near the low values for coniferous forests have high early productivities on good sites Maximum values are in the Pacific Northwest (Table 3). Inter- (Fujimori, 1972, 1977). estingly, the values for leaf area and mass substantially lower for temperate deciduous in northwestern coniferous forests also far forests (24.1 ton/ha for tulip poplar, exceed leaf areas developed by red alder Liriodendron tulipifera) and temperate ever- (Alnus rubra), one of the most common and green hardwood forests (28.0 ton/ha) (Art productive of the northwestern deciduous and Marks, 1971). Conifer plantations, with hardwoods; values in red alder stands, con- a reported maximum of 29.1 ton/ha for verted from biomass values, represent less Cryptomeria japonica, approach the higher than 10 m2/m2 (which is very high for a productivity values for northwestern stands. deciduous hardwood stand). In many other mesic temperate forests, however, annual productivity in early years typically equals or exceeds that in the Productivity Pacific Northwest. The key to the larger biomass accumulations in the Pacific North- Productivity of the northwestern west is clearly the sustained height growth American temperate forests is generally com- and longevity of the dominants, not the parable to forest stands in other temperate differences in productivity rates. This regions. Biomass in young stands probably growth is aided by the trees' ability to accumulates at 15 to 25 tons/ha annually in accumulate and maintain a large amount of fully stocked stands on better than average foliage. Northwestern tree species continue

Table 3. Leaf biomass and projected leaf areas for four forest types in the Pacific Northwest, three forest formations in Japan, and tropical rain forest.

Number of Leaf Projected 1 Type stands mass leaf area 22 mt/ha m /m

Douglas-fir (young) 10 19 9.7

Douglas-fir/western hemlock (old) 19 23 11.7

Sitka spruce/western hemlock 4 21 13.2

Noble fir 1 18 10

Deciduous hardwood forest (Japan) 14 3.1 3 to 7

Evergreen hardwood forest (Japan) 40 8.6 5 to 9

Conifer (Japan)2 66 16.9 6 to 10

Tropical rain forest 6 9.4 7 to 12

1Datasources: Pacific Northwest, see appendix; Japan, Tadaki, 1977; tropical rain forest, Art and Marks, 1971. 2No stands of pine or Cumpressaceae included. J. F. FRANKLIN & R. H. WARING 63

Figure 1. Comparison of the growth rates of Douglas-fir and lobiolly pine. Pine has I.- 4C a faster earlier growth rate, but the sus- CD DOUGL AS -FIR tained growth of the Douglas-fir results in the latter eventually overtaking the former. LU Ia)110 to grow substantially in diameter and height, and stands in biomass, long after

I- those in other temperate regions have 0 reached equilibrium. This is well illus- I- trated by comparing growth of loblolly pine 50 (Pinus taeda) in the southeast and Douglas- LU 20 fir in the Pacific Northwest (Worthington, I.- 1954). Initially, the pine outgrows the LU Douglas-fir, being 100 percent taller at U, 10 years; however, Douglas-fir overtakes a 15 - the pine in diameter growth at 5 years and C in height growth at 30 years (Figure 1). Wood production from a single (100-year) 4 Jo rotation of Douglas-fir is about 22 percent I- greater than yields from two 50-year rota- 0 tions of pine. Recent studies of height I.-. growth patterns torhigher elevation 0 20 T%J J'' Douglas-fir, noble fir,and mountain hemlock AGE OF TREE(years) have further documentedsustained height growth of northwesternspecies into their second and third centuries(Curtis et al., 1974; Herman et al.,1979; Herman and Franklin, 1977).

Table 4. Aboveground net primary productionestimates for coniferousforests in the Pacific Northwest (west of thecrest of the Cascade Range)

Stand Net primary Community type age Biomass productivity Source

years mt/ha mt/ha/yr

Coast redwood "old" 3,200 14.3 Westman and Whittaker, 1975

Western hemlock 26 192 36.2 Fujimori, 1971

Western hemlock/Sitka spruce 110 871 10.3 Fujimori et al., 1976

Sitka spruce/western hemlock 130 1,080 14.7 Gholz, 1979

Western hemlock/Sitka spruce 130 1,492 12.3 Gholz, 1979

Douglas-fir 150 865 10.5 Gholz, 1979

Douglas-fir 125 449 6.6 Gholz, 1979

Douglas-fir/western hemlock 100 661 12.7 Fujimori et al., 1976

Douglas-fir/western hemlock 150 527 9.3 Cholz, 1979

Noble fir/Douglas-fir 115 880 13.0 Fujimori et al., 1976

Douglas-fir/western hemlock 450 718 10.8 Crier and Logan, 1977 64 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Gross productivity rates are probably mid-1800's. Some suggest that many har±:ood greater in many tropical rain forests and genera were eliminated by cold temperatures in warm-temperate evergreen broadleaf f or- during glacial epochs (Kuchler, 1946; Gray ests, but lower respiration rates in the and Hooker, 1882). Most hardwood extinctions Pacific Northwest result in greater net pro- actually occurred during the Pliocene, how- ductivity. However, total autotrophic ever, eliminating glaciation as a factor. respiration appears much higher in north- Furthermore, some scientists (Silen, 1962) western coniferous forests than in temper- feel that favorable Pleistocene environments ate deciduous forests. Grier and Logan in the Pacific Northwest, including the (1978) estimated respiration by a 450-year- availability of migration routes, were old Douglas-fir stand at 150 ton/ha/year; factors contributing to the survival of the estimates for a mixed oak and pine forest outstanding conifer gene pool. in New York and a tulip poplar forest in Moisture and temperate deficiencies Tennessee were 15.2 and 15.9 ton/ha have also been proposed as important factors (Woodwell and Botkin, 1970; Sollins et al., in eliminating hardwoods. Chaney and others 1973). The large respiration cost reflects (1944) suggest that arid periods were re- the much larger foliar biomasses and the sponsible for hardwood losses. Daubenmire presence of respiring foliage during the (1975, 1976) identifies the annual distribu- relatively warm winters. The net effect of tion of the heat budget, i.e., summer heat the high levels of autotrophic respiration deficiencies coupled with an inability to is to accentuate differences in productivity utilize the frequent warm days in the spring between northwestern conifer and temperate and fall. Regal (1977) proposes that gymno- deciduous hardwood forests, making the con- sperms survive as dominants only in environ- trast in gross production even greater than ments that are, in some way, harsh or that in net primary production. rigorous, but he concedes uncertainty as to In summary, the coastal regions of the how the coniferous forests of the Pacific Pacific Northwest are dominated by conifer- Northwest conform to this hypothesis. ous forest stands having biomass accumula- Research conducted under the auspices tions far exceeding forests in other of the Coniferous Forest Biome clearly indi- northern temperate forest regions. Leaf cates that existing forests are very well masses and projected leaf areas greatly adapted to the current climatic regime. In exceed those found in temperate deciduous a variety of ways, the evergreen coniferous hardwood forests. The large biomass values habit appears superior to that of a decidu- result from sustained growth of tree species ous hardwood within the macroclimatic with long lifespans rather than from great- regime of warm, relatively dry summers and ly superior net annual productivities. mild, wet winters. Since comparable climatic regimes have existed for several epochs, we propose that these were also key EVERGREEN CONIFER DOMINA10E factors in the evolution of the north- western coniferous forests and the competi- Another outstanding feature of the f or- tive elimination of much of the original ests of the Pacific Northwest is their hardwood flora. dominance by evergreen coniferous trees. Typically, forests in moderate environments in north temperate regions are dominated by Climate deciduous hardwoods or by a mixture of hardwoods and conifers. This is true of The climatic regime in the Pacific natural forests in Asia, Europe, and the Northwest has striking contrasts to the eastern United States. Yet, in the Pacific climate in other temperate forest regions. Northwest the ratio of conifers to hard- Salient elements shown in Figures 2, 3, and woods is more than 1,000:1 (Kuchier, 1946), 4 illustrate the temperature regime, pre- a unique phenomenon. Furthermore, the few cipitation pattern, and vapor pressure hardwoods that are present tend to occur as deficits for several stations in the Pacific pioneer species (e.g., red alder) or occupy Northwest and in temperate forest regions of environmentally marginal or severe habitats the eastern United States and Europe. (e.g., oaks), while in other temperate Climatically, the region experiences regions conifers tend to pioneer or be push- wet, mild winters and warm, relatively dry ed toward more severe environments (see e.g., summers. The dormant season, when shoot Regal, 1977). growth is inactive, is characterized by What factors have been responsible for heavy precipitation with daytime tempera- the evolution of these temperate forests in tures usually above freezing. The growing which conifers so completely dominate hard- season has warm temperatures associated woods? Scientists have speculated about with clear days, relatively little precipi- this since the time of von Humboldt in the tation, and frequent vapor pressure defi- J.F. FRANKLIN & R. H. WARING 65 cits, except directly on the Pacific Coast ably because of interactions between mari- (i.e., in the Picea sitchensis Zone of time and continental air masses and mountain Franklin and Dyrness, 1973).Water storage ranges. Along the coast, where the maritime in snowpack, soils, and vegetation, as well influence is strongest, mild temperatures as pulses of fog, clouds, or cool maritime are associated with prolonged cloudiness air which reduce evaporation, are obviously and narrow diurnal and seasonal fluctuations important during the summer drought period in temperature (6 to 10 C). Winters are experienced in the Pacific Northwest. extremely wet and freezing temperatures are Climate in the region varies consider- rare. Summers are cool and relatively dry, but extended periods of cloudiness and fog greatly reduce evaporation. Valleys located in the lee of the Coast Ranges are drier 30 and subject to greater temperature extremes and evaporative demand. For example, Eureka on the California coast contrasts with Roseburg in Oregon's Umpqua Valley, 20 PORTLAND which is located between the Cascade and Coastal ranges (Figures 2,3, and 4). On EUREKA the western slopes of the Cascade Range, percipitation again increases and tempera- 10 ture regimes moderate until subalpine environments, with their cooler temperatures and deep winter snowpacks, are encountered. Similar patterns occur elsewhere in the . 0 ------1 C-) w 0.3 ------

-I0 4 ,IJqi g.iiiwi.iii 30 0.2 w z a- 0 NEW HAVEN I- w SAPPORO O.I I-

I- A 0.3 > VESKDALEMUIR '1 40.2I- -J ESKDALEMUIR SAPPORO LLi NEW HAVEN -I0-9 / ----,---- J FMAMJ J ASO ND FRANKFURT

ru Figure 2. Temperature patterns that illus- F MAM J J A SO ND trate the contrast between the Pacific Northwest and other temperate forest regions MONTH of the world. Four stations in the Pacific Northwest are illustrated in section A, Figure 3. Relative distribution of precipi- including one (Eureka) on the immediate tation in the Pacific Northwest (section A) coast. Stations from the eastern United and other temperate forest regions through- States (New Haven), Japan (Sapporo), Scot- out the world (section B). Note the rela- land (Eskdalemuir), and Europe (Frankfurt) tively dry summer period in section A and are illustrated in section B. Note the the equitable distribution of precipitation higher winter temperatures in the Pacific in section B. Northwest. 66 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

region, although areas to the south are, of cent of the total precipitation fails during course, warmer and drier while those to the the growing season. In other temperate north are cooler and moister. forest regions, summers are typically hot- The climatic contrasts with other ter and more humid, and winters are colder. temperate forest regions are striking Night temperatures during the growing sea- (Figures 2,3, and 4). Major forest regions son in the Pa8ific Northwest generally re- in the eastern United States, eastern Asia, main below 12 C. Near the coast, or along and Europe have precipitation more evenly cold air drainages in the mountain valleys, distributed with no reduction during the nights often experience 10°C. Cool nights growing season (Figure 3). Throughout most may create dew, but this quickly evaporates of the Pacific Northwest, less than 10 per- on clear warm days and evaporative demands are ultimately much higher than those ex- perienced at similar temperatures in other temperate forest regions. Past regional ROSE BURG comparisons have underestimated evaporative differences by failing to consider differ- 20 ences in humidity. This method underesti- PORTLA mates evaporation in the Pacific Northwest by 25 to 60 percent for July and August, as seen by comparing maximum temperatures (Figure 2) with maximum vapor pressure deficits (Figure 4).

.0 E 10 How Environment Favors Evergreen Conifers I SEATTLE

C-, Almost all structural features of the

Li northwestern forests are functionally ad- LU vantageous under the moisture, temperature, 0 and nutrient regimes of the Pacific North- EUREKA west--massiveness, evergreenness, conifer LU wood structure, and needle leaves. Factors favoring these habits can be aggregated I I I I I I I U) into three categories: U) (1) Possibility of nongrowing season LU 20 assimilation, a- (2) Constraint of photosynthesis by unfavorable moisture regimes in FRANKFURT the summer, and 0 (3) Peculiarities of the nutrient 0. regime. > HAVEN Nongrowing Season Assimilation. Mild temperatures permit substantial photosyn- 1.: thesis during the so-called dormant season of fall, winter, and spring. Conifers can assimilate over a broad temperature range. Considerable carbon uptake is possible below freezing (Ungerson and Scherdin, 1968) even by coastal species such as Sitka spruce SKDAMUIR (Neilson et al., 1972). Significant winter accumulations of dry matter by conifers have o1 I I I I I I I been documented in climates s diverse as A 'iF MAMJ J S OND those of western Norway and Great Britain MONTH (Hagem, 1947, 1962) (Rutter, 1957; Pollard and Wareing, 1968). Sitka spruce seedlings Figure 4. Monthly vapor pressure deficits in Scotland actually doubled their dry for selected stations in the Pacific North- weight between late September and mid-April west (section A) and other temperate forest (Bradbury and Malcom, 1979). regions of the world (section B). Summer Substantial net photosynthesis occurs deficits are generally much higher in the over a wide range of environments during Pacific Morthwest; the Eureka station is the dormant season in the Pacific North- 7ocated on the immediate Pacific Coast. west. Winter temperatures are mild and sub- J.F. FRANKLIN & R. H. WARING 67

freezing temperatures uncommon, even in Unfavorable Summer Moisture Regimes. montane environments. This is equally true Now we can consider the second of the fac- of soil and air temperature; frozen soils tors--constraint of summer or growing sea- are extremely uncommon even in subalpine son photosynthesis by unfavorable moisture environments, so water uptake is not a regimes. Extended periods of vapor pres- major problem. Model simulations indicate sure deficits during the summers force that as much as half of the annual net car- stomata on leaf surfaces to close, reducing bon assimilation by Douglas-fir occurs be- water loss and subsequent carbon dioxide tween October and May (Eminlngham and Waring, uptake. Effects of summer drought are 1977) (Figure 5). This long period of particularly evident on dry sites, where favorable temperature (and moisture condi- nearly 70 percent of the annual net photo- tions, as will be seen) is entirely lost to synthesis probably occurs outside of the the deciduous hardwoods. The winter photo- growing season. Such site-to-site varia- synthetic opportunity of the evergreen tions are apparent in Figure 5, where the conifers is further enhanced by their long, effects of summer drought are compared in conical crowns that intercept greater such contrasting sites as the coastal Sltka amounts of light during the low angles of spruce zone environment and a hot, dry the winter sun. habitat type in the Cascade Mountains where Douglas-fir is the climax species.

00 I OC

øs (I) >., 0 0 a('J WCJ Liii 50 I 5C JcsJ -Jc,.J

'0 100 200 300 1111 Zils -[El] YEAR DAY YEAR DAY

oc SIT K A COASTAL 0I SPRIJCE U)

JcJ

cn 1 growing season I I , I

ISI' -Ills] tEl El Iiil] YEAR DAY YEAR DAY

Figure 5. Simulated photosynthetic rates for Douglas-firrowth (1 to 2 m tall) in different forest environments characteristic of the Pacific Northwest. Maximal (upper) line shows potential photosynthesis without constraints due to moisture stress, frost, or low soil temperature; lower line incorporates these constraints, with the difference between the two projections shaded. A high proportion of the yearly photosynthesis occurs outside the "growing season" on all of these sites. "Western hemlock Cascades" is fori moderate forest site, "Mountain Hemlock Cascades" for a very cold and snowy subalpine forest site, "Sitka Spruce Coastal" for a very favorable coastal site, and "Douglas-fir Cascades" for a very dry site. 68 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Stomatal closure results from both are completely closed. Because evaporative soil moisture deficiencies and high evapor- demand usually exceeds critical limits ative demand (1-laligren, 1977; Running et during the growing season over much of the al., 1975). Seasonal reductions in avail- Pacific Northwest, the environment is ob- able soil water cause plant water deficits viously less than optimum for plants de- in many locations and will limit the degree pendent upon this season for carbon uptake. to which stomata may open (Running et al., Cool temperatures at night during the sum- 1975). Increasing evaporative demand, mer months also mean that evergreens are measured by the water vapor deficit of the not penalized as severely by respiration atmosphere, can also bring about stomatal losses as might he the case in temperate closure, even in the presence of adequate regions with warm summer nights. soil water (Figure 6). Hundreds of field Large volumes of sapwood are a struc- measurements reveal that both conifers and tural feature of conifer forests that also hardwoods are affected. helps dampen the effect of dry summer days. Evergreen conifers still have signifi- Both hardwoods and conifers utilize some cant advantages over hardwoods during water from conducting tissues to help meet periods of moisture deficiency even though daily transpiration requirements (Gibbs, stomatal closure reduces photosynthesis in 1958). However, the conifers have cells both groups. Heat exchange is less inhibit- that are easier to recharge and that, be- ed in needle-shaped than broad leaves, cause the trees grow larger, store much more maintaining closer to ambient temperatures water (Figure 7). A single 80-m Douglas-fir (Gates, 1968), particularly when stomata tree may store 4,000 liters of water

Ill

0.7 U)

E 0.6 0 8 ' 0.5 C.) C 0 04 C.) V C 0 0 0.2

LIII

10 20 30 40 50 60 Vapor pressure deficit (mb)

Figure 6. Maximum stomatal conductances recorded at different evaporative demands (vapor pressure deficits) for a variety of native species growing under condi ti ons with adequate soil water. Conifers: 1 is Douglas-fir (n = 312), 2 is western hemlock (n = 404). Deciduous trees: 3 is Pacific dogwbod (n 402), 4 is bigleaf maple (n 68). Evergreen broadleaf trees: 5 is golden chinkapin (n = 159). Deciduous shrub: 6 is vine maple (n = 429). Evergreen broadleaf shrubs: 7 is Pacific rhododendron (n = 451), 8 is salal (n = 435). J. F. FRANKLIN & R. H. WARING 69

(Running et al., 1975). A forest stand can sequences between disturbances organic have more than 250 m3/ha of water available, matter accumulates on the forest floor, enough to supply up to half the daily water particularly as slowly decomposed coarse budget (Waring and Running, 1978). There- woody debris--large logs and branches. fore, the sapwood represents a significant Ultimately, this creates conditions for buffer against extremes in transpiration large episodic losses of nitrogen and other demand and helps offset the disadvantage of nutrients as a result of wildflres.1 lifting water to great heights. Further- The pecularities of these nutrient more, although full hydration occurs during regimes combine to favor plants that have the winter, conifers may partially recharge relatively low nutrient requirements, con- sapwood after sunnier rain showers. Many servatively use acquired nutrients, and can hardwoods have no mechanism for effectively accumulate nutrients during the wet season refilling the larger evacuated vessels until when decomposition is most active. Ever- the next spring. green conifers appear to have advantages Large leaf areas may provide additional over deciduous hardwoods on all scores. structural advantages for evergreen conifers Conifers generally have lower nutrient in the dry summer climate of the Pacific requirements and use nutrients more effi- Northwest. Water is sorted on and in the ciently than most hardwoods. Foliage reten- foliage in proportion to its area. The tion for several years is obviously advanta- large needle mass also serves as a condens- geous in reducing annual nutrient require- ing surface for fog or dew, thus supple- ments; current foliage may be only 15 to 16 menting summer precipitation. percent of the total in Douglas-fir forests Summarizing contrasts in conifer-hard- (Overton et al., 1973; Pike et al., 1977). wood response to summer moisture deficienc- The relatively low levels of nutrients ies, both groups suffer stomatal closure and found in foliage are also evidence of lower reduction in photosynthesis. Conifers have conifer requirements. Nitrogen in healthy excellent control of water loss without in- foliage of 450-year-old Douglas-fir rarely creasing their leaf temperatures, however. exceeds 0.8 percent (dry weight basis), They also can develop greater water storage less than half the level of most hardwoods capacities than hardwoods and utilize these (Rodin and Bazilevich, 1967). Similar con- adaptations to reduce the impact of stress trasts have been demonstrated with calcium. common during the growing season. Northwestern conifers also meet in- creasing proportions of their total nutrient Adaptations to Nutrient Regime. We can requirements by redistribution from older now consider the last of the three environ- tissue, especially senescent needles. Half mental influences--the distinctive nutrient of the nitrogen required by a 100-year-old regime of the Pacific Northwest. Nutrients stand of Douglas-fir (down to 30 kg/ha/yr clearly rank below temperature and moisture from a high of 50) is met by translocation in their influence on the evolution of these forests, but they are still an import- ant factor. The region has a nutrient regime that contrasts with that character- 1 There are a large arrayof organisms istic of other temperate forest regions, associated with nitrogen fixation in the partially because of the winter-wet, summer- Pacific Northwest. Successional pioneers dry climate. Decomposition and subsequent nutrient in the genera of Alnus and Ceanothus, as well as other higher plants, have nitrogen- release from the organic layer occurs fixing microbia' associates. mostly during the cool, wet "dormant" sea- Large amounts son in the Pacific Northwest and may essen- of nitrogen--SO to 300 kg/ha/yr--can be tially cease during the relatively dry fixed by such plants during early stages of sunnier (Figure 8). Slow summer decomposi- forest development, partially or completely tion has been reported from such diverse balancing losses associated with catastroph- ic fires. sites as Douglas-fir and western hemlock Foliose lichens endemic to the forests at low to middle elevations and sub- old-growth forests provide further, con- alpine fir forests at high elevations in the tinuing nitrogen inputs of 3 to 5 kg/ha/yr. Finally, large boles which, as snags and Cascade Range (Fogel and Cromack, 1979; down logs, survive major disturbances, are Turner and Singer, 1976). In the western a source of slowly available nitrogen as Oregon Cascade Range almost no measurable well as the site for substantial microbial decomposition occurs in July and August fixation. All of these pathways for (Fogel and Cromack, 1979). fixation and retention of nitrogen may The massiveness of the forests also represent adaptations to catastrophic wild- contributes to the uniqueness of the nutri- fires and related nitrogen deficiencies in ent regime by binding large amounts of nu- a region otherwise favorable to vegetative trients into standing crops. Over the long growth. 70 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

15 U wIi. ° 10 Id Figure 7. Seasonal variation in sapwood water storage of old-growth Douglas-fir

U I I II ' (section B) in relation to evaporative de- 5 I II a. I I II I I I Periodic summer storms I II g mand (section A).

I II 0 I $ Ill totaling less than 10 cm precipitation a. ..l #ilI, ' ' "I l'_ - reduced the evaporative demand, but clear weather following the storms encouraged a bc partial recharge before depletion began 0 again. With the onset of fall precipita- I-4 tion, the evaporative demand remained below

8C 2 ml and sap.vood recharged at a constant 4 rate until January when filled. In April 1976 the average evaporative demand ex- ceeded 5 ml; some water columns in the sap- o 6C 0 0 wood were broken and the water was utilized for transpiration. Recharge is still 4a. possible after April, but only under ab- U, C JUN JUL AUG SEP OCT NOV DEC JAN FEB MAR APR MA normally low evaporative demand.

80-

60- 0 Ui 0 40-

>- I_I on- F 0Z 0 3 5 7 9 II I 3 5 7 9 II I 3 MONTH

Ui CD 16 i 100 CD 2 I 2 4 I 0= 12 I 4 I 8 C, Ui Ui

I CD W r ¼) tOO 200 300 400 500 600 DAYS ELAPSED

Figure 8. Decomposition rate for leaf litter stored in litter bags for two years, illustrat- ing the highly seasonal nature of decomposition in the Pacific Northwest and its relation to precipitation (courtesy Kermit Cromack, Jr.) 3.F. FRANKLIN & R.H. WARING 71

(Cole et al., 1975). Other northwestern FOREST MASSIVENESS conifers behave similarly and may be even more conservative. The advantages of being massive are Deciduous hardwoods also redistribute not as clear as those of being tvergreen. substantial amounts of nutrients from Massiveness is, to a degree, related to foliage prior to leaf fall, but their total some of the same environmental factorsthat requirements are higher. Mature hardwoods favor evergreenness, however. reportedly require 70 kg/ha of nitrogen to Size or massiveness results from the develop their canopy each year, and less sustained growth and longevity of the tree than one-third of this can be met by trans- species that occur in the Pacific North- location from storage sites within the tree west. The fact that many species sustain (Bormann et al., 1977). their height and diameter growth for more Nutrient cycles also tigten during suc- than two or three centuries has already cession accentuating problems for a decidu- been mentioned. It is also important to ous hardwood. Trees are increasingly de- recognize that every coniferous genus rep- pendent upon the forest floor, rather than resented in the Pacific Northwest (save the soil, for nutrients (Cole et al. ,1975). only Juniperus) has its largest and often Yet litter quality declines and litter longest-lived representative here--and often decay slows, making this a poorer source of its second and third largest as well nutri ents. (Table 5). Hence, nutrient regimes in the Pacific Such a circumstance requires at least Northwest again appear to be penalizing two conditions. First, there must be hardwoods. Total nutrient requirements are species' gene pools that favor persistent higher for hardwoods than evergreen coni- growth and long life. Second, there must fers. Requirements must be largely met by be environmental conditions that allow the absorption from soil and forest floor since expression of this genetic potential--or at hardwoods cannot provide as much of their least do not select against such geno- nutrient requirements by internal redistri- types. Such environments are not necessar- bution. Yet decomposition and nutrient ily pervasive in the temperate zone of the release are lowest during summer months world. Periodic storms with high winds when hardwood nutrient demand is high; the (hurricanes and typhoons) are, in fact, large pulses of nutrients during the wet characteristic of most temperate forest fall and winter is of less value regions. Indeed, Fujimori (1971) suggests for deciduous trees since they are less that infrequent strong winds, such as those capable than evergreens of absorbing that disturb or weaken forest communities, nutrients during the dormant season (Mooney are a key factor in the development of and Rundel, 1979). massive, long-lived forests in the Pacific In summary evergreen coniferous trees Northwest. Less favorable conditions for are well adapted to the existing moisture, development of pathogens is one of several temperature, and nutrient regimes in the alternative hypotheses. Neither explana- Pacific Northwest. Deciduous hardwood tion seems completely satisfactory. species have, on the other hand, numerous Large size and longevity have adaptive disadvantages in competing with conifers. advantages. Competitively, they obviously First, they cannot utilize the "dormant' allow a species to overtop one of smaller season for photosynthesis. Second, they structure or out-persist a species of short are dependent upon assimilation during the lifespan, or both. Long-lived species growing season, a time when photosynthesis classed as pioneers or shade-intolerant are is frequently constrained by atmospheric able to span the long periods between and soil moisture deficiencies. Third, destructive episodes. Forest sites in the hardwoods have higher nutrient requirements Pacific Northwest can go for many centuries and a higher proportion must be met by up- between disturbances sufficient to allow take from the soil and litter layers; regeneration of shade-intolerant species. again, this must be done during the growing For example, Hemstrom (1979) calculated the season when decomposition and nutrient average fire-return period for Mount Rainier release are at minimal levels due to re- National Park, a site typical of much of the duced soil moisture. Dominance by ever- Cascade and Coastal ranges, to be more than green conifers appears to be an evolutionary 400 years. A short-lived, shade-intolerant response to a climate with cool, wet winters species is clearly at a disadvantage under and warm, dry summers. such disturbance regimes. As with many organisms large size allows for buffering against adverse environ- mental conditions and stresses of various types. The value of the large sapwood storage areas in conifers in reducing 72 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Table 5. Typical and maximumages and dimensions attainedby selected speciesof forest trees on better sites in the PacificNorthwest1

Typical Maximum

Species Age Diameter Height Age Diameter

years cm in years cm

Silver fir (Abies amabilis) 400+ 90-110 44-55 590 206

Noble fir (Abies procera) 400+ 100-150 45-70 >600 270

Port-Or ford- cedar (Chamaecyparis lawsoniana) 500+ 120-180 60 359

Alaska yellow-cedar (Chamaecyparis nootkatenis) 1,000+ 100-150 30-40 3,500 297

Western larch (Larix occidentalis) 700+ 140 50 915 233

Incense-cedar (Libocedrus decurrens) 500+ 90 120 >542 368

Engelmann spruce (Picea engelmannii) 400+ 100+ 45-50 >500 231

Sitka spruce (Picea sitchensis) 500 180-230 70-75 >750 525

Sugar pine (Pinus lambertiana) 400 100-125 4555 -- 306

Western white pine (Pinus monticola) 400+ 110 60 615 197

Ponderosa pine (Pinus ponderosa) 600+ 75-125 30-50 726 267

Douglas-fir (Pseudotsuga menziesii) 750+ 150-220 70-80 1,200 434

Coast redwood (Sequoia sempervirens) 1,250+ 150-380 75-100 2,200 501

Western redcedar (Thuja plicata) 1,000+ 150-300 60+ >1,200 631

Western hemlock (Tsjgheterophylla) 400+ 90-120 50-65 >500 260

Mountain hemlock (Tsuga mertensiana) 400+ 75-100 35+ >800 221

1Typical values mainly from Franklinand Dyrness,1973; maximum diametersfrom American Forestry Association,1973; maximumages fromFoweils,1965; or personal observations by the authors. d. F. FRANKLIN & R. H. WARING 73 effects of high moisture deficiencies has In 1975, an age structure analysis was already been pointed out. The large mass conducted in an old-growth Douglas-fir of various organs, such as leaves, are also stand at H. J. Andrews Experimental Forest valuable for storage of nutrients and carbo- in the western Cascades of Oregon. Experi- hydrates for use during times of high demand mental Watershed No. 10, a lO-hectare (the growing season) or stress. drainage, was clearcut. Previously, all of the trees in this drainage more than 15 cm diameter at breast height (dbh) had been SUCCESSIONAL ASPECTS OF stem mapped, recorded by dbh and species, NORTHWESTERN FORESTS and tagged at stump level. Following clear- cutting, rings were counted on stumps of The lack of quantitative data on more than 600 of the 2,700 inventoried various aspects of forest succession in the stems, including a large proportion of the Pacific Northwest is astounding. Foresters dominant Douglas-firs. and botanists have been observing these f or- The age distribution of the counted ests for nearly a century, yet most suc- Douglas-fir trees on Watershed No. 10 is cessional analyses are either anecdotal shown in Figure 9A. A disturbance in about (e.g., Munger, 1930, 1940) or based upon in- 1800 is obvious from a wave of younger ferences drawn from current size class Douglas-firs; this partial burn is also distributions (e.g., Franklin, 1966). apparent in the age distribution of hem- Quantitative data have been especially locks, most of which date from 1800. The scarce for older forests. Some data have surprising result is the very wide range been collected on compositional and struc- in ages of dominant, old-growth Douglas-firs tural changes in recently logged or burned in this stand--from 275 to 540 years of areas (Dyrness, 1973). age. Furthermore, there is no evidence of This situation is rapidly changing and multiple peaks or waves of establishment-- there are many interesting new findings in just a gradually increasing number of in- regard to changes in diversity, leaf and dividuals followed by a broad-crested peak biomass development, and nitrogen budgets and gradually declining period of establish- during forest succession (Long and Turner, ment (Figure 9B). Analysis of separate 1975). Another interesting development is habitat segments on this diverse watershed the increased recognition of multiple path- (Hawk, 1979), such as the moist lower slope ways in the development of stands on a and dry ridgetop situations, provided no given site, i.e., several possible species explanation for the forest age pattern; a series contrasted with a single sequence similar age distribution was found on all of pioneer and climax species. habitats. We will consider briefly two aspects of Watershed No. 10 might be considered forest succession which have been explored an aberrant situation, especially in view in recent studies: (1) age structures in of the overall decadence of the stand old-growth Douglas-fir/western hemlock for- (Grier and Logan, 1977) and relatively low ests and (2) dynamics of coarse woody debris site quality. Subsequent age structure in a Douglas-fir forest chronosequence. analyses, however, have revealed similar patterns elsewhere. Joseph Means (pers. Age Structures in Old-Growth comm., 1979) analyzed a dense, thrifty Douglas-fir Stands Douglas-fir stand at about 1,000 m on a cool, moist habitat type. The same pattern, Foresters and ecologists have always with a 125-year age range in the dominant assumed that the old-growth forests domin- Douglas-firs, is present (Figure 10). Ring ated by Douglas-fir are even-aged. The counts on several clearcuts surrounding Douglas-firs in these stands presumably Thornton T. Munger Research Natural Area in were established over short time periods the Wind River drainage of the southern following major fires or other disturbances Washington Cascade Range reveal an even more In part, these assumptions were based upon extended age range (200 years) in the domin- observations of forest development and ant Douglas-firs (Figure 11); this stand is Douglas-fir regeneration following the ex- at around 500 m. The Douglas-fir age tensive fires in the mid and late 1800's- structures reported by Boyce and Bruce-Wagg as well as in the Yacholt and Tillamook (1953) are further evidence for wide ranges Burns of the twentieth century (Munger, of age in old-growth stands; the implications 1930, 1940). For a time it was even be- of these early data were apparently over- lieved that new Douglas-fir forests sprang looked. almost instantly from seed stored in the The conclusion from all of these litter layers (Hofmann, 1971), a hypothesis analyses is that many of the old-growth later disproved by Isaac (1943). No one Douglas-fir forests are not even-aged. For bothered to analyze age structures of any some reason, many of these stands did not old-growth stands, however, to test their hypothesized even-aged nature. 74 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

close up rapidly following the disturbance appear to be the pattern followed by many or series of disturbances that destroyed the of the old-growth stands. Successional previous stands. Douglas-fir has apparently studies during coming years should provide taken a long period (100 to 200 years) to evidence of additional patterns and the fully reoccupy many of these sites. There responsible factors. Indeed, a recent study are several possible explanations. The of tree ages in the Cowlitz River drainage disturbance or disturbances that gave rise of Mount Rainier National Park shows that to these stands, many of which are 400 to establishment of shade-intolerance tree 500 years of age, may have been so extensive species, such as Douglas-fir and western as to eliminate seed source; gradual re- white pine, is still taking place more than colonization of the area would have been 80 years after the last wildfire (Figure required, with a few individuals becoming 12) (Hemstrom, 1979). established and eventually providing the seed source for development of a closed Coarse Woody Debris in a Forest stand. The age structure patterns fit Chronosequence Harper's (1978) hypothesized sequence of this type. Competing vegetation may have Structural changes associated with suc- delayed establishment of trees. Multiple cessional development of forest stands in disturbances subsequent to the first one the Douglas-fir region are currently under may have wiped out portions of young stands, study. These studies were stimulated, in creating open for establishment of part, by an analysis of old-growth forests even younger cohorts; reburns of young (Franklin et al., 1979) that revealed Douglas-fir stands occur, with survival of precious little knowledge of northwestern individual and small patches of trees. forest structure beyond measurements of In any case, the assumed pattern of wood volumes and production. A series of forest succession with early establishment nine Cascade Range stands have been studied of even-aged Douglas-fir stands does not thus far, ranging in age from about 100 years to more than 1,000 years. A major structural feature is the amount and distri- bution of coarse woody debris as standing 'I'; dead (snags) and down (logs and chunks) (Table 6). fl DOUGL AS- FIRS One of the most surprising findings 60 - HJ ANDREWS (OR) from this survey was the large amount of Watershed 10 dead wood in young stands. Much wood is being carried from the old into the new stand. Wildfire or windthrow may kill the 50 (n=298) previous stand but consumes very little of

Cl) the wood; indeed, one or, more probably, Lu ILl several subsequent fires would be required to eliminate the large snags and down logs. I.- 40 Consequently, large amounts of woody debris 0tj bridge the disturbance and remain important structural features of the young stand for Lu 30 several centuries because of their slow rate of decomposition. By the time the 2 woody debris carried over has largely dis- appeared, stems in the young stand are sufficiently large to provide an input of large woody debris. As a result, there seems to be a rather high level of woody debris found at all stages in forest suc- cession. The large amount of coarse woody debris provides a major structural con- trast between the natural T!second_growth!T stands and the managed forests created after 575 47 375 275 175 75 logging. A second interesting feature is the TREE AGES (25 yr. classes) suggestion of greater amounts of woody There is a trend Figure 9A. Age classdistributionof debris with stand age. Douglas-fir treeson Watershed No.10 at the toward greater absolute amounts as well as H. J. Andrews ExperimentalForest in the a higher ratio of dead/live organic matter western Oregon CascadeRange. Tabulation in the stands more than 750 years of age of all counts by 25-year age classes. (Figure 13). Amounts of coarse woody debris J.F. FRANKLIN & R. H. WARING 75

30

25

-J o 20 > 0 z 5 0LL

LU m 10 z

5

400 420 440 460 480 500 520 540 AGE CLASS (10 yr. classes)

Figure 9B. Age class distribution of Douglas-fir trees on Watershed No. 10 at the H. J. Andrews Experimental Forest in the western Oregon Cascade Range. Tally of old-growth trees by 10-year age classes.

'5 ft DOUGLAS-FIRS H.J ANDRE4'S (OR) (Silver Fir/Foarnflower Habitat Type)T

Z j c rii I.:..::.._ ... 330 350 400 450 475 AGE IN YEARS (corrected for stump height)

Figure 10. Age-class distribution of Douglas-fir trees in an old-growth stand locatedat about 900 m in the H. J. Andrews Experimental Forest on the Oregon CascadeRange. 76 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

at a given age vary widely, almost certainly amounts of live biomass in very old stands because of peculiarities in development of (Table 6). A current hypotheses is that individual stands. This variability makes live organic biomass in a stand may peak at it difficult to substantiate any statistical! around 300 to 400 years, total biomass trends associated with stand age. There (live and dead) at around 750 years, and is, however, some corollary evidence from dead (coarse woody debris) at 800 to 1,000 an analysis of old-growth stands at Mount or more years. Many more stand analyses are Rainier National Park that suggests reduced required, however, given the variability in patterns of stand development.

15

C/) LU LU

I ro 0IL U) w m z

250 300 350 400 450 AGE IN YEARS

Figure 11. Age-class distribution of Douglas-fir trees in old-growth stands located around the periphery of the Thornton T. Munger Research Natural Area in the Wind River vallei of the southern Washington Cascade Range.

TREE AGES INTENSIVE SAMPLE TRANSECTS - TRANSECT I n-94 20 TRANSECT 2 n=$O0 / (I) TRANSECT3 n=I00 /,/\ LU \ LU FIRE IN1886-7 I /11 \\ \ 0U- /

LU $0

z

0 0 50 AGE CLASS

Figure 12. Age-class distribution of trees in stands developed following wildfires in the later 1800's in the Cowlitz River drainage, Mount Rainier National Park, Washington (from Hemstrom, 1979). J. F. FRANKLIN & R. H. WARING 77

250

C0 - ISO E z-. 0 o 50 0 z Figure 13. Total amounts (mt/ha) and per- 25 ujuJ cent of the total organic matter provided 0I- I- by coarse woody debris (standing dead trees 5 and down logs) in a chronosequence of 0 Douglas-fir/western hemlock forests located S in the Cascade Range of Oregon and Washing- (0 ton; only a weak relationship with age is 0 I I I apparent in this preliminary data set. 0 200 400 600 800 000 AGE OF STAND

Table 6. Coarse woody debris in a chronosequence of stands from mid-elevations in the northern Oregon and southern Washington Cascade Range1

Live Coarsewoodydebris Dead/total 2 Stand Age biomass3 Snags Logs Total biomass

yrs mt/ha mt/ha

HJA RS 24 100 564 37 113 150 21

HJA RS 26 130 934 48 70 118 11

MR 1 250 1,318 67 85 152 10

Bagby 250 1,069 122 129 251 19

HJA RS 2 450 1,189 58 90 148 11

UJA RS 3 450 991 79 131 210 17

Squaw 750 1,094 85 119 204 16

MR 2 1,000+ 638 48 156 204 24

MR 3 1,000+ 931 120 112 232 20

1llnpublished dataon file at the Forestry Sciences Laboratory, Corvallis, Oregon. 2"HJA RS"refers to hectare 'reference stands" or permanent sample plots at H.J. Andrews Experimental Forest in the western Cascades of Oregon. "MR" stands are similar plots in Mount Rainier National Park, Washington. Baghy and Squaw are located in the northern Oregon Cascade Range. 3lncluding 20percent of live aboveground biomass as estimate of live belowground biomass. 78 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

OLD-GROWTh FOREST ECOSYSTEMS Fun c t ion

Old-growth forests are distinctive eco- Functional aspects of forests include systems that have not been well understood primary production and the cycling of by either foresters or the lay public. In- nutrients and energy. Productivity in old- deed, no one was really very interested in growth forests is typically high, despite them until recently. Some viewed these for- statements to the contrary. The large leaf ests as biological deserts although, insofar areas and masses found in northwestern for- as biologic diversity is concerned, that ests were mentioned earlier, and there is description is most applicable to the dense, no indication that levels decline signifi- productive young forest. Others viewed them cantly in older stands. A single long- solely in aesthetic or religious terms. tn crowned old-growth Douglas-fir tree may any case, with their broadened sense of land have as many as 66 million needles and stewardship, foresters are thinking in- 2,800 m2 of needle surface area. With such creasingly in terms of maintaining and re- large and intact photosynthetic factories, creating such systems in order to provide a production values are maintained at com- diversity of habitats and organisms. parable levels over many centuries. How- Questions have arisen as to the essential ever, respiration costs are high in old- features of old-growth forests, however. growth stands because of their large live What are their key characteristics and how biomasses, greatly reducing the amount of do they differ from managed stands or from net production. the natural second-growth forests that On the more practical level, little follow wildfire? accumulation of additional live biomass or General features of old-growth (>200 board feet occurs in most old-growth stands. years old) forest stands in the Douglas-fir Substantial wood increment is taking place region now have been described (Franklin on individual trees, including associated et al., 1979). We have extracted a few western hemlock and other shade-tolerant highlights from that characterization and species. Typically, this wood growth is will briefly examine the compositional largely offset by mortality and decay (what is there), functional (how it runs), losses in living trees. In a 250-year-old and structural (how it's put together) fea- Douglas-fir stand in the Mount Hood National tures of old-growth forests. The emphasis Forest annual wood increment over 10 years will be on structure, since this provides a was 15.8 m3/ha an episode of heavy mor- major key to the distinctiveness of old- tality (14.1 mi/ha/yr) caused by bark growth stands. and windthrow nearly offset this large growth. In the Thornton T. Munger Research Natural Area in the Gif ford Pinchot Composition National Forest a 450-year-old Douglas-f in western hemlock stand grew 7.4 rn3/ha/yr The composition of old-growth forests over 12 years; the average annual mortality is obviously different from that of young was 6.7 m3/ha/yr. Hence, both stands stands. Changes in composition--the array registered small met gains. Over the long of plant and animal species--is, after all, run, living biomass in stands in old stands a keystone of ecological succession. Many probably fluctuates around a plateau in species, including some saprophytic plants, response to episodes of heavy and light some epiphytic lichens, and several verte- mortality. brates, find optimum habitat conditions in Old-growth forests are known to be old-growth forests. There are relatively highly retentive of nutrients. Complex few species of plants or animals that are detnital pathways exist in such stands and found only in old-growth forests, however. the release of energy and nutrients from Some organisms may require old-growth for dead organic matter is slow. This is re- maintenance of viable populations, although flected in the low levels of nutrients and that is not yet clear. Currently, verte- other dissolved and suspended materials in brate/old-growth relationships are best streams from old-growth forests (see understood, and a list of 14 birds and nine Fredriksen, 1970, 1972). Mechanisms for mammals finding their optimum habitat in fixation of atmospheric nitrogen are also old-growth Douglas-fir forests has been well developed in old-growth forests, pro- compiled (Franklin et al., 1979). Several viding for substantial increments by foliose of these, such as the northern spotted owl lichens in tree crowns and by microbial (Strix occidentalis) and the red tree vole fixation in coarse woody debris (see Carroll, (Arborimus longicaudus), may be examples of this volume; Triska and Cromack, this species that require a reservoir of their volume). optimum habitat in old-growth forest to survive. J. F. FRANKLIN & R. H. WARING 79

Structure and the way in which energy and nutrients are cycled. Finally, logs are at least as Structural diversity is characteristic important (and possibly more so) to the of old-growth forests. There is, for stream component as they are to the example, a large range in tree sizes, a more terrestrial component of the ecosystem varied canopy, and greater patchiness in the (see Triska and Cromack; Swanson; and unders tory. Cummins, all this volume). There are, however, three structural The most conspicuous structural com- components of overwhelming importance--the ponent is probably the live, old-growth individual, large, old-growth tree, the Douglas-fir tree. Diameters of 1 to 2 m and large, standing dead tree or snag, and the heights of 50 to 90 m are typical. The large, dead, down trunks or logs. These trees are highly individualistic, having structural components are, in large measure, been shaped over the centuries by a wide unique to an old-growth forest ecosystem, riage in forces. The large, deep, irregular setting it apart from young growth and. crown is an important ecological feature especially, managed stands. These compon- (Figure 15). Live branch systems often ex- ents are all related (Figure 14), with the tend two-thirds of the length of the bole. tree playing a progression of roles from the Flattened, fan-shaped branch arrays are time it is alive through its routing to an characteristic and provide extensive hori- unrecognizable component of the forest zontal surfaces for the development of epi- floor. Further, most of the unique (or at phytic communities and wildlife habitat. least distinctive) compositional and func- Carroll (this volume) discusses the role of tional features of old-growth forests can such canopies in nutrient cycling and the be related to these structures (Table 7); importance of canopy lichens (especially that is, these structural components nake Lobaria oregana) in nitrogen fixation. possible much of the uniqueness of old- growth forests in terms of flora and fauna

STANDING DEAD t-1j eiii

LIVE I I WIND. GIVITY.. 1FOREST OLD-GROWTh I I FLOOR TREESJ I

DECAY! DECAY DECAY DECAY CLASSt- CLASS CLASS CLASS j_J 2 3 4 DOWN DEAD

RouTING OF FOREST TREES FROM LIVE THROUGH VARIoUs DEAD ORGIc COMPARTMENTS

Figure 14. Diagrammatic illustration of the relationships between the key structural features (live trees, snags, and down logs) of old-growth forest stands. 80 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Standing dead trees or snags are well known for the fire and safety hazards they represent and, more recently, as critical habitat for wildlife (dine et al., 1979). m Thomas and others (1979) have thoroughly analyzed the role of snags as sites for nesting, food sources, and other uses by wildlife. In the Blue Mountains of Oregon, m snags are t1e primary location for 39 birds and 24 mammals species that utilize the cavities. Furthermore, a direct correla- tion is indicated between numbers of snags m and related wildlife populations. Snags undergo a steady process of decay and dis- integration, and a variety of standing dead size and decay classes are necessary to meet differing animal requirements. Snags also play the same functional roles as down logs. Down dead trees, also known as logs or m coarse woody debris, are nearly as conspic- uous as the large live trees. Large masses of logs constitute an important component of old-growth forests (Table 6). In addi- tion to their volume and weight, these logs can occupy 10 to 20 percent of the ground surface area. Logs provide several import- ant habitat and functional roles (Table 7). Many animals utilize logs as food sources, protection, and living sites. The logs provide important pathways for small mam- mals that may be important in providing for the spread of mycorrhizal-forming fungi (Maser et al., 1978). Down logs also serve Figure 15. Schematic illustration of the as habitat for reproduction of some tree branch systems of an old-growth Douglas-fir species, especially western hemlock. In tree, illustrating the deep crown character- natural stands this is important in provid- is tic of many of the trees (courtesy Wm. ing seedlings and saplings for potential Denison and G. Carroll). canopy replacements. Logs, of course, represent large storehouses of energy and nutrients and, as pointed out by Triska and CONCLUSIONS Cromack (this volume), are sites where significant bacterial fixation of nitrogen Studies of our forest ecosystems during takes place. the last decade have produced many signifi- These structural features of old-growth cant new insights into the structure and forests provide one handle for foresters to functioning of forests in the Pacific North- use in perpetuating or mimicking natural west. We have much improved understandings of how forests are adapted to their environ- processes. Silvicultural methods can be developed for creating stands with these ment and how they respond to various natural characteristics as well as individual struc- and man-created disturbances. These find- ings contribute to improved management of tural (and, hence, compositional and func- forest lands, and the development of appli- tional features) of the virgin forests. It cable results can be expected to accelerate will be a challenge for foresters to see if as we enter our third generation of eco- they can learn to manage dead wood as system-level studies. I strongly suspect imaginatively as they do live!Or, to put that, however much we currently think we it another way, to manage for decadence as know, we are going to be in for many more well as board feet! There certainly is Surprises. evidence that they can--for example, in the new snag management policies. 3.F. FRANKLIN & R. H. IARING 81

Doucjlas-fir Table . Relat1onship of the keg structural components of old-growth forests to compositional and functional attributes ofthese forests

Compositional Structural Functional role element role

Individual, large old-growth tree

Distinctive epiphytes Site of N-fixation Distinctive vertebrates Ionic storage Distinctive invertebrates Interception of H20 nutrients, light

Large standing dead

Utilized by cavity Energy and nutrient dwellers and other source vertebrates

Large down dead on land

Distinctive animal Site of N-fixation communities Energy and nutrient Seedbed or nursery source for seedlings

Large down dead on stream

Distinctive animal Site of N-fixation communities Energy and nutrient Creates habitat source diversity Maintains physical stability of stream Retains high-quality energy materials for processing 82 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

ACKNOWLEDGEMENTS Cole, D. W., J. Turner, and S. P. Gessel. 1975. Elemental cycling in Douglas This work Is aggregated from that of fir ecosystems of the Pacific North- many others. The discussion of evergreen west: a comparative examination. conifer dominance is taken largely from Proc. Twelfth International Botanical Waring and Franklin (1979) and that on the Congress (Leningrad) (in press). old-growth forest from Franklin and others (1979), which includes contributions by K. Curtis, R. 0., F. R. Herman, and D. J. Cromack, Jr., W. Denison, A. McKee, C. DeMars. 1974. Height growth and site Maser, J. Sedell, F. Swanson, and G. Juday. index for Douglas-fir in high-eleva- W. Moir has been a contributor to these tion forests of the Oregon-Washington ideas and directed studies at Mount Rainier Cascades. Forest Sci. 20(4):3O7-3l5. which provided data utilized here. The dissertation research of H. Gholz and N. Daubenmire, R. 1975. Floristic plant geo- Hemstrom provided data and ideas. J. Means graphy of eastern Washington and provided data and assistance on the age northern Idaho. J. Biogeography 2:1- structure analyses, and S. Lewis provided 18. data from her analysis of the Wind River stand. T. Thomas and M. James collected the Daubenmire, R. 1977. Derivation of the data on dead and down coarse woody debris flora of the Pacific Northwest. In in the chronosequence stands. Additional Terrestrial and Aquatic Ecological input has been provided by P. Sollins, G. Studies of the Pacific Northwest. Carroll, G. Hawk, W. Emmingham, and R. Cheney: Eastern Washington State Lambert. College Press.

Dyrness, C. T. 1973. Early stages of plant LITERATURE CITED succession following logging and burning in the western Cascades of American Forestry Association. 1973. AFA's Oregon. Ecology 54(1):57-69. social register of big trees. Amer. Forests 79(4):2l-47. Emmingham, W. H., and R. H. Waring. 1972. An index of photosynthesis for com- Art, H. W., and P. L. Marks. 1971. A sum- paring forest sites in western Oregon. mary table of biomass and net annual Can. J. Forest Res. 7(1):165-l74. primary production in forest ecosystems of the world. In Forest Biomass Fogel, R., and K. Cromack, Jr. 1977. Studies, Univ. of Maine Life Sd. and Effect of habitat and substrate quality Agric. Expt. Sta. Misc. Pubi. 132. on Douglas-fir litter decomposition in western Oregon. Can. J. Bot. 55(12): Bormann, F. H., G. E. Likens, and J. M. 1632-1640. Melillo. 1977. Nitrogen budget for Fowells, H. A. 1965. Silvics of Forest an aggrading northern hardwood forest Trees of the United States. USDA ecosystem. Science 196:981-983. Agric. Handbook 271. Boyce, J. S., and J. W. Bruce Wagg. 1953. Franklin, J. F. 1966. Vegetation and soils Conk rot of old-growth Douglas-fir in in the subalpine forests of the south- western Oregon. Oregon State Forestry ern Washington Cascade Range. Ph.D. Dept. Res. Div. Bull. 4. thesis, Washington State Univ., Pullman. Bradbury, I. K., and D. C. Malcolm. 1979 Dry matter accumulation by Picea sit- Franklin, J. F., and C. T. Dyrness. 1973. chensis seedlings during winter. Can. Natural vegetation of Oregon and J. Forest Res. 8:207-213. Washington. USDA Forest Service Gen. Tech. Rep. PNW-8. Chaney, R. W., C. Condit, and D.I. Axelrod. 1944. Pliocene Floras of California Franklin, J. F., K. Cromack, Jr., W. Carnegie Inst. Wash. and Oregon. Denison, A. McKee, C. Maser, J. Sedell, Pubi. 533. F. Swanson, and G. Juday. 1979. Eco- logical characteristics of old-growth Cline, S. P., A. B. Berg, and H. M. Wight. forest ecosystems in the Douglas-fir 1979. Snag characteristics and region. USDA Forest Service Gem. dynamics in Douglas-fir forests, Tech. Rep. (in preparation). western Oregon. J. Wildlife Manage- ment (accepted for publication). J.F. FRANKLIN & R. H. WARING 83

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Ungerson, J., and G. Scherdin. 1968. Waring, R. H., and S. W. Running. 1978. Jahresgarig von Photosynthese und Atmung Sapwood water storage: its contribu- unter naturlichen Bedingungen bei tion to transpiration and effect upon Pinus silvestris L. an ihrer Nordgrenze water conductance through the stems of in der Subarktis. Flora 157:391-400. old-growth Douglas-fir. Plant, Cell, and Environment 1:131-140. Walker, R. B., D.R. M. Scott, S. 0. Salo, and K. L. Reed. 1972. Terrestrial Westman, W. E., and R. H. Whittaker. 1975. process studies in conifers--a review. The pygmy forest region of northern In Research on Coniferous Forest Eco- California: studies on biomass and systems, Proc. Symp. Northwest Scienti- primary productivity. J. Ecol. 63(2): fic Assoc., edited by J. L. Franklin, 493-520. L. J. Dempster, and R. H. Waring, pp. 211-215. USDA Forest Service, Woodwell, C. M., and D. B. Botkin. 1970. Pacific Northwest Forest and Range Metabolism of terrestrial ecosystems Expt. Sta., Portland, Oregon. by gas exchange techniques: the Brookhaven approach. In Analysis of Waring, R. H., and J. F. Franklin. 1979. Temperate Forest Ecosystems, edited by Evergreen coniferous forests of the D. E. Reichle, pp. 73-85. New York: Pacific Northwest. Science 204:1380- Springer-Verlag. 1386. Worthington, N. 1954. The loblolly pine of the south versus the Douglas fir of the Pacific Northwest. Pulp and Paper 28(1O):34-35, 87-88, 90. 86 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Appendix 1. Data sources for biornass and leaf area in stands in the Pacific Northwest

Projected Source Dominant Stand Basal Abovegroundbiomass leaf and plot species age area Total Wood1 Foliage area identification2

yrs "2/ha mt/ha m2/m2

Douglas-fir 70 60 422 406 16 8.1 Santantonio(Dry) Douglas-fir 110 63 661 650 11 5.6 Fujimori etal., 1976 Douglas-fir 100 56 478 466 12 6.1 Franklin (RS24) Douglas-fir 120 72 531 509 22 11.2 Santantonio(Wet) Douglas-fir 125 54 449 437 12 6.1 Gholz, 1979(III) Douglas-fir 130 90 792 772 20 10.2 Franklin (RS26) Douglas-fir 150 72 527 509 18 9.2 Gholz, 1979(IV) Douglas-fir 150 84 865 849 16 7.4 Gholz, 1979(II) Douglas-fir 150 90 786 762 24 12.2 Franklin (MR13) Douglas-fir 170 72 532 510 22 10.2 Santantonlo(Modal) Group average 71 604 585 19 9.7

Noble fir 130 98 880 862 18 9.9 Fujimori etal., 1976

Sitka spruce/hemlock 121 100 916 908 8 5.1 Grier, 1976 (Plot 12) Sitka spruce/hemlock 130 118 1,080 1,057 23 14.1 Cholz, 1979(IA) Sitka spruce/hemlock 130 111 1,492 1,460 32 20.2 Gholz, 1979(IB) Group average 110 1,163 1,142 21 13.4

Western hemlock 26 49 192 171 21 13.4 Fujimori,1971

Douglas-fir/hemlock 250 106 1,117 1,094 23 11.7 Franklin(MR 1) Douglas-fir/hemlock 250 99 991 968 23 11.7 Franklin(Bagby) Douglas-fir/hemlock 450 68 715 701 14 7.1 Franklin(RS 1) Douglas-fir/hemlock 450 84 911 893 18 9.2 Franklin(RS 2) Douglas-fir/hemlock 450 92 826 801 25 12.7 Franklin(RS 3) Douglas-fir/hemlock 450 99 1,223 1,203 20 10.2 Franklin(RS 28) Douglas-fir/hemlock 450 118 1,237 1,208 29 14.7 Franklin(PS 29) Douglas-fir/hemlock 450 116 1,137 1,107 30 15.2 Franklin(RS 30) Douglas-fir/hemlock 450 92 1,039 1,018 21 10.7 Franklin(RS 31) Douglas-fir/hemlock 450 129 1,423 1,392 30 15.2 Franklin(RS 27) Douglas-fir/hemlock 500 50 317 303 14 7.1 Franklin(MR 6) Douglas-fir/hemlock 500 81 590 567 23 11.7 Franklin(MR 5) Douglas-fir/hemlock 500 76 585 559 26 13.2 Franklin(MR 8) Douglas-fir/hemlock 500 65 606 586 19 9.7 Franklin(MR 4) Douglas-fir/hemlock 500 89 957 933 24 12.2 Franklin(MR 11) Douglas-fir/hemlock 750 79 927 908 18 9.2 Franklin(Squaw) Douglas-fir/hemlock 1,000 69 541 520 21 10.7 Franklin(MR 2) Douglas-fir/hemlock 1,000 98 789 760 29 14.7 Franklin(MR 3) Douglas-fir/hemlock 1,000 74 563 539 24 12.2 Franklin(MR 14) Group average 89 868 845 23 11.7

1 Bole, bark, and branches. 2Daniel Santantonio: personal counication; stands located on wet, modal, and dry sites in McKenzie River drainage of Oregon Cascade Range. J.F. Franklin: data on file at Forestry Sciences Laboratory, Corvallis, Oregon. "RS" plots are hectare reference stands or permanent sample plots located at elevations between 360 and 1,200 m on the H. J. Andrews Experimental Ecological Reserve in the Western Cascades of Oregon. "Bagby' is a plot in the Bagby Research Natural Area, Mount Hood National Forest, Oregon. "Squaw" is located in the Squaw Creek drainage, a tributary of the South Fork of the Santiam River, Willamette National Forest, Oregon. "MR" plots are hectare reference stands or permanent sample plots located at elevations below 1,200 m in Mount Rainier National Park, Washington. Forest Canopies: Complex and Independent Subsystems

George C. Carroll

The growth of trees, indeed that of of such samples begins to deteriorate the all vascular plants, involves the transfer moment the water is collected, with the of matter and energy through two critical degree of alteration in water chemistry interfaces between the organism and its varying with the climate, the length of the environment: one between roots and the soil interval before the sample is processed, and a second between the canopy and the and the load of microbial cells and other atmosphere. Studies on the root-soil inter- suspended particulates in the water. Be- f ace have largely dealt with the movement yond this, the size of the collecting area of plant nutrients other than carbon, while for field samples is seldom adequate to investigations in the canopy have centered provide a sample large enough for multiple on carbon fixation and energy budgets analyses (Lewis and Grant, 1978). Use of (Monteith, 1975). Where the movement of small sampling areas generates high varia- nutrients across the canopy interface has bility in the data and requires that large been investigated, the canopy has been re- numbers of collectors be installed to pro- garded as a homogeneous black box for which vide estimates of satisfactory precision at only total inputs from the atmosphere and a stand level (Kimmins, 1973; Best, 1976). forest floor and total outputs to the forest Most of the throughfall studies in the floor can be known. Thus, multiple ex- literature provide insufficient information changes of substances within the canopy it- about sampling design, collector construc- self and the processes which mediate such tion, and/or sample processing to allow con- exchanges have largely been ignored. sistent interpretation of the results. Even the measurement of net inputs and Lewis and Grant (1978) have discussed outputs for the canopy subsystem has often this entire array of difficulties with ad- proved fraught with difficulties. The col- mirable succinctness and have proposed an lection, sorting, and chemical analysis of improved design for throughfall collectors. litterfall is a time-consuming and expen- WhIle use of such collectors will resolve sive task which has burdened ecosystems certain of the problems discussed (adequate investigations since their inception. In sample size, collection of snow), they do moist climates substantial amounts of not help with the fundamental quandary of material may move from the canopy to the sample integrity versus cumulative collec- forest floor in solution or in suspension. tions. The only truly satisfactory method While an exhaustive review of the litera- for handling throughfail involves immediate ture on elemental cycling in stemfiow and filtration of the water through microbio- throughfall is be;ond the purview of the logical filters and freezing the filtrate present discussion, some mention of the prior to analysis; if tared filters are problems involved is in order, if only to used, estimates for the microparticulate justify the microcosm experiments discussed fraction in throughfall can also be gener- in this paper. Many of the difficulties ated. Such an approach is labor-intensive associated with througofall/stemflow col- and can only be used on an episodic basis. lection and analysis relace to the necessity Because concentrations of substances in for a cumulative sample if seasonal or canopy wash change over short intervals annual totals are to be generated for ele- during the course of single rainstorms and mental budgets. Collectors conLining water seasonally, from one rainstorm to the next, are left in the field for periods varying data from single-storm episodes or portions from one day to four ; the integrity thereof cannot be simply extrapolated to provide annual totals.

F!A 88 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Even if such extrapolations were legiti- menziesii (Mirb.) Franco) trees located at mate and if the data reported in the litera- two sites within the H. J. Andrews Experi- ture could be regarded as an accurate re- mental Forest. Both sites were located in flection of real nutrient exchanges, most stands corresponding to the Tshe/RhmalBene investigations of elemental cycling in community type (Franklin and Dyrness, 1970) stemfiow ind throughfail suffer from a and were composed predominantly of 400- to fundamental debility: they are essentially 500-year-old Douglas-fir trees. Samples descriptive and empirical, and as such they were taken from the canopies of permanently lack predictive power. The information rigged trees (Denison et al., 1972) and from such studies is peculiar to the forest stored overnight at the laboratory at 4°C. stands, seasons, and climatic conditions for The following day they were picked clean, which it was garnered. Consequently, few placed in funnel assemblies, and misted for inferences are possible from existing one at 16°C with previously collected studies about probable nutrient exchanges incident rainwater that had been stored in canopy wash from different forest stands frozen until just prior to use. After mist- under a different climatic regime. Thus, ing, the leachates were filtered sequen- the basic measurement of nutrient concen- tially through 30 pm nylon mesh and Nude- trations in precipitation, stenflow, and pore filters with 0.2 jm pore size; aliquots throughfail must be repeated each time a were removed for cation, total dissolved new ecosystem is studied. This will con- solids, and total nitrogen determinations; tinue to be the situation as long as we the remainder of the filtrate was lyophi- regard the canopy as a black box, as long lized, reconstituted to 10 ml, and stored as we lack basic knowledge of the processes at -20°C for subsequent analysis. In some involved in nutrient exchanges as incident cases where nitrogen concentrations were precipitation flows and trickles over extremely low, determinations of total canopy surfaces. nitrogen were carried out on the lyophilized samples. A flow chart is presented in Figure 1 NUTRIENT EXCHANGES IN AN OLD- and a synopsis of analytical methods with GROWTH CONIFEROUS CANOPY references is shown in Table 1. In all cases net fluxes of materials were computed During the last ten years, as a result by subtracting concentrations of substances of pioneering work of W. C. Denison and his in the control rainwater from those in the colleagues, access techniques for the can- corresponding leachates and by correcting opies of old-growth Douglas fir trees have for the amount of water with dissolved been developed, and a large amount of substance retained by the components in the information is available on the bionass and funnel assemblies. In order to assess the distribution of various canopy components possible magnitude of nutrient transfers (Denison et al., 1972; Denison, 1973; Pike mediated by the canopy solution, we initiated et al., 1975; Pike et al., 1977). The a biweekly, and later a monthly, sampling availability of accessible, described and laboratory misting program. canopies has permitted me and my colleagues We have misted Lobaria oregana, moss to make a more analytical approach towards holsters, 2- to 3-year-old foliage and estimating annual nutrient fluxes in the twigs, dead twigs, and living twigs 0.5 to canopy wash. In brief, we hope to construct 2.0 cm in diameter from three heights in the simulation models of nutrient fluxes in the canopy during each regular sampling epi- canopy solution, based on experiments with sode. The sample has been expanded to in- laboratory microcosms in which isolated clude 1-year-old foliage, 5- to 7-year-old canopy components are misted with rainfall foliage, trunk bark, Alectoria spp., and nutrient concentrations in the water Sphaerophorus Platismatia glauca, are monitored before and after contact with Hypogymnia spp., and Lobaria pulmonaria on the canopy sample. After describing our a quarterly basis. Occasionally we have progress and comparing results with those misted rotting Lobaria thalli, both from the from the pertinent literature, I will dis- canopy and from the forest floor. This pro- cuss the role of insects in the system gram has provided information in fluxes of briefly. cations (Na+, K+, Ca, Mg), total organic nitrogen, and total phosphorus both in dis- solved and particulate form. Subsequently, Nutrient Exchanges in the we have carried out prolonged misting experi- Canopy Solution ments with some of the dominant canopy com- ponents. Since the data for the cation Materials and Methods. All studies fluxes have been treated differently from described were carried out with samples those for other nutrients, they are dealt from old-growth Douglas fir (Pseudotsuga with first. G. C. CARROLL 89

Results: cations. Information on 1. Uptake of Ca and Mg from the cation fluxes was analyzed and summarized incident rainwater occurs quite commonly by my colleague, Dr. L. H. Pike, for the bi- for the four components regularly tested. weekly misting episodes from September 1976 Uptake of Na+ occurs less commonly and seems through August 1977. A multivariate to be restricted to Lobaria and moss; uptake approach was taken in attempting to assess of K+ occurred only once in all the samples the importance of several factors which may monitored. influence cation fluxes from canopy com- 2. Generally, the concentration of ponents. Specifically, multiple regressions cations in the incident rain is the most were carried out with cations concentration important independent variable in the multi- in incident rainwater, day in the water year ple regressions. In virtually every case an when samples were collected, presence or increase in the concentration of a cation in absence of at least 2.0 cm rain 1;the three the incident rainwater has resulted either days preceding sample collection, and height in increased uptake or decreased leaching of sample in the canopy as independent of that cation by the canopy component. variables and mean net cation flux as the 3. The leaching of Na+ and K+ from dependent variable. This information is foliage and of Na+ from twigs is strongly summarized in Table 2. We do not ascribe influenced by the day in the water year great significance to the absolute numbers when the samples were collected, with leach- in the upper portion of the table, but many ing losses decreasing with increasing ex- of the trends are highly significant, with posure to rain in the field during the fall the r2 in the multiple regressions often and winter. and + greater than 0.7. Actual plots of Ca 4. Loss of Kfrom the lichen 5± fluxes for Lobaria oregana are provided Lobaria oregana is strongly affected by the in Pike (1978). occurrence of rain in the three days prior Reference to Table 2 reveals several to sample collection (leaching losses de- general trends: creased after rain) and by the height in

fresh wt. * start sample storage cleaning misting collection determination * **

wet wt. determination 02 30um par tic u Ia tes

drywLof measure drying; drywt. volume of tared filters filtrates determination

Ii! 1 digestion; N, P total dissolved and cation solids analysis determination

other organic ano'ses

total P P I a------reconstitution conductivity It rates protein I lyOPhitization&JtolOmls. j pOlyols cations total N

Figure 1. Flow chart for processing and analyzing canopy samples and leachates. Table 1. Synopsis of chemical analyses for leachates -n'.0 Analysis Method Nature of sample No. of samplessampling per period 1U)0,r'l Suspended 0.2-30particulates, m Serial filtrationweights+ 0.2 pin ofthrough Nucleopore material 30p onmeshfilters; tared dryfilters No prior treatment 36 + 2 controls m-TiLI) Leachate volume Measured in graduated cylinder Filtered leachate 36 + 2 controls -a(I,rn Pigment (post_filtration 0.D. reading (A=410 mm) Filtered leachate 36 + 2 controls 1'-Im Total dissolvedoptical solids density) Evaporation foilof 5 boatsml aliquots (tared); in subsequenttin- Filtered leachate 36 + 2 controls m(I,-n pH Beckman pHweights meter of tared boats Filtered, samples pooled 9 + 1 control C,,C-)rn Conductivity Markeon conductivity meter i Filtered, samples pooled 9 + I control rn-LI) Total organic nitrogen Perchlorjc acidaliquots; digest N ofdetermined 200 as NH4+ by Filtered, samples pooled 9 + 1 control IC,, ++ ++ ) indophenol1974) blue method (Jaenicke 9 + 1 control TotalCations phosphorus (Na+,g+ ,Ca ,Mg PerchioricAtomic absorption acidbluealiquots; digestmethod sPectrophotometry P of(Jaenicke,determined 200 il 1974)by molybden FilteredFiltered, centratedsamples pooled to 10 ml pooled, con- 9 + 1 control Total protein Measurement bindingSedman595of absorptionon byand Coornassie increase Blue at G-250 on to protein (Bradford 1977) 1976; Filtered, centratedpooled, con- to 10 ml 9 + 1 control Total polyols Periodate hydephotometricoxidation(A57o formed nm) followed usingdetermination(Tibbling, chromotrophic 1968) of formalde- acid Crossberg, by spectro Filtered, centratedpooled, con- to 10 ml 9 + 1 control G. C. CARROLL 91

the canopy where the sample was collected In our initial consideration of data (leaching losses less for samples collected from our biweekly and monthly misting pro- high in the canopy). Pike (1978) has pro- gram we discovered that the meteorological vided a chart of these trends. history of the samples prior to collection Similar trends have already been re- greatly affected fluxes of particulate and ported or can be inferred from other reports dissolved nitrogen from canopy components. in the literature. For instance, studies To assess the susceptibility of various com- ponents in canopy leaching, misting episodes by Lang, Reiners, and Heier (1976) have + documented uptake of and losses of K were designated "Wet" (>0.5 cm rain in three from thalli of Platismatia glauca, a chloro- days preceding sample collection) or "Dry" phycophilous lichen. Throughfall studies (<0.5 cm rain in same period), and the data of Abee and Lavender (1972) have shown that for biweekly (9/20/76 - 12/27/76) and concentrations of K+ in the throughfall monthly (1/10/77 2/12/78) episodes were decrease greatly during the course of a lumped accordingly. Figures 2 through 5 rainy season in the Pacific Northwest. show these data in summary form. Although Particulate matter >0.2pm <3Opm col- the standard errors are high for some com- lected from these misting episodes has not ponents, several striking trends are evi- been analyzed for cations. Where concen- dent: trations in solution are low (e.g., Mg), 1. Net fluxes of both dissolved and fluxes in particulate form may completely particulate nitrogen are high for cyanophy- overshadow the effects reported here. If cophilous lichens and relatively low for such material is derived from microepi- tree components. Nitrogen content for phytes, it may be extraordinarily efficient filterable solids = microparticulates varies in cation uptake; this has been well demon- from 3 to 4 percent. strated by Odum et al.(1970) and Witkamp 2. Chlorophycophilous lichens and (1970) for microepiphylls in a tropical rain moss bolsters take up dissolved nitrogen forest in Puerto Rico. In any case, as from the incident rain. Table 2 makes clear, the multiple exchanges 3. Fluxes of dissolved nitrogen are of cations in a canopy can be affected by a higher for "dry" episodes than for "wet" number of factors, and any predictive episodes; for particulate nitrogen this models for cation fluxes in real canopies pattern is reversed. These trends are will be necessarily complex. particularly striking for cyanophycophilouS Results: nitrog. The canopies of lichens. the stands studied here contain large popu- 4. Older foliage tends to leach more lations of cyanophycophilous lichens which dissolved nitrogen than younger foliage. are capable of fixing nitrogen (Pike et al., The differences in leaching patterns 1977; Caldwell et al., 1979). Because such between wet and dry episodes suggest that stands are frequently nitrogen-limited, the important changes in the leaching potential flow of fixed nitrogen through the canopy of canopy components occur during the transi- has been a focus for our laboratory and tion from a dry to a wet canopy. We in- field studies and related modeling efforts. vestigated this transition by monitoring Total organic nitrogen in solution has been nutrient fluxes during prolonged (6-48 hr) analyzed by an extremely sensitive micro- laboratory misting experiments. Our method which involves block digestion of results for one such experiment with Alec- 0.2 ml samples with 25 p1 of perchloric acid toria (a chlorophycophilous lichen) and and which can reliably detect as little as Lobaria (a cyanophycophilou3 lichen) have 0.03 pg of nitrogen (Jaenicke, 1974). The been discussed by Pike (1978). For Alec- colorimetric reagents are added to the same toria, dissolved nitrogen is taken up from tube in which the digestion is carried out. the incident rainwater almost from the The analysis is simpler, faster, and far start of the experiment, while particulate more sensitive than the conventional micro- nitrogen is released. For Lobaria, an Kjeldahl digestiou followed by ammonia dis- initial pulse of leaching releases nitrogen tillation; it deserves to be widely adopted to the incident rain; after 2 to 3 by laboratories where organic nitrogen and (1-1.5 cm rain), uptake from the incident ammonia are of interest. Nitrate concen- rain commences, and when cumulative net trations in throughfall have been found to flux for a prolonged experiment is plotted, be very low in the Pacific Northwest, so the Lobaria is also found to be a net sink nitrate was not analyzed in this study. for dissolved nitrogen (Figs. 9-10). While Organic nitrogen in particulate matter was cumulative nitrogen output in particulates determined by digesting with a conventional only partially compensates for uptake of Kjeldahl procedure tared NuclepoLe filters dissolved nitrogen in Alectoria, the two on which microparticulates had been col- quantities are roughly equivalent in lected and by measuring the nitrogen in the Lobaria. More recent misting experiments digest spectrophotometrically as described have shown similar patterns for other can- above. opy surfaces, notably 2- to 4-year-old Table 2. Trends in net cation fluxes from four canopy components as influenced by several independent factors1 N)LU Lobaria Moss (2-3 yrs)Foliage (0.5-2.0 cm diain.)Dead twigs -V)'1 T1 Data from misting episodes Ca Mg Na K Ca Mg Na K Ca Mg Na K Ca Mg Na K v)-nrn Mean net flux (ng± SX g-ml') -10.1 ±1.7 -1.5±0.39 ±3.9 10.0 ±13.6131.5 ±4.111.5 ±0.65 1.7 ±5.116.8 ±18.1 95.7 -5.1±2.1 ±0.23 0.60 ±1.510.2 ±3.452.7 ±1.9 2.8 ±0.21 ±1.41.23 9.75 ±5.552.2 C,-)rn Mean controlconcentration rainwater (ppm) .90 .19 1.56 .66 .88 .19 1.60 .58 .93 .18 1.53 .57 .92 .19 1.69 .55 ni-IC-)rn No. of samples showing: UptakeOutput 38 4 3111 1131 42 0 28 8 1125 33 9 35 1 2016 28 8 36 0 36 0 27 9 29 7 32 4 36 0 m(-I) T1 Factors affectinc net fluxes inCation incident concentration rainwater (1) (1) (1) (1) (1) (1) (1) (1) (3) (1) (1) + (2) ni-< WetDay or in dry water period(Sept. year 1 = Day 1) + + (2) - + + (4) + (2) - (1) (1) + (2) (2) (1) V)I- Height in canopy(Dry = 0, Wet = 1) (2) (4)(3) (2)(1) (2)(3) (2)(3) (3) (2) (2) (2) (3) Maximumvariablesregression r2 in with multiple above .79 .78 .81 .26 .61 .76 .76 .89 .40 .39 .60 .85 .34 .50 fieldBlankindicate duringspaces order threeindicate of entrydays no prior intosignificant multipleto collection; effect. stepwise samples regression 1+from and dryand, - indicateperiods by extension, werethe directionexposed relative to of 0.3importance cm or less in influencingprecipitation. cation fluxes. change in flux with increasing values of the variable listed.Samples from "wet" periods were exposed to 2.0 cm or more precipitation in the Numbers in parentheses G. C. CARROLL 93

E 0) 0) z 0

D

0 z

lopuloor 1.5-2 Fl F2-3 F5-7 barkDO-i 01-2 moss aIsp hysp pIsp spgi Figure 2. Mean net fluxes of dissolved nitrogen from canopy components collected during dry periods. Less than 0.3 cm of rain fell in the three days preceding collections. Bars indicate one standard error above and below the mean. lopu = Lobaria pulmonaria; loor = Lobaria oregana; roor = rotten Lobaria oregana; L.5-2.0 = living twigs 0.5-2.0 cm in diameter; Fl = age class 1 foliage, 0-1 yr old; F2-3 = age classes 2-3 foliage; P5-7 = age classes 5-7 foliage; D0-1 = dead twigs 0-1 cm in diameter; Dl-2 = dead twigs 1-2 cm in diameter; alsp = Alectoria app.; hysp = Hypogyrnnia spp.; plsp = Platismatia spp.; spgl = Sphaerophoros globosus.

N Net Fluxes - Wet Episodes

U3 Cyano - Tree Components Moss Chioro- phycophious I phycophilous Lichens I Lichens EU2 I I I I

0) I

I 0) I

I I I 0.1

! 4 z I i .4 4 I x o 2 I I U-

0 I I z -° I

loorroor 15-2F2-3 F5-7DO-i mass hysp plsp Figure 3. Mean net fluxes of dissolved nitrogen from canopy components collected luring wet periods. More than 2.0 cm of rain fell in the three days preceding collections. Bars indicate one standard error above and below the mean. Code names for canopy components are the same as in Figure 2. 94 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

FS Net FluxesDry Episodes

6

E

) Cyano- Tree Components Moss Chiorophycophilous phycophilous Lichens 4 Lichens I',

x 2

Z +

o I . ? ? lopu loor 1.5-2 F2-3 F5-7barkDO-i 01-2 moss alsphysp plsp spgl

Figure 4. Mean net fluxes of filterable solids <30 pm >0.2 pm from canopy components collected during dry periods. Less than 0.3 cm of rain fell in the three days preceding collections. Bars indicate one standard error above and below the mean. FS = filterable solids. Code names for canopy components are the same as in Figure 2. G. C. CARROLL 95

FS NetHuxesWet Episodes

14.

13_

::

I I

I - I

Tree Components Moss Chlorophycophilous Iichens

o

I x I I

-5.U- I I

Cyano-

3- phycophilous I Lichens

I I I 2_

1 + .

Lor Ror 12 F2'-3F57 Dd-1 Mss Hy1spPI'sp

Figure 5. Mean net fluxes of filterable solids <30 im >0.2im from canopy components collected during wet periods. More than 2.0 cm of rain fell in the three days preceding collections. Bars indicate one standard error above and below the mean. FS = filterable solids. Code names for canopy components are the same as in Figure 2. 96 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

foliage (Fig. 6), living twigs, and moss Examination of the microparticulate bolsters. For the tree components the net fraction from misting episodes with foliage fluxes per unit weight are lower than for reveals a large number of fungal and algal the epiphytes, and longer periods of mist- cells, which are also pre- ing are required before uptake of dissolved dominant on needle and twig surfaces nitrogen begins. (Bernstein et al., 1973; Bernstein and The behavior of canopy surfaces in Carroll, 1977; Carroll, 1979; Carroll et regard to their interactions with dissolved al., 1980). In fact the observed differ- nitrogen becomes more explicable when the ences between cyanophycophilous lichens nature of the released particulates is and other canopy components in efficiency examined. Particulates washed from the of dissolved nitrogen uptake can be largely surface of Lobaria and other cyanophyco- ascribed to the prevalence of on philous lichens consist almost exclusively lichen surfaces and of eukaryotic micro- of rod-shaped bacteria (Fig. 7); inspection organisms on other canopy surfaces: the of the surface of a Lobaria oregana thallus response time and doubling times for bacter- with the scanning electron microscope after ial cells are much faster than those for a misting episode reveals dense populations eukaryotic microorganisms. In summary, all of similar bacteria (Fig. 8). Caidwell canopy surfaces examined during leaching et al. (1979) have isolated and identified time-course experiments have proved ulti- bacteria from this substrate. They report mately to be net sinks for dissolved nitro- 5-10 x l0 colony-forming units (CFU)/g gen. For some components (chlorophycophilous from Lobaria collected during dry periods lichens) this involves nitrogen uptake by and 100-200 x l0 CFU/g during wet periods, the sample itself; for most other leaching observations consistent with data on out- substrates nitrogen uptake is mediated by puts of microparticulates during dry and epiphytic microorganisms whose cells are wet misting episodes in the laboratory. released into the rainwater as the popula- Pseudomonas fluorescens, Arthrobacter-like tions grow. rods, and Gram-negative aerobic rods were found to be dominant bacterial taxa on Lobaria thalli.

FOLIAGE yr 2-4 Time Course of N Flux during Leaching Episode

_...Dissolved N - -N in Filterable Solids

a)

20-

:: 200 400 600 O0

Cumulative Volume (ml)

Figure6. Cumulative net flux ofdissolved nitrogenfrom foliage age classes 2-4 yr during aprolonged misting episode. G. C. CARROLL 97

These results are consistent with the trend is clear: as multiple layers of data of Lang et al. (1976), who showed nitro- lichen are added to the microcosm, less and gen uptake as for Platismatia glauca, less nitrogen escapes in dissolved form and and with numerous throughfall studies show- more and more is released in particulate ing coniferous canopies to be net sinks for form, as bacterial cell mass. Similar dissolved nitrogen in incident rainfall experiments with other canopy components (Tamin, 1951; Voigt, 1960; Nihlgaard, 1970; revealed the same trend. Foster, 1974; Miller et al., 1976; Feller, In addition to laboratory time-course 1977; Cronan, 1980). This effect is parti- experiments, we attempted to monitor the cularly pronounced where glass wool plugs fluxes of nitrogen in the field during a have been inserted in the necks of the single rainstorm in February 1979. Samples collecting funnels to partially block the were taken from six 0.3 m2 throughfall entrance of microparticulate matter into the collection troughs placed at random beneath collecting funnel. a single old-growth tree (MINERVA) at one Given this consistency, one may ask of our collection sites in the H. J. how far the patterns of nitrogen uptake and Andrews Experimental Forest. Incident rain- loss observed for individual components in fall was collected in a single sampler microcosm rainstorms can be extended to located in an adjacent clearcut.Water actual canopies in the field, where multiple samples beneath the tree were taken at 1, layers of intermingled components are stack- 2,3, and 4 hours, those in the clearcut at ed to a depth of 40 to 50 m. Loading the 2 and 4 hours. Samples were filtered in the funnels with multiple layers of a single field and were stored on ice prior to canopy component prior to misting represents analysis. Although samples for the control a first approximation to the field situa- rainwater were not replicated in this pre- tion. Figures 9 and 10 show results from a liminary experiment, the trends in nitrogen prolonged misting of Lobaria oregana in fluxes are readily apparent in Figure 11: which different amounts of lichen were put nitrogen was taken up from the incident into the funnels. In Figure 9 a mean dry rain throughout the portion of the storm weight of 1.8 g per funnel was used; in that was monitored, a result that might Figure 10, 16.8 g per funnel was used. The have been predicted on the basis of our

Figure 7. Bacteria from a thallus of Lobaria oreqana collected on a Nucleopore filter as seen under the scanning electron microsopce (x 2,500). 98 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Figure 8. Bacteria on the surface of a Lobaria thallus as seen under the scanning electron microscope (x 1,800).

LOBARIA OREGANA (I)

Time Course of N Flux LOBARIA OREGANA (IV) ° during Leaching Episode Time Course of N Flux -- - DisoIned N - - - 40 during Leaching Episode - - - - N in FiIterobIe SoIid - -

30 60 - 0ioIvd N -- - - N n FilieobIe SoIid - - $

a' 40 -, 4,- ,0' 0 0) 3.

IL; Z 20 p

4, z 3. I,

0 200 400 6 800

Cumulative Volume (ml) Cumulative Volume (ml)

Figure 9. Cumulative net flux of nitrogen Figure 10. Cumulative net flux of nitrogen from Lobaria ore gana during a prolonged from Lobaria oregana during a prolonged misting episode; 1.8 g dry weight of Lobaria misting episode; 16.8 g dry weight of were placed in each funnel. Lobaria were placed in each funnel. 9. C. OLL 99

nt Rin

E

C 0 0 C

C U0

C

0) 0 z

2 3 4 Time (.hr)

Figure 11. Concentrations of dissolved nitrogen in incident precipitation and throughfall during the course of a single rainstorm in the field. microcosm experiments. However, when pat- These include: (1) nitrogen is the only terns of particulate output from the canopy limiting nutrient; (2) grazing of microbial are considered, the extrapolation fails. cell mass does not occur; (3) microbial Analysis of filter weights frotn the field growth is non-colonial; (4) the canopy experiment reveals an initial flux of strata are homogeneous; (5) nitrogen is not particulates out of the canopy during the lost from the system in gaseous form; and first hour of the storm and low levels of (6) the flow of nitrogen into microbial suspended particulates in the throughf all cells is unidirectional; i.e., losses of thereafter. An entire canopy is, of course, nitrogen from microbial cells do not occur. more complex than a funnel with several Although certain of these assumptions are layers of Lobaria. blatantly incorrect (no. 4 above), most of In an attempt to deal with this com- them are reasonable, at least over the time plexity and to resolve discrepancies be- span of a single storm event. Currently tween laboratory and field observations, we the model deals with the behavior of stacked have resorted to computer simulation models. strata of only one component, Lobaria My colleague, Dr. W. J. Massman, has oregana. developed a preliminary model of canopy Considering the assumptions and limi- nitrogen fluxes in which the paranount role tations of this model, the degree of of surface microorganisms in regulating qualitative agreement between the predic- nitrogen uptake and release is explicitly tions of the simulation runs and the ob- recognized. The model is based on chemo- served patterns of nitrogen flux in both stat theory, but has been generalized such laboratory and field is encouraging. that neither a constant dilution rate nor Specifically, runs of the model for just a a constant volume must he assumed. Further, single stratum show a rough agreement with the model allows for luxury nitrogen con- time-course experiments in the laboratory; sumption by microbes. Certain simplifying most notably, dissolved nitrogen is released assumptions have, however, been made. initially, but is taken up later as bacterial 100 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

growth and release of particulate nitrogen If the specific nitrogenous compounds commences. When several strata are stacked, leached from Lobaria were identified, radio- such that the output from one becomes the isotopes could be employed to follow their input for the next lower one, the model pre- fate in subsequent transformations within dicts that efficiency of uptake will in- the canopy. Cooper and Carroll (1978) crease, but that the output of particulates attempted to isolate and identify dominant will be delayed. With five strata in the organic nitrogenous compounds in Lobaria model, this delay amounts to four or five leachates. They found that simple pre- hours. Thus, for our field experiment liminary fractionation of the leachates by (Fig. 11) we might well have seem a pulse of means of dialysis and extraction in acetone particulates from the bottom of the canopy did not result in nitrogen enrichment in if the storm had been monitored for several any fraction; they concluded that a number more hours. During storms of short duration of different nitrogen-containing molecules the microparticulate fraction may never be were present. Ribitol, a five-carbon sugar- flushed from the canopy. Instead it may be alcohol, was, however, identified as a major left as a particulate residue as water component of these leachates. Subsequent evaporates from the tree, only to be washed studies have shown that ribitol accumulates from the canopy during the initial phases of in the thalli during dry periods and leaches the next storm. This process could well very rapidly in subsequent rainstorms. account for the observed flush of micro- The chemistry of organic molecular particulates at the beginning of the single transformations in the canopy is undoubtedly storm we monitored. extremely complex. A great deal of further Results: phosphorus and organic investigation is required before these matter. Concentrations of phosphorus and transformations can be understood, even in certain organic substances have also been broad outline. measured during laboratory misting experi- ments. In general, much lower levels of phosphorus than nitrogen are present in the Insects and Canopy Processes canopy solution; patterns of leaching and uptake resemble those for nitrogen. The In the last ten years the role of can- occurrence of higher levels of phosphorus opy in regulating growth of in throughfall than in incident precipita- trees in forest ecosystems has been investi- tion in coniferous stands has been widely gated by a number of workers. Such studies reported in the literature (Attiwill, 1966; have largely focused on the activities of Nihlgaard, 1970; Abee and Lavender, 1972; defoliating insects, particularly their Foster, 1974; Hart and Parent, 1974; effects on primary production (Franklin, Henderson et al., 1977). Although phos- 1970; Rafes, 1970; Reichle et al., 1973), phorus concentrations were so low in both and on elemental cycling (Kiminins, 1972; incident rain and throughfall during the Nilsson, 1978; Schroeder, 1978). Defoli- storm sequence mentioned earlier that no ating and sucking insects appear to be of consistent trends were evident, data from little importance in old-growth canopies. earlier studies at the same site in which However, in collaboration with an entomolo- throughfall and incident rain were field- gist, Dr. David Voegtlin, we have noted filtered indicate net losses of phosphorus subtle and pervasive effects of the fauna from the canopy. Thus, while microbial on nutrient exchanges within the canopy. uptake of phosphorus certainly occurs, phos- Materials and methods. Census work phorus is probably not a limiting element on canopy consumers was carried out over a for microbial growth in most canopies. 3-year period. Initially, we implemented a Fluxes of organic matter in the canopy biweekly sampling program in which import- have been little investigated here or in ant and distinctive canopy habitats were conventional throughfall studies. Where sampled on a cumulative or episodic basis. total organic matter or concentrations of More recently, intensive sampling of arthro- specific organic molecules have been deter- pod communities on needles and twigs has mined in throughf all and stemflow, they been carried out. The habitats sampled and have been found to be high and to account techniques used are summarized in Table 3. for a significant return of fixed carbon to Results: canopy arthropods. The the forest floor (Tamm, 1951; Carlisle, data from the arthropod census suggest that 1965; Carlisle et al., 1966; Gersper and the canopy fauna partitions the tree very Holowaychuck, 1971; Eaton et al., 1973). finely, both with regard to habitat type and Concentrations of ammonia and nitrate are phenology. To date, 1,200 to 1,500 taxa low in throughf all from coniferous stands have been collected, from 50 to 70 percent in the Pacific Northwest and the bulk of of them more than once. Only about 150 of nitrogen in solution is in organic form; these taxa can be considered common. In this also appears to be the case for phos- many cases they are abundant only in one phorus. habitat or during one particular season. SamplingTable 3. technique Biweekly sampling technigues, Douglas-fir canopy arthropod Technique description Numbertaken of andsamples location survey (Sept. 1976 samplingDuration ofperiod Sept. 1977) Information produced Sticky screens 20 cm2with screenshardware stikem of cloth¼"special coated 12 screens,theof 4 3lower, onhalyards each middle, run intoand Cumulative;left screens up 2 weeks Qualitative theinformation movement onand phenology upper canopy movementevidenceofingthropods, flying by spidersbyfor insects suchwingless intercanopy as provides balloon- ar- Tuligren A series ofwhich lightfunnels use above heat to and drive 9 samples systemsystem);(3 per inbranch onelower, branch middle, Episodic; takenevery 2 weeks Quantitativeinicroarthropodsepiphyte-lodged information inhabiting onlitter- Vacuum A backpackwith blowercollectingarthropods the intake vesselinto a 3 samples,faceand foliage upperarea sur-ofcanopy branch Episodic; taken Semi-quantitativeperched soilinforma- habitat adapted for sucking andsystems filtration used for vacuumed tullgren every 2 weeks movingtwigs.foundistion estimated) (surfacearthropodson the needles onarea notarthropods vacuumed col-and Collects rapidly Filtration Branchiets washedfilteredorously vig- andthrough the washa 6 samples,from3 3dead living branch branchiets and systems chosen used Episodic; everytaken 2 weeks Quantitativeassociatedslowerlected information bymoving other with onorganisms techniques.foliage Table 3 continued on next page series of nested sieves for tullgren and vacuum and dead branchlet material C-,P D1I- Table 3. Biweekly sampling techniques, Euglas-fir canopy arthropod survey (Sept. 1976 - Sept. 1977) N.) Sampling technique Technique description Numbertaken ofand samples location samplingDuration ofperiod Information produced Cr,-1(-I)P1Q Pitfall Plastic containers hung 4 samples, located from Cumulative; fluid Qualitative information on T1 ethylene-glycolcontainin cavities water-alcohol- on trunk, mixture lower to upper canopy weekschangedin containers every 2 movementthe trunk of arthropods on =(-I)P1 Trunk stickies Screens ofhung sameto trapfrom size arthropodshalyards, as held 4 samples, locatedthe four near pitfalls Cumulative;left screens in place 2 Qualitativemovement information of arthropods on on C)P1Cl)rn fromapproximately trunk 1 cm away weeks onthe trunk trunk of andflying also insects landing P1Cd-) C1 Blacklight A large funnelinto trap canopy run on halyard 1 sample, nighttrap runevery one 2 weeks Episodic;hours 8-12 Qualitativenight-flying canopy.information insects on in the Funnels fixed so mC) abovelightthat it,only 42 insects m, can flyingsee the m1(I)Cd-, Emergence traps Tent-shaped traps set 6 samples, traps located Cumulative; traps Qualitative information used C- on forest floor screenshalyardsin vicinity and stickyof tree with weeksleft in place 2 whichassoilthe a meanscanopyinsects of come collecteddetermining from the in Cr) Cookie cutter Equal sizeduniform1 dm2samples taken habitat from a 4 samples,canopyinlarge taken lower moss from to bolstersmiddle Episodic; everyonce month Quantiativemicroarthropods uniforminformation habitat on in a fairly G. C. CARROLL 103

Distribution throughout the canopy is often the canopy. Bernstein and Carroll (1977) highly aggregated. The major groups of and Carroll (1979) made visual estimates of arthropods and the techniques used to col- microbial standing crops for various age- lect them are listed in Table 4. classes of needles at several heights in the In terms of abundance, microarthropods canopy, where mites are most abundant associated with needles and twigs were the (Voegtlin, unpub.). When microbial standing dominant group in the canopy. Mites, in crops are considered with regard to needle particular a new species of Camisia, Camisia age, a striking pattern frequently emerges. carrollii Andre, were very numerous on Percent cover and cell volume per needle needles and small twigs. Microscopic obser- rise steadily from year 1 through year 3 vations of both frass and gut contents re- and then drop precipitously on year 4 vealed that these organisms feed almost needles. The microbial populations then exclusively on epiphytic microbial cells. return to peak abundance at year 8. More Fungivorous psocids and collembolans were recently these patterns have been confirmed also prevalent in the foliage. Numerous (Carroll, unpub.) using the method of small invertebrates, including tardigrades, Swisher and Carroll (1980), in which the rotifers, and testate amoebae were present hydrolysis of fluorescein diacetate and on various canopy surfaces. We did not release of fluorescein dye is used as an study this truly microfaunal community, but index of microbial standing crop. A these organisms presumably graze on popula- plausible explanation for such patterns tions of epiphytic bacteria. invokes grazing by foliar microarthropods, While we have no data on the intensity which feed selectively on needles 4 to 6 with which canopy microorganisms are grazed, years old. Andre and Voegtlin (in press) indirect evidence suggests that the canopy have noted that populations of the twig- microfauna may significantly affect standing dwelling mite Camisia carrollii are concen- crops of microepiphytes and thus indirectly trated on twigs 4 to 10 years old. Thus, affect patterns of nutrient exchange within

Table 4. Sampling techniques used during biweekly sampling and major categories of arthropods collected by each method

Arthropods Techniques Commonly collected Infrequently collected

Sticky screens Diptera, Neuroptera, Hymenoptera, Trichoptera, Plecoptera, Homoptera, Hemiptera, Coleoptera Acarina, Coilembola, Thysanop tera

Tullgren and Acarina, Collembola, Coleoptera Diptera larvae, Araneae, cookie cutter larvae and adults Pseudococcidae, Hymenoptera

Vacuum Acarina, Collembola, Thysanoptera, Coleoptera, Psocoptera Diptera larvae, larvae Homop tera

Filtration Acarina, Collembola, Thysanoptera, Araneae, Hymenoptera Diptera larvae, Lepidoptera larvae, Homop tera

Pitfall Collembola, Araneae, Phalangida, Acarina, Hymenoptera, Coleoptera, Diptera, Psocoptera Lepidoptera

Trunk stickies Araneae, Diptera, Phalangida, Acarina, Collembola Coleoptera, Psocoptera

Blacklight Lepidoptera (moths), Trichoptera, Ephemeroptera, Homoptera Plecoptera, Diptera, Coleoptera, Hymenoptera, Hemiptera

Emergence Diptera, Coliembola Hymenoptera r

104 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

there is precedent for such precise parti- pressure and, as a consequence, their popu- tioning of habitats among foliage- and twig- lations never build to levels which signifi- dwelling microarthropods. cantly affect the trees. Census studies by Voegtlin have shown a relative paucity of defoliatorsand suck- ing insects. Measurement of frass-fall CON CLUS IONS during periods of peak needle consumption in the summer suggests that less than 1 per- Studies in the canopy of an old-growth cent of the new foliage is consumed by coniferous forest have revealed biological caterpillars each year. Voegtlin (unpub.) communities whose diversity and trophic considers this striking aspect of old-growth structure resemble those found in the soil canopy insect communities to be a resultof and streams. Primary producer, decomposer, the large numbers of spiders, other pre- and consumer populations are all prominent dators, and parasitoids found in the canopy. and appear to function in elemental cycling During the winter months large numbers of within the canopy in a fashion parallel to We mycetophilid flies and adults of aquatic that in the soil and aquatic systems. insects are trapped on sticky screens. now have evidence for the operation of Studies with emergence traps reveal that mechanisms for the conservation of nutrients these insects originate in the forest floor within the canopy. With regard to nitrogen or streams, where they feed as larvae. these mechanisms involve the fixation of This input of adult insects from the forest atmospheric nitrogen by cyanophycophilous floor may provide a food source for spiders lichens, the loss of organic nitrogen from and other canopy predators during the winter such lichens through leaching, the uptake and early spring and serve to maintain their of leached organics from dilute canopy populations at high levels throughout the solution by microorganisms and other epi- phytes, and the consumption of a portion of year. Thus, herbivorous insects in these forests never experience a season in which the resulting microbial production by can- to develop relatively free from opy microarthropods. Thus, leached

SCHEME OF CANOPY NITROGEN FLOW

ATMOSPHERIC N2 SOIL N2 Loboria

bacteria 1c I cOnsumptiOn and decomposition lungi n needle feeders / rainfall

leaching of N /7 CANOPY SOLUTION predators

moss ''

consumption

bacteria on Lobo r a and moss Q 8 .8 non -cyanophilic needle and twig lichens mcroepuphytes mites. fly larvae. Collembola

micro litter frass, exuviae, carcasses micro micro litter litter transient litter litter Insects

FOREST FLOOR

Figure 12. Scheme of nitrogen fluxes in canopy. G. C. CARROLL 105

organics serve indirectly as a Lose for many the canopy inhabitants, wherever they occur canopy food chains.Conservation of nutri- within that climatic zone.Indeed, micro- ents within the canopy operates continually epiphytes are abundant on the leaves of against the force of gravity; in old-growth broadleaved tropical evergreens (Odum et stands canopy production must be balanced al., 1970; Reynolds, 1975), and several ultimately by a return of materials to the studies suggest that they function in up- forest floor (see Fig. 12). take of canopy nutrients just as those Microorganisms and epiphytes piay a studied in the Andrews Forest do (Odum Ct key role in regulating fluxes of nutrients ci., 1970; Witkamp, 1970).If the canopy from the bottom of the tree.These pro- nitrogen rncdel developed for the old-growth cesses are probably not of universal Douglas-fir trees in the Andrews Forest occurrence in forest stands, and therefore were to be tested in functionally similar it is of interest to consider the climatic forests elsewhere, evergreen broadleaved and biological factors which enhance develop- forests throughout the tropics and the gym- ment of these canopy pcpulations,A on- nosperm forests of New Zealand and South mary requirement for any system in which America should provide appropriate stands. leaching plays a role is the input of Closer to home, the nodel could be tested atmospheric moisture in the form of rain or by experimental manipulation of the canopy fog.Leaching is a solution process.In nutrient regime with fertilization or insect addition, poikilohydnic organisms such as defoliation programs.Such an approach lichens, mosses, and microepiphytes require deserves serious consideration. periodic additions of liquid water in order to survive.As a result, the processes described above will not be of much import'- ACKNOWLEDGMENTS ance in desert environments withi.Oapre- cipitation or in subarctic and subalpine The original work cited in this review stands where much of the annual preciPitation has been a collaborative effort.In parti- is recieved as snow that falls from the cular I should like to acknowledge the con- canopy before melting.Beyund this, condi- tributions of Bra. William Denison, tions which lead to the availability of William Slessnan, Lawrence Pmkeand David fixed carbon and nitrogen in the canopy Voegtlin.Bill Honper, Terry Montlick, and solution will foster growth of heterorL'opliic Robert Rydol] nave dealt with computer pro'- microepiphytes.These conditions intude gramoming and data analysis.Fanny Carroll the prevalence of readily leached surfaces Judi Iioretmann. and Jan Wroncy have been such as those of older evergreen leaves and responsible for the laboratory misting ox- cyanophycophi loud lichens.Evergreen perioments and water analyses.Undergcaduate foliage persists for a number of years, work-study students have put in hundreds of providing addi tional surface area for the hours, in routine laboratory work and buildup of perennial colonies of micrcepf- analyses; our program would not have been phytes.Conversely, deciduous canopies in possible without their continuing contribu- which the leaves ore shed annually should tions.This work has been supported with show less evidence of nutrient uptake md funds from NSF grants BMS 7514003 end BED release by microbial cells.Other situa- 78-03583. tions where concentrations of macroelemencs in the canopy solution may be high involve: (1) aphid infestations, which are widely LITERATURE CITID reported to encourage the growth of yeasts and sooty molds on canopy surfaces coated Abee, A., and D. Lavender.1972.Nutrient with honeydew (Fraser. 1937; Reynolds, cycling in throughfall and litterfoll 1973); (2) outbreaks of defoliating insects in 430-yr-old Douglas-fir stands. 1mm (Kimmins, 1972; Nilsson, 1978; Schroeder, Research on Coniferous Forest Eco- 1978); (3) folior fertilization; and (4) systems, Proc. Symp. Northwest atmospheric pollution.In this final in-- Scientific Assn., edited by J.F. stance, the extent of nutrient enrichment Franklin, L. J. Dompster, and R. H. in precipitation from pollution is attested Waring, pp. 133-144.USDA Forest to by the enhanced growth of pigmented fungi Service, Pacific Northwest Forest and on painted surfaces in cities and by the Range Expt. Sta., Portland, Oregon. necessity for adding microbicides to paint to prevent such growth. Andre, H., and D. Voegtlin.1980. Some In view of the above considerations, observations on the biology of Camissia canopies of moist evergreen forests in carrollii Andre.Acarologia (in temperate and tropical regions should prove press). to be microbiologically active, whatever the specific identities of the trees and 106 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEMANALYSIS

Life in tall trees. Attiwill, P. M. 1966. The chemical com- Denison, W. C. 1973. position of rainwater in relation to Sd. American 228:74-80. recycling of nutrients in mature Rhoades, Eucalyptus forest. P1. Soil 24:390- Denison, W. C., D. M. Tracy, F. M. 1972. Direct, non- 406. and N. Sherwood. destructive measurement of biomass and Bernstein, M. E., and G. C. Carroll. 1977 structure in living old-growth Douglas- Microbial populations on Douglas fir fir. In Research on Coniferous Forest Ecosystems, Proc. of Symp. of Northwest needle surfaces. Microbial Ecol. 4: Scientific Assoc., edited by J. F. 41-52. Franklin, L. J. Dempster, and R. H. USDA Forest Bernstein, H. E., H. M. Howard, and G. C. Waring, pp. 147-158. Service, Pacific Northwest Expt. Sta., Carroll. 1973. Fluorescence micro- scopy of Douglas fir foliage. Can. 2. Portland, Oregon. Microbiol. 19:1129-1130. Eaton, J. S., G. E. Likens, and F. H. Throughf all and stem- Best, C. R. 1976. Treatment and Biota of Bormann. 1973. an Ecosystem Affect Nutrient Cycling, f low chemistry in a northern hardwood Ph.D. thesis, University of Georgia, forest. J. Ecol. 61:495-508. Athens. Feller, M. C. 1977. Nutrient movement Bradford, M. M. 1976. A rapid and sensi- through western hemlock-western red tive method for the quantification of cedar ecosystems in southwestern microgram quantities of protein utiliz- British Columbia. Ecology 58:1269- ing the principle of protein-dye bind- 1283. ing. Analyt. Biochem. 72:248-254. Foster, N. W. 1974. Annual macroelement Caldwell, B. A., C. Hagedorn, and W. C. transfer from Pinus banksiana Lamb. Denison. 1979. Bacterial ecology of forest to soil. Can. J. Forest Res. an old-growth Douglas fir canopy. 4:470-476. Microbial Ecol. 5:91-103. Franklin, R. T. 1970. Insect influences Carlisle, A. 1965. Carbohydrates in the on the forest canopy. In Analysts of precipitation beneath sessile oak, Temperate Forest Ecosystems, edited by Quercus petraea (Mattushna) Liebl. P1. 0. E. Reichle, pp. 86-99. New York: Soil 22:399-400. Springer-Verlag.

Carlisle, A., A. H. F. Brown, and E. J. Fraser, L. M. 1937. Distribution of sooty White. 1966. The organic matter and mold fungi and its relation to certain nutrient elements in the precipitation aspects of their physiology. Proc. beneath a sessile oak canopy. J. Linn. Soc. New South Wales 62:35-56. Ecol. 54:87-98. Gersper, P. L., and H. Holowaychuk. 1971. Carroll, G. C. 1979. Needle microepiphytes Some effects of stemflow from forest in a Douglas fir canopy: biomass and canopy trees on chemical properties distribution patterns. Can. J. Bot. of soils. Ecology 52:691-702. 57:1000-1007. Hart, G. E., and D. R. Parent. 1974. Carroll, G. C., L. H. Pike, J. R. Perkins, Chemistry of throughfall under Douglas and N. A. Sherwood. 1980. Biomass fir and Rocky Mountain juniper. Amer. and distribution patterns of conifer Mid. Natur. 92:191-201. twig microepiphytes in a Douglas fir forest. Can. J. Bot. (in press). Henderson, C. S., V. F. Harris, D. E. Todd, and T. Grizzard. 1977. Quantity and Cronan, C.5. 1980. Solution chemistry of chemistry of throughfall as influenced a New Hampshire subalpine ecosystem: by forest-type and season. J. Ecol. a biogeochemical analysis. Oikos (in 65: 365-374. press). Jaenicke, L. 1974. A rapid micromethod Cooper, G., and G.C. Carroll. 1978. for the determination of nitrogen and Ribitol as a major component of water phosphate in biological material. soluble leachates from Lobaria oregana. Analyt. Biochem. 61:623-627. The Bryologist 8:568-572. G. C. CARROLL 107

Kimmins, J. P. 1972. Relative contribu- Pike, L. H., R. A. Rydeil, and W. C. Denison. tions of leaching, litterfali, and 1977. A 400-year-old Douglas fir tree defoliation by Neodiprion sertifer and its epiphytes: biomass, surface (Hymenoptera) to the removal of area, and their distributions. Can. J. Cesium-l34. Oikos 23:226-234. Forest Res. 7:680-699.

Kimmins, J. P. 1973. Some statistical Rafes, P. M. 1970. Estimation of the aspects of sampling throughfall pre- effects of phytophagous insects on cipitation in nutrient cycling studies forest production. In Analysis of in British Columbia coastal forests. Temperate Forest Ecosystems, edited by Ecology 54:1008-1019. D. E. Reichle, pp. 100-106. New York: Springer-Verlag. Lang, C. E., W. A. Reiners, and R. K. Heier. 1976. Potential alteration of precipi- Reichle, D. E., R. A. Goldstein, R.I. Van tation chemistry by epiphytic lichens. Hook, Jr., and G. J. Dodson. 1973. Oecologia 25:229-241. Analysis of insect consumption in a forest canopy. Ecology 54:1076-1084. Lewis, W. M., Jr., and N. C. Grant. 1978. Sampling and chemical interpretation of Reynolds, 0. R. 1972. Stratification of precipitation for mass balance studies. tropical epiphylls. Kalikasan, Water Resources Res. 14:1098-1104. Philipp. J. Biol. 1:7-10.

Miller, H. G., J. M. Cooper, and J. D. Reynolds, D. R. 1975. Observations on Miller. 1976. Effect of nitrogen growth forms of sooty mold fungi. supply on nutrients in litter fall and Nova Hedwigia 26:179-193. crown leaching in a stand of Corsican pine. J. Applied Ecol. 13:233-248. Schroeder, L. A. 1978. Consumption of black cherry leaves by phytophagous Monteith, J. L., ed. 1975. Vegetation and insects. Amer. Midl. Natur. 100:294- the Atmosphere, Vols. I and II. New 306. York: Academic Press, Inc. Sedmake, J. J., and S. Grossberg. 1977. Nihlgaard, B. 1970. Precipitation, its A rapid, sensitive, and versatile assay chemical composition and effect on soil for protein using Coomassie Brilliant water in a beech and a spruce forest in Blue G-250. Analyt. Biochem. 79:544- south Sweden. Oikos 21:208-217. 552.

Nilsson, I. 1978. The influence of Swisher, R., and G.C. Carroll. 1980. Dasychira pudibunda (Lepidoptera) on Fluorescein diacetate as an estimator plant nutrient transports and tree of microbial biomass on coniferous growth in a beech Fagus sylvatica for- needle surfaces. Microbial. Ecol. (in est in southern Sweden. Oikos 30: press). 133-148. Tamm, C. 0. 1951. Removal of plant nutri- Odum, H. T., G. A. Briscoe, and C. B. ents from tree crowns by rain. Briscoe. 1970. Fallout radioactivity Physiol. Plant 4:184-188. and epiphytes. In A Tropical Rain Forest, edited by H. T. Odum and R.F. Tibbling, G. 1968. A routine method for Pigeon, pp. H-l67-H-176. USAEC Techni- microdetermination of mannitol in cal Information Center, Oak Ridge, serum. Scand. J. Clin. Lab. Invest. Tenn. 22: 7-10.

Pike, L. H. 1978. The importance of epi- Voigt, C. K. 1960. Alteration of the com- phytic lichens in mineral cycling. position of rainwater by trees. Amer. The Bryologist 81:247-257. Midl. Natur. 63:321-326.

Pike, L. H., W. C. Denison, 0. M. Tracy, Witkamp, M. 1970. Mineral retention by M. A. Sherwood, and F. M. Rhoades. epiphyllic organisms. In A Tropical 1975. Floristic survey of epiphytic Rain Forest, edited by H.T. Odum 3nd lichens and bryophytes growing on old- R.F. Pigeon, pp. H-l77-H-179. TJSAEC growth conifers in western Oregon. Technical Information Center, Oak The Bryologist 78:389-402. Ridge, Tenn. Aspects of the Microbial Ecology of Forest ECOsystems

Dennis Parkinson

INTRODUCTION time play a very important role in nutrient release from decomposing leaf litter. In Since the 1950's there have been regu- general, there is an increase in decomposi- mr and, at times, detailed studies of the tion rates in the t mperature "transect" microbial ecology of forest soils in which from pole to equator. Finally, the avail- most detailed attention was given to micro- ability of suitable decomposer organisms organisms in the organic horizon. In the is essential. It is well known that follow- initial studies a great deal of attention ing an initial weathering period, during was paid to the microorganisms isolated which time leaching of soluble nutrients from the different layers of the organic from freshl.y fallen litter occurs, the de- horizon. The fungi were, and in fact still composition process is effected by micro- are, the group of microorganisms most organisms and litter and soil invertebrates. studied, and attempts have been made to Therefore, interest has been re-directed to elucidate "successional patterns" of these the roles of decomposer organisms in litter organisms and their roles in decomposing decomposition and consequent nutrient cycl- leaf litter on the forest floor (Hayes, ing. 1979) Whilst the range of interactions be- Subsequently, interest became more tween invertebrate fauna and microflora has directed to the general phenomenon of been known for a considerable period of organic matter decomposition in forest time, only relatively recently have detailed soils. Through detailed studies, mainly studies been made in attempt to quantify using litter bag methods, information was these interactions and to assess their gathered on rates of organic matter decom- possible consequences in the cycling of position on a range of sites. From such nutrients in forest ecosystems. studies a number of generalizations have In this presentation attention will he been postulated (and have become part of centered on two aspects of forest microbial the lore of decomposition!). Quality of the ecology that have received considerable substrate(s) undergoing decomposition has attention over the past few years. Firstly, been shown to be a major factor governing to microbial biomass determinations in de- decomposition rates; there being a negative composing litter on the forest floor. This correlation of such rates with initial may appear to be a "perennial topic"; how- lignin content and C:N of the substrates, ever, new methods of obtaining reliable and a positive correlation with soluble data are being developed to allow better carbohydrate and (to a lesser extent) N and quantitative assessment of nutrient tie-up P contents. Climatic factors of temperature (and release) in the microorganisms. and moisture were found to be important Secondly, some comments will be made on governing factors. Thus, in dry exposed recent work on specific -fauna inter- sites decomposition rates were severely actions which may affect the pattern of restricted in standing dead material, but fungal colonization and decomposition of tended to increase within the soil profile. organic matter. Whereas in wet climates, decomposition A considerable body of excellent publi- rates of standing dead and surface litter cations is available in both these areas, were high but might decline with profile but this presentation will deal specifically depth. Of course, freeze-thaw and drying- with two case studies involving the author. re-wetting events over short periods of References to the research will be minimized.

fj 110 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

STUDIES ON MICROBIAL BIOMASS gations of the organic horizon of forest OF FOREST LITTER LAYERS soils (Parkinson et al., 1978). This method was used in a detailed One of the factors impeding the devel- study of three spruce (Picea abies) soils in opment of studies on the participation of the Soiling area of Germany, but only one microorganisms in forest ecosystems has site (a 95-year-old spruce site) will be been the lack of suitable methods for rapid- discussed here. Firstly, tests showed that ly assessing total microbial biomass in measurements on composite organic horizon soils and organic matter, fluctuations of samples could give an accurate index of the that biomass, and the relative contributions microbial biomass in the organic horizon of fungi and bacteria to this biomass. (L, F, and H layers). Then the Anderson Direct observation methods have been used and Domsch (1978) method was used on regu- in several studies of fungi in leaf litter larly taken samples (at least once per decomposing on the forest floor, but the month over 10 months) from the field, and techniques used (Frankland, 1975; Visser the effects of moisture content and temper- and Parkinson, 1975) are time consuming and ature of the organic horizon were investi- probably underestimate total lengths of gated under laboratory conditions. From fungal hyphae associated with the leaf these studies the following major points debris. Furthermore, in many cases, it is emerged: difficult to distinguish live hyphae from 1. Maximum total microbial biomass dead. The use of phase-contrast microscopy developed at about 15°C and in the 60 to partly overcomes the difficulty of dis- 80 percent moisture range. These data tinguishing hyphae with cell contents from allowed simple predictions for the spruce empty hyphae. Using this method, Frankland forest site which were testable against (1975) calculated that of the 289 ig fungi actual determinations on field samples. g1 L layer litter (deciduous woodland) March samples were taken at field conditions about 35 percent was "live" (possessed cell where the temperature of the organic layer contents), whilst Visser and Parkinson was + 1.5°C with 65 percent moisture, and (1975) calculated that the fungal standing from these data the predicted total micro- crop of L layer leaves in a Populus tre- bial biomass was 180.0 to 190.0 mg C 100 muloides woodland at the time of snowmelt gdwtl. In May the organic horizon temper- was about 1,421 mg dwt m2 with more than ature and moisture conditions were + 14.0°C 50 percent of observed hyphae containing and 65 percent, the predicted microbial protoplasm. biomass was 320.0 to 330.0 mg C 100 gdwt1, These data can be compared with those and the observed value was 304.0 ± 8.4 mg for live hyphal data obtained for oak-beech C 100 gdwt1. forest L and F layer litter of 79 to 82 per- 2. Seasonal microbial biomass changes cent and 15 to 20 percent respectively ranged between 194 mg C 100 gdwt1 (late (Nagel de Boois and Jarisen, 1971), and 76 to autumn-winter) and 310 mg C 100 gdwt1 (late 97 percent of observed mycelium being active spring-sumner). However, particularly in during initial stages of decomposition of autumn and spring when more marked diurnal beech leaves (Waid, Preston, and Harris, variations in temperature would be expected, 1973). However, Soderstrom (1979), using considerable microbial biomass variations fluorescent staining (fluorescein diacetate), would be expected and in fact were observed. TT1iT has recorded much lower values for In autumn, between 6 and 20 September total hyphae in soil (2-3%). microbial biomass increased by 48 percent, Direct observation methods, being time whereas in the next 10 days (20-30 Sept.) consuming in operation, are difficult to it fell by 7 percent and by late October apply in large comparative studies on fungal it had fallen by a further 32 percent. In biomass changes that require very frequent the spring, between 9-17 March there was a sampling (replicate). Chemical techniques 43 percent increase in microbial biomass have been developed for specific studies which was followed (17 March 4 April) by (e.g., chitin determination, Swift, 1973) a 27 percent fall. These periods would be or for general investigations (ATP deter- expected to be ones of a drastic changes minations). Recently Anderson and Domsch in nutrient tie-up and release. Gross (1978) described a rapid method for total calculations of C "tie-up" and release microbial biomass determinations in soil during the year (not taking into account samples, and when this method is coupled any "internal recycling" of C within the with the selective inhibition method decomposer complex) would indicate an over- (Anderson and Domsch, 1975) determinations all release of 105 mg C 100 gdwt1 organic of bacterial and fungal biomass are possible. horizon between 20 September and 9 March; While this total method was originally de- while, between 9 March and 6 June there was veloped for studies on agricultural soils, a C tie-up of 116 mg C 100 gdwt1. it has been valuable for detailed investi- 2. PARKI25ON 111

3. Considering the annual mean tem- of the recycling orml crob I fri carbon within perature (and the absence of limiting the complex decomposer system. However, moisture conditions at the experimental they do indicate the availability of site during the study period), an annual resources to support the level of microbial mean microbial hiomass of about 212 mg C biomass recorded. 100 gdwt' (or about 9.6 g microbial C m') The method of Anderson and Domsch could be expected. Selective inhibition (1978) was also applied to a study of three experiments indicated the average partition- spruce forests of different ages (Parkinson ing of the total microbial biomass was 77 et al., in press). In this study an attempt percent fungi and 23 percent bacteria. was made to asses direct relationships be- 4. In view of the comments made re- tween primary production parameters and de- garding the calculation of bacterial main- composer biomass and respiratory activity. tenance requirements and substrate available Fortunately, a considerable body of data for microbial growth in forest soils (Gray on the primary producers was available since and Williams, 1971; Hissett and Gray, 1976), the three chosen spruce sites were studied an attempt was made to assess the implica- in the German IBP (many of these data were tions of the annual microbial bioniass in published by Ulrich et al., 1974, and un- the organic horizon of the spruce forest. published data were provided by Dr. Heller). The following summary carbon balance sheet The ages of the three study Sites were could be made up: 48, 95, and 123 years. The highest above- ground standing crop was seen in the 95- Input of above year-old site and the lowest value was at

ground litter : 230 g C m2 yr' the oldest site. Aboveground productivity Estimated input of was highest at the youngest site; the root exudates lowest value was recorded at the oldest

and dead roots : 70 g C m2 yr' site. Output of leachates Estimation of annual productivity per from the H layer unit weight of standing crop (based on un- (data from Ulrich, pub. data, Heller, pers. comm.) yielded the

pers. comm.) : 34 g C m2 yr somewhat curious data given in Table 1, with the middle-aged site showing the low- i.e., in a 'steady state' condition (no est value. Table 1 also presents similar accumulation, no depletion) 266 g C m2 yr data based on estimations of standing crop would be available for microbial maintenance and productivity made in 1968 (Ulrich and growth. et al., 1974). However, in the 95-year-old spruce for- The total standing crop of roots in est studied it was more reasonable to assume the organic horizon was significantly higher that some organic matter accumulation was at the youngest site, and the proportion of still occurring. In comparing weights per mycorrhizal roots was also highest at this square meter of organic horizons of spruce site. forests of different ages in the Solling Data on the organic horizon at each area it was estimated that accumulation at study site are given in Table 1. These the study site could be occurring at the indicate that the contribution of L + F1 rate of 20 g C m2 yr. layers to the total organic horizon varied Therefore, 246 g C m2 yr would considerably from site to site (highest in actually be available for microbial main- the youngest site, lowest in the oldest). tenance and development. They also indicate variations from site to Data from selective inhibition studies site in percent C, percent N and C/N. From indicated that the average yearly total the data on total weight of organic matter microbial biomass of 9.6 g C m2 was made up (m2) of the organic horizon at each site, of 2.2 g bacterial C and 7.4 g fungal C. it would appear that the weight of the Assuming a yield coefficient of 0.5 and a organic horizon (or2) at the middle-aged maintenance constant of 0.001 hr1 (Hissett site (95 years), i.e., 4,545 g or2 was much and Gray, 1976), then: 56.6 g C or2 yr less than would be expected. Given the age would be available for bacterial maintenance of the site plus the data obtained from the and turnover, of which 38.5 g C m' yr1 other sites, 9,000 to 10,000 gdwt litter would be required for maintenance, leaving m2 would be expected for this site. 18.1 g C m2 yr' available for 'turnover' The data on basal respiration of the (which would allow a mean generation time total organic horizon material (measured at of about 45 days). 189.4 g C m2 yr 22°C) are given in Table 2. However, the would be available for fungal maintenance mean annual temperature for all sites was and growth. 6.2°C. Laboratory experiments at this mean Undoubtedly these calculations are annual temperature indicated that the loss primitive, as they do not take any account of carbon or2 yr' at each site would be 112FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Table 1. General data on primary producers and allied material for each of the study sites.

Site age 48 years 95 years 123 years

Aboveground standing crop 1968 (g m2) 14,300 24,446 23,500

Aboveground standing crop 1977 (g nr2) 17,741 26,884 15,823

Aboveground productivity 1968 (g m2 yr) 849 886 651

Aboveground productivity 1977 (g m2 yr1) 767 525 441

Productivity 1968 0.059 0.036 0.029 Standing crop

Productivity 1977 0.043 0.0195 0.028 Standing crop

Total weight (g m2) organic horizon 5,207 4,545 11,453

Percent contribution of L + F1 to organic horizon 10.3 7.3 5.8

Percent organic matter in organic horizon (composite) 83.6 75.8 69.3

Percent C 42.5 39.2 36.6

Percent N 1.6 1.4 1.3

Roots (<5 mm diam.) standing crop (g m2) in organic horizon 216 78 146

Mycorrhizal roots (g m2) 97 10 43

Table 2. Average yearly basal respiration of composite organic horizon samples from the three study sites (measurements made at 22°C)

Average yearly value

ml CO2 + 100 g dwt hr g C + f2 hr

48-year-old site 3.47 0.097

95-year-old site 1.80 0.044

123-year-old site 1.36 0.084 D. PARKINSON 113

approximately: 48-year-old site: 266 C Judging by the data in Table 1,the major m2 yr; 95-year-old site: 114 g C myr; differences between the three study sites 123-year-old site: 206 g C m2 yr1. were: General data on total microbial bio- 1. There was a higher contribution of mass at each of the three study sites are L + F1 layer material to the total organic given in Table 3. Selective inhibition horizon (10.3% at the youngest site, 7.3% at experiments indicated no significant varia- the middle-aged site, and 5.8% at the oldest tions in the percentage contribution of site). In a detailed study of the 95-year- bacteria and fungi to this total biomass old site, Parkinson et al. showed the L + F1 over the 10-month study (the ratio bacteria: layer material to be the locus of highest fungi remaining constant at 20:80). The biological activity and microbial biomass. data indicate that, on the basis of 100 Therefore, this greater contribution at the gdwt organic horizon samples, average total youngest site is probably an important microbial biomass was highest in the young- phenomenon in allowing the high values. est site and lowest at the oldest site. 2. The percentage carbon in the organic When calculated on a square-meter basis layer was highest at the youngest site, and this order was altered, the youngest site the C/N was narrowest. still holding the highest microbial bio- 3. There was a higher standing crop of mass but the middle-aged site holding the roots in the organic horizon of the youngest lowest. Similar relationships were ob- site. There were also considerably more served when considering data on maximum mycorrhizal rootlets in the F2 and H layers microbial biomass change at each site over of the youngest site than in the other the study period -- a parameter which is at sites. best crude because of the demonstrated Presumably this larger root standing short-term large fluctuations in total crop would, via exudates and sloughed-off microbial biomass in coniferous forest material plus input of dead roots, enhance organic horizons (Parkinson et al., 1978). microbial activity and development. A pro- By any form of calculation, the organic portion of the microbial biomass determined, horizon of the youngest site emerged as at least in the spring and summer samples, having both the highest activity (as indi- could be mycorrhizal fungal material (hyphae cated by basal respiration measurements in growing into the organic horizon from Table 2) and the highest microbial biomass mycorrhizal sheaths). (Table 3). Furthermore thevariations These factors at the youngest site are (both positive and negative) in total enhanced by the figures given in Table 1 on microbial biomass during the study period primary productivity per unit aboveground (Nov. July) were much greater at this site standing crop, where the youngest site gave than at the other two sites. Since the the highest values both in 1968 and 1977 important environmental factors of tempera- (0.059 and 0.043). ture and moisture content of the organic The oldest site which, on the basis of horizon at each site were essentially unit weight (100 gdwt) of organic horizon, similar, other reasons must be sought for had the lowest basal respiration and total the higher microbial activity and biomass microbial hiomass values, was also the site (plus fluctuations) at the youngest site. with the highest amounts of F2 and H layer

Table 3. Summary of total microbial biomass values in composite organic horizon samples from the three study sites.

Average yearlytotal microbial Maximum minimum biomassvalues bionass values

mg C 100 gdwt g C if2 mg C 100 gdwt gC m2

48-year-old site 571.9 29.8 342.7 17.9

95-year-old site 260.0 11.8 116.4 5.3

123-year-old site 209.7 24.0 84.6 9.7 Table 4. Summary of microbial and primary producer (and allied) data on a comparative, proportional basis respiration Basal Microbial (decomposer) parametersAverage total biomass biomassMax-mm Productivitystanding crop producer Roots(and <5allied) mm parameters butionPercent of contri- L + F1 U,-Ti 1. if2 U,ITi-n 48-year-old site 2.21.0 1.02.53 1.03.38 1.02.2 1.02.77 1.23L78 -C-,Uim 123-year-old95-year-old site 1.9 2.03 1.8 1.4 1.87 1.0 mVI-n 2. 100 gdwt1 C-)0rn 95-year-old48-year-old site 1.322.55 2.721.24 1.384.05 2.21.0 1.353.26 1.231.78 U,m-1Id,0 123-year-old site 1.0 1.0 1.0 1.4 1.0 1.0 VII- 0. PARKINSON 115

material per sample (and, natur.l1y, per lationships of primary producers and de- m2). The total amount of roots at this site composers, and further indicate the power was not significantly different from that of the physiological method (Anderson and found at the middle-aged site, but higher Domsch, 1978) for microbial biomass deter- amounts of mycorrhizal roots were present minations. as compared with the middle-aged site. The previous comments indicate some Data on aboveground productivity per unit interesting approaches, given a speedy standing crop (Table 1) at the oldest site method for microbial biomass assessment. changed only very slightly in the 1968-1977 The data can be further extended to con- period (0.0288 in 1968 and 0.0278 in 1977). sideration of nutrient cycling if knowledge However, similar data for the middle-aged of the other nutrients held in microbial site (Table 1) indicated a considerable tissue is considered (Visser and Parkinson, decline in primary productivity per unit 1975). Regrettably, too little is known on standing crop of primary producers during actual microbial turnover rates in forest the same period (0.036 in 1968 and 0.0195 in soils, the actual of 1977) the important soil bacteria and fungi, and When calculating microbial biomass on on death and decay rates of the various a square-meter basis for each site, it is components of the litter and soil microblota. impossible to deal with the paradox of the low total weight (m2) of the organic hori- zon at the middle-aged site. However, weights (m2) of the organic horizon at each study site compared with similar measure- ments obtained in 1968 (Ulrich et al., 1974) as follows: _Site A Site B Site C 1968 data (Ulrich et al., 1974) 5,200 g m 4,900 g m 11,100 g m 1976-1977 data (Parkinson et al., in press) 5,207 g m2 4,545 g m2 11,453 g m2

No significant change in the mass of organic horizon has occurred over almost a INTERACTION BETWEEN MICROFLORA decade. Does this mean there is a steady AND FAUNA IN FOREST LITTER state condition in this horizon at each site? Efficient organic matter decomposition Table 4 summarizes the comparative in the surface layers of forest soils is (proportional) relationships of several effected by the joint activities of the microbial (decomposer) parameters and pri- microflora and the soil fauna. Bacteria mary producer (and allied) parameters for and fungi are generally considered to play each site. The data are given both for unit by far the major role in the actual oxida- weights (100 gdwt) of organic horizon and tion of organic carbon, although it has been on a square-meter basis. These data rein- demonstrated that some of the soil animals force the comments made earlier on the three can act as agents of primary decomposition study sites. It is well known that chemical because they possess cellulolytic enzymes quality of litter substrates and input of in their guts. Nevertheless, the major material from roots (live and dead) are roles in organic matter decomposition attri- important factors in affecting decomposer buted to the soil fauna are: biomass and activity in any soil, and the 1. Transmission of microbial lnoculum data exemplify this fact for the three in organic matter. study sites. However, relationships between 2. Fragmentation of large pieces of primary productive vigour (productivity! organic matter, with the consequent in- standing crop) and decomposer activity and crease in surface area exposed for microbial biomass (per m2) are also indicated.While development. the proportional relationships of basal 3. Possible enhancement of microbial respiratory activity and primary producti- activity because of changes in the chemical vity per unit standing crop for the three constitution of organic material during sites are very similar, other relationships passage through the animal gut. are not as direct as might have been ex- 4. Possible effects (stimulatory or pected. The situation, particularly at the inhibitory) on the microflora as a result middle-aged site, has been complicated by a of animal grazing on that microflora. complex history of the vegetation (probably Among the fauna active in the organic prior to 1968). The data provided here layers of the forest floor are various indicate the type of parameters which should groups which, at least during part of their be considered in attempting to derive re- life history, consume microbial tissue. A 116 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS good deal of attention has been directed to hyphae. A food preference study (Visser the consumption of fungi by microarthropods, and Whittaker, 1977) confirmed that selec- and when attempts have been made to assess tive feeding by 0. subtenuis on sterile the actual amounts of consumption of fungi dark fungi did, in fact, occur. by various groups of these microarthropods Following this, the effect of grazing in field locations, the values obtained by 0. subtenuis on the two commonly record- have been frequently low. Various taxa of ed, potentially competitive, groups of the microarthropods that graze on fungi do litter fungi (Basidiomycetes and sterile not consume all species of fungi they dark forms) was investigated. A single com- selectively consume specific groups of the mon Basidiomycete species and a single com- mycoflora in decomposing litter. The mon sterile dark form, which possessed possible implications of this selective similar growth rates when grown on L layer grazing will be discussed later. leaf litter, were chosen for study. The Active consumption of microbial tissue microcosm experiments have been described by microarthropods could restrict nutrient in detail (Parkinson et al., 1977; in press), loss (via leaching) from decomposing organic so only the general conclusions will be out- matter. Further indication of role of soil lined here. The selective grazing by the animals as stabilizers of nutrient cycling Collembola could have significant effects comes from the evidence that these organ- both on fungal growth in the L layer leaf isms concentrate certain nutrient elements litter surfaces, and on the colonization by (K and Ca) in their tissues. Also the fungi of dead leaf material on the litter faeces of some microarthropods (particularly surface. In essence, the selective grazing mites) are slowly decomposed and thus nutri-. by the animals on the sterile dark fungus ents held in the faeces are only slowly re- tilted the balance of competition in favor leased (elemental leaching is retarded). of the Basidiomycete. An interesting addi- In a cool, temperate, deciduous forest tional fact is that the Basidiomycete used dominated by Populus tremuloides (Lousier in these experiments was apparently toxic and Parkinson, 1976, 1978 have given gen- to the test animals. The Basidiomycete was eral decomposition and nutrient dynamics of capable of actively utilizing cellulose this area), Mitchell (1976) calculated that whereas the sterile dark form was not, consumption of fungi by Oribatid mites was hence the selective grazing of the animals 6 g m yr1, a figure which represented could have very marked effects on the rate about 2 percent of the fungal standing and course of litter decomposition. crop. In this particular forest, Visser Thus grazing by invertebrates on fungi and Parkinson (1975) observed a high fungal in forest litter is probably a much more standing crop (1,421 mg dwt nr2) in the complex phenomenon than would appear from litter layer at the time of snowmelt quantitative studies on ingestion, i.e., (April), and that this standing crop rapid- relatively low grazing levels could have ly declined (to 786 mg dwt nr2) immediately magnified effects, if selective, by rein- following snowmelt. This quantitative forcing or switching competitive relation- change in fungal standing crop was accom- ships between litter fungi. panied by a significant qualitative change When Collembola are allowed to move in the fungal community in the L layer freely in microcosms containing sterile litter. Before snowmelt, Basidiomycetes leaves or coarse sterile macerate for 5 to were isolated with a frequency of about 3 10 days, it is found that when pieces of percent, and after snowmelt their frequency the sterile substrate are plated many of of occurrence was about 14 percent. Before them yield bacteria and/or fungi. With snowmelt, sterile dark hyphal forms were respect to 0. subtenuis, very few fecal isolated with about 26 percent frequency, pellets of this animal yielded fungi when but this feil to 14 percent after snowinelt. plated onto 2 percent malt agar (only 2 of At the same time, Collembola were observed 40 plated pellets yield fungi in this to be numerous and active in the litter case, a Mortierella even though they con- layer, suggesting that high grazing acti- tained fungal hyphae). Thus it appears that vity by these animals could be one factor the animals carry microbial "inoculum" on responsible for this decline in fungal their external surfaces and are efficient standing crop. spreaders of inoculum within organic matter. A detailed study showed that one Apart from this being an interesting and species of the Collembola (Onychiurus sub- potentially important phenomenon in nature, tenuis) was particularly frequent in the it does cause problems in studying, by surface organic matter during the snowmelt respirometric methods, the positive or period (about 4,500 animals m2 in the L negative effects of animal grazing on fungal layer). Examination of gut contents and of growth and activity in decomposing litter faeces indicated this species was selec- it has been suggested that grazing re- tively grazing on fungi possessing dark moves senescent hyphae and stimulates fungal growth. D. PARKINSON 117

This contribution has dealt with only Nagel-de Boois, H. M. ,and E. Jansen. two aspects of the microbiology of forest 1971. The growth of fungai mycelium organic matter. Topics such as wood de- in forest soil layers. Rev. Ecol. composition, inycorrhizal associations and Biol. Sol. 8:509-520. the biology of mycorrhizal fungi, nitrogen transformations and a range of intermicrobe Parkinson, D., S. Visser, and J. B. interactions are currently under detailed Whittaker. 1977. Effects of Collem- study. These studies will provide clearer bolan grazing on fungal colonization ideas on the detailed functions of decom- of leaf litter. In Coil Orms as poser organisms in forest ecosystems. Components of Ecosystems, Ecol. Bull. (Stockholm) 25:75-79.

LITERATURE CITED Parkinson, D., K. H. Domsch, and J. P. E. Anderson. 1978. Die entwicklung Anderson, J. P. E., and K. H. Domsch. 1975. mikrobieller Biomassen un orgamischen Measurement of bacterial and fungal Horizont eines Fichtenstandortes. contributions to respiration of selec- Oecol. Plant 13:355-366. ted agricultural and forest soils. Can. J. Microbiol. 21:314-322. Parkinson, D., K. H. Domsch, and J. P. E. Anderson. Studies on the relationship Anderson, J. P. E., and K. H. Domsch. 1978. of microbial biomass to primary pro- A physiological method for the quanti- duction in three spruce forest soils. tative measurement of microbial bio- Bakt. Centrbl. (in press). mass in soils. Soil Biol. Biochem. 10: 215-221. Parkinson, D., S. Visser, and J. B. Whittaker. Effects of Collembolan Frankland, J. C. 1975. Fungal decomposi- grazing on fungal colonization of leaf tion of leaf litter in a deciduous litter. Soil Biol. Biochem. (in woodland. In Biodegradation et Humi- press). fication, edited by G. Kilbertus et al. pp. 33-44. Sarreguemines, France: Soderstrom, B. 1979. Seasonal fluctuations Pierron Editeur. of active fungal biomass in horizons of a podzolized pine-forest soil in cen- Gray, T. R. G., and S. T. Williams. 1971. tral Sweden. Soil Biol. Biochem. 11: Microbial productivity in soil. In 149-154. Microbes and Biological Productivity. Symp. Soc. Gem. Microbiol. 21:255-286. Swift, M. J. 1973. The estimation of mycelial biomass by determination of Hayes, A. J. 1979. The microbiology of the hexosamirie content of wood tissue decomposition. Sd. Frog. decayed by fungi. Soil Biol. BiochEm. (Oxford) 66:25-42. 5:321-332.

Hissett, R., and T. R. G. Gray. 1976. Ulrich, B., R. Mayer, and H. Heller. 1974. Microsites and time changes in soil Data analysis and data synthesis of microbe ecology. In The Role of forest ecosystems. Gottinger Bodenk. Terrestrial and Aquatic Organisms in Ber. 30:1-459. Decomposition Processes, edited by J. M. Anderson and A. Macfadyen, pp. Visser, S., and D. Parkinson. 1975. Litter 23-29. Oxford: Blackwell Sci. Publ. respiration and fungal growth under low temperature conditions. In Biodegrada- Lousier, J. D., and D. Parkinson. 1976. tion et Humification, edited by G.

Litter decomposition in a cool temper- Kilbertus et al. , pp. 88-97. ate deciduous forest. Cam. J. Bot. Sarreguemines, France: Pierron Editeur. 54:419-436. Vlsser, S., and J. B. Whittaker. 1977. Lousier, J. D., and II. Parksinson. 1978. Feeding preferences for certain litter Chemical element dynamics in decom- fungi by Onychiurus subtenuis. Oikos posing leaf litter. Can. J. Bot. 56: 29:320-325. 2795-2812. Waid, J. S., K. J. Preston, and P. J. Mitchell, M. J. 1974. Ecology of oribatid Harris. 1973. Autoradiographic tech- mites in an aspen woodland soil. niques to detect active microbial cells Ph.D. thesis, University of Calgary, in natural habitats. In Modern Methods Alberta, Canada. in Microbial Eco), Ecol. Bull. (Stockholm) 17:317-322. The Dynamic Be!owground Ecosystem'

\V. F. Harris, Dan Santantonio, and D. McGinty

INTRODUCTION 200 t/ha, e.g., Rodin and Provdvin (n.d.) in Rodin and Bazilevich, 1967). Broad- Roots comprise the primary interface leaved and subtropical forest types are between plant and soil for uptake of water characterized by a maximum of 70 to 100 and nutrients. Much is known about the bio- t/ha dry weight of root organic matter chemistry, cell physiology, and membrane (Bazilevich and Rodin, 1968). Regardless physics associated with these important pro- of the type of forest, a consistent struc- cesses (Devlin, 1966; Larcher, 1975; and tural relationship exists between root and Pitman, 1976). In this paper we discuss shoot across a wide variety of environments the role of the belowground ecosystem, inhabited by trees (Fig. 3, Santantonio et especially the autotrophic root component, al., 1977). Researchers have used this re- in the structure and function of forest lationship to develop regression equations ecosystems. Beyond recognizing roles of to estimate the logarithm of root system anchoring terrestrial plants and uptake of biomass from the logarithm of stem diameter water and nutrients, this component of the at breast height. Consistent structural forest has been largely neglected in an eco- relations have been applied widely to esti- system context. In order to focus our dis- mate biomass of tree components from easily cussion on the properties of the belowground measured plant dimensions by using these ecosystem, we use the term "rhizosphere" to equations, an approach termed "dimensional include roots, mycorrhizae, microbes, and analysis" by Whittaker and Woodwell (1968, rhizophagus invertebrates. Each component 1971). The proportion of total biomass re- of the rhizosphere merits review and presented by roots is lowest for forests and speculation as to its own specific roles. ranges up to 90 percent for tundra and cer- However, we have chosen to develop our dis- tain grasslands. This is because forests cussion on the entire subsystem rather than accumulate large amounts of woody material individual components. Many answers to aboveground, whereas tundra and grassland questions we pose about dynamics of below- communities invest heavily into their ground subsystems rely on continuing structure belowground. Studies of root blo- research into detailed processes at organism mass have been summarized in reviews by and community levels. Ovington (1962), by Rodin and Bazilevich Roots comprise a substantial portion (1967), and by Santantonio and others (1977). of forest ecosystems, generally accounting The most reliable methods of estimating for 15 to 25 percent of total biomass. The total root biomass usually consist of a com- range of values reported for individual bination of excavation and soil coring tech- stands, however, extends from 9 to 44 per- niques. Root systems of a limited number of cent (Santantonio et al., 1977). The great- trees are excavated to develop logarithmic est amount of root biomass accumulates in regression equations to estimate large temperate old-growth conifer forests (over structural roots. Soil cores or soil mono- liths are taken to estimate small and fine roots on a unit area basis.

1Researchsupported jointly by the National Science Foundation'sEcosystem Studies Program under Interatency Agreement No. DEB-77-26722, and theOffice of Health and Environmental Research, U.S. Department of Energy, undercontract W-74O5-eng-26 with Union Carbide Corporation. Publication No. 1350 from the Environmental Sciences Division. 120FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Such a large amount of organic matter, usually based on an arbitrarily chosen dia- accumulated at considerable metabolic ex- meter ranging from 1.0 to 10 mm. These pense, clearly could serve several purposes, roots are distributed in upper soil layers; such. as storage of plant carbohydrates and generally 90 percent are in the top 30 cm. essential nutrients. The following dis- In peat soils, however, the same proportion cussion briefly reviews recent findings on is in the top 10 cm (Heikurainen, 1957). the behavior of belowground ecosystems and It has long been known that a seasonal suggests some questions yet to be resolved. periodicity of root growth is common in In particular, seasonal production/turnover woody plants (see reviews by Lyr and Hoff- of root biomass, role of root processes in man, 1967; Kozlowski, 1971; Hermann, 1977; nutrient turnover, root exudation, and the and Santantonio et al., 1977). For example, significance of belowground dynamics to the radial growth of woody roots (with second- energy balance of the forest ecosystems are ary xylem thickening) can closely follow considered. the pattern of radial increment growth Before proceeding further, let us note aboveground (Fayle, 1968). Studies con- why understanding the belowground ecosystem cerned with seasonal periodicity of root is important. Our concept of forest root elongation, initiation of laterals, and dynamics incorporates several reasonable but subsequent growth have not clarified generally untested assumptions. For ex- whether periods of inactivity reflect phys- ample, root production has been assumed to iological or environmentally mediated dor- be related to shoot production in the same mancy. Sutton (1969) concluded that pri- manner as biomass, i.e., mary growth of roots is probably dominated by environmental conditions. Control pro- root production shoot production bably lies in the interaction of endogenous = (k) root biomass shoot biomass and environmental mechanisms, but this re- mains to be demonstrated satisfactorily. Lacking information, the constant (k) has While there is considerable informa- been assumed to equal 1.0. Assumptions tion on the phenology of root growth, there such as these have arisen primarily because is an insufficient basis for making esti- of technical problems and excessive labor mates of root production and turnover. The required for research on forest tree roots earliest studies of root production are (Newbould, 1967; Lieth, 1968). Recent probably those of Heikurainen (1957) and progress in this area of study is related Kalela (1957). Both studies involved Scots to two factors. First, much work emanates pine (Pinus sylvestris L.) in Finland and from large integrated studies of forest eco- both reported a modal pattern of rapid systems such as those initiated as part of growth to peak root biomass in the spring the International Biological Program. These and a gradual decline during the summer to studies supported skilled and dedicated a low of about 50 percent of the peak level. technicians necessary to obtain the requi- A biomodal peak in root biomass has been site data. Second, as more became known reported far an oak woodland in central about the metabolism of forest ecosystems, Minnesota, USA (Ovington et al., 1963) and the potential role of roots in ecosystem a stand of European beech (g sylvatica function and their energy demands associ- L.) in the Soiling area of West Germany ated with the accumulation and turnover of (Gdttche, 1972). In both instances, bio- carbon and other essential elements sur- mass peaked in spring with a second but faced as a central link coupling physiolog- lower peak in the fall. Investigations by ical processes and their environmental con- Harris and others (1978) in a 45-year-old straints with ecosystem behavior. Some in- yellow poplar (Liriodendron tulipifera L.) teresting findings are counter to what has stand in east Tennessee also revealed a been commonly assumed. A few examples spring-fall biomodal peak, while for loblolly follow. pine (Pinus taeda L.) in North Carolina the modality was less clear with peaks observed in late fall, late winter, and possibly late SEASONAL ACCIJMIJLATION/ TURNOVER spring. The year-to-year consistency ob- OF ROOT ORGANIC MATTER served for yellow poplar (Harris et al., 1978) suggests a strong measure of endo- Root biomass of forests is not static. genous control. As with root elongation, It changes annually and represents a vary- the correlations of periods of peak biomass ing proportion of the total biomass during with environmental patterns are inconclu- stand development. By far the most dynamic sive. Current studies of mature Douglas-fir component of root biomass is the fraction in western Oregon, however, reveal changing defined as "fine roots." No standard de- seasonal patterns of standing crop of roots finition exists for fine roots. The dis- <5 mm diam. from one year (moderately dry) tinction between fine and large roots is to the next (wet) (Santantonio, 1979). H.F. HARRIS, D. SANTANTONJO, & D. McGINTY 121

The surprising result of recent studies t/ha, with a net annual turnover (translo- on seasonal dynamics of fine roots is the cation and sloughing) of equal magnitude. large flux of organic matter which is in- This value of net annual small root pro- volved large in an absolute sense as well duction is 2.8 times larger than mean as relative to other organic matter fluxes annual aboveground wood production deter- of forest ecosystem (Harris et al., 1975). mined for the study area from alloinetric Using a coring device, Harris and others equations and periodic (1965 to 1970) dbh (1978) sampled a yellow poplar forest stand inventory (Sollins et al., 1973). intensively over a two-year period. The Other experimental data on ecosystem lateral root biomass of yellow poplar show- carbon metabolism for the same Liriodendron ed considerable variation in the smaller forest study area corroborate the existence root size classes (Fig. 1). Small roots of a large, annual belowground allocation within this forest were characterized by a of carbon. Estimated net photosynthetic in- peak in late winter (1 March), a minimum in flux and soil-litter carbon efflux yield an mid-May, a second peak in mid-September, amount of unaccounted carbon input to soil and a minimum in early winter (December to equivalent to 7.5 tons organic matter per January). This pattern appears to be con- hectare (Harris et al., 1975; Edwards and sistent among successive years.Based on Harris, 1977). For temperate deciduous summation of positive seasonal differences forests, the common assumption that below- between minimum and subsequent peak bio- ground primary production is a fraction of mass, net root biomass production was 9.0 aboveground primary production proportional

ORNL-DWG 73-7168R3 1000 LIRIODENDRON FOREST ROOT BIOMASS DYNAMICS - <0.5cm DIAM 900 I

800 700 71\ \\ 600 / I______I \____ I IJ I // -__ ::E 400 \\ ,1 300 \ 200

too (0) 0 1973 L 0 .1972 1400

I a1971 I >05cm DIAM I.- POOLED DATA 1200

-..---.-

800

600

400

200 (b) 0 JAN FEB MAR APR MAY JUNE JULY AUG SEPT OCT NOV DEC

Figure 1. Seasonal distribution of lateral root biomass in a Liriodendron forest for

(a) roots <5 mm diam. and (b) roots > 5 mm diam. (5 ± 1 SE). Net biomass production and turnover were calculated from differences in pool size through the year. Based on monthly 'umraary of core data, no consistent pattern of biornass dynamics could be detected for roots >5 mm diam. 122FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

to biomass pooi size would lead to an under- with a late-spring peak (8.3 t/ha in June) estimate of total annual root production. and a November minimum (2.1 t/ha). Keyes The results from yellow poplar are not did not separate live and dead roots, but an extreme example. While the number of he observed rapid appçarance and disappear- studiesis limited, a sufficient range of ance of root tips, suggesting rapid turn- forest ecosystem types is represented to over even on the good site where no season- indicate that the large flux of organic al pattern was observed. matter belowground is a general property of McGinty (1976) found no seasonal pat- forest ecosystems. In mature (70-170 yrs), tern of fine root biomass in a mixed hard- natural stands of Douglas-fir in western wood watershed at Coweeta (western North Oregon, Santantonio (1979) has found that Carolina). McGinty suggested that the seasonal patterns and ratios of live-to- absence of a seasonal pattern might reflect dead roots (<5 mm diam.) distinctly differ niche differentiation belowground, but he between wet and dry sites (Figs. 2 and 3). did not separate living and dead root com- Accounting for quantitative changes in live ponents. McGinty indicated there may be a and dead fine roots from one month to the "root capacity" for a mature forest-soil next, root growth, mortality, and decom- combination as the forest matures, net position from March 1977 to March 1978 were root production equilibrates with root estimated. Root growth was 8.5, 10.2, and mortality. While McGinty's study did not 10.1 t/ha for wet, moderate, and dry sites, provide a conclusive estimate of primary respectively; root mortality was 10.9, 12.2, production of roots, growth into filled and 13.1 t/ha, respectively; and root de- trenches represented a fine root production of composition was 12.3, 12.5, and 18.4 t/ha, 6.0 t/ha/yr. Given the standing pool of respectively. roots, <25 mm of 27 t/ha, this suggests a In another study of 40-year-old turnover time of 4 to 5 years. His mea- Douglas-fir stands, Keyes (1979) found a sured decay rates for roots would support a contrasting pattern in biomass of roots turnover time at least as rapid as proposed. <2 inn diameter between "good" and "poor" sites. On the good site, no seasonal pat- tern was apparent (mean of 2.5 t/ha), while on the poor site there was a modal pattern ORNL-CWG 79- 24235 16

I' ORNL-DWG 79-21234 14 I I I I 1 141 ADRY I' I 12 '5' 12 I \ 0 / I.- I AWET \ / '5. 'S MODE RATE _\\ '-S 0 I A '5'.! '- 10 10 '-5J 0 I i\ r Ui '\ ___\ Ui I' w \ '\' I- 4 \ / '5/ 4 E V MODERATE 0 6 \___\ t.. / -S \ .5.' / -S / 5.-, 0 0 U, DRY 04 440 0Ui Ui PEAK MOISTURE STRESS T > J

2 PEAK MOISTURE STRESS GROWING SEASON cPOUL4i(, C.AOPd

M A M J J A S 0 N DJ F M M A M J J A S 0-N 0 J F M 1977 1978 1977 1978 MONTH MONTH

Figure 2. Seasonal fluctuations of live fine Figure 3. Scasonal fluctuations of dead fine roots of Douglas-fir on three sites. Stand- roots of Douglas-fir on three sites. Stand- ard errors o[ estimate are approxLaately ard errors of estimate are approximately equal to 1.0 t/ha. equal to ± 1.0 t/ha. W. F. HARRIS, D. SANTANTONIO, & D. McGINTY 123

McGinty's large size cut-off (25 mm) vastly Analysis of total and proportional efflux underestimates the dynamics of fine roots of CO2 from the soil surface (Edward and (<5 mm) or absorbing roots (<1 mm). Thus Harris, 1977) and experimental measurements his estimates of production and turnover of root decay rate (H.F. Harris, unpub. should be considered conservative. data) corroborate the prompt metabolism of McClaugherty (1980) studied fine root root detritus. Similar findings (Kanazawa production and turnover in a red pine plan- et al., 1976; McGinty, 1976; Persson, 1978, tation (54 yrs old) and a natural mixed 1979; Santantonio, 1979; and Keyes, 1979) hardwood stand in southern New England. all point to prompt disappearance of fine Root production in the pine plantation was root organic matter. We are thus left with 4.1 t/ha; mortality was 4.3 t/ha. Based on the following generalization: the soil of CO2 evolution attributable to root organic temperate coniferous and deciduous forest matter decay (an equivalent of 0.7 t/ha) and ecosystems annually receives an input of estimates of herbivore consumption (0.8 root organic matter equal to or much greater t/ha), 2.8 t/ha were transferred to soil than the input from any other source; this organic matter. A similar pattern of fine organic matter is promptly metabolized by root dynamics was observed in the natural heterotrophs. hardwood stand. Production was 5.3 t/ha; Information on root biomass dynamics mortality was 4.2 t/ha; CO2 loss was only of tropical forests is extremely limited. 0.9 t/ha; herbivore consumption was 0.3 However, one recent study suggests that for t/ha; transfer to soil organic matter was certain tropical forest types, production 3.0 t/ha. While these results are in con- of root organic matter also may be large trast with other studies cited here which with turnover equally rapid, similar to the suggest prompt (ml yr) turnover of root general pattern emerging from analysis of organic matter, these findings are consist- temperate forests. Jordan and Escalente ent with the general accumulation of organic (1979) observed significant root growth matter in northern temperate forest soils. activity at the soil surface in "tierra Another recently completed study in forme" (never flooded) forests growing on Abies amabilis forests in the Pacific North- oxisols in the Amazon Territory of Vene- west region (Grier et al., ms.fri prep.) zuela. The surface growth appeared to be further strengthens the case for large in response to litterfaltl. Roots (<6 mm) throughput of organic matter belowground. grew around fallen litter but were subse- Net primary production above- and below- quently sloughed as the "captured" litter ground was studied in 23-year-old and 180- decayed. This growth amounted to 117 year-old stands. Total organic matter g/m2/yr, a flux equivalent to 12 percent of (aboveground plus belowground) in the two aboveground detritus inputs. Such a re- stands was 77 and 585 t/ha, respectively. sponse may represent a highly developed Belowground net production was 9.9 and 11.7 adaptation to the lower available nutrients t/ha, respectively, with root detritus pro- in highly weathered tropical soils. duction amounting to 8.1 and 11.0 t/ha, Before leaving the subject of root respectively. Aboveground production was organic matter dynamics, we should mention 6.5 t/ha in the 23-year-old stands and 4.6 the dynamics of larger structural roots t/ha in the 180-year-old stands. (5 m diameter). Generally, this organic Recent studies in coniferous forests matter component is much more stable, cer- have shown that a significant fraction of tainly not exhibiting significant seasonal the small root turnover is comprised of or even annual dynamics. However, it would mycorrhizal roots (Fogel and Hunt, 1979; be incorrect to consider this a static Grier et al., ms. in review). The relative pun1. Again, evidence is sparse, but contributions of mycorrhizal and non- Kolesnikov (1968) observed that a cyclic mycorrhizal roots to root turnover in renewal of large structural roots occurs deciduous forests is presently unknown. during the development of a forest stand. The large accumulation of root organic One cannot pass up the speculation that a matter is a seasonal phenomenon. The net physiological balance might exist within annual accumulation of structural root individual forest trees, causing this main organic matter (not to be confused with fine structural component to shift so that the root production) is much smaller and can fine root structure continually invades best be described as a ratio of total "new" areas of its soil habitat. Whether aboveground and belowground biomass times this speculation will withstand closer ob- the net annual aboveground production. servation, and what the controlling factors What, then, is the fate of seasonal fluxes and mechanisms might be, remain to be of organic matter belowground? Most of this answered. material is promptly metabolized by soil heterotrophs (Edwards and Harris, 1977). 124 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

ROOT ORGANIC ACCUMULATION 1977; Cromack at al., 1979). Results thus DURING STAND DEVELOPMENT far implicate a complex control system in which forest trees exert a strong influence During forest stand development, the over their chemical environment suggestive amount of root organic matter increases on of a high degree of co-adaptation. an absolute basis, but the proportion of the Radiotracer studies with '3Cs have total biomass as root organic matter de- shown that over 50 percent of 13Cs in creases. Patterns of root/shoot ratio be- roots of tagged yellow poplar seedlings was tween deciduous and coniferous forests vary transferred to culture solutions in less (Rodin and Bazelivich, 1967). Generally, than 7 days (Cox, 1972). Sandberg and coniferous forests reach an equilibrium others (1969) estimated that during one root/shoot ratio earlier in stand d'evelop- growing season 75 percent of 137Cs transfers ment (i.e., at a lower total biomass) than by yellow poplar seedlings grown in sand is the case for deciduous forests. was due to exudation-leaching. In their analysis of a cesium-tagged yellow poplar forest, Wailer and Olson (1967) considered ThE SIGNIFICANCE OF ROOT DYNAMICS root exudation leaching processes as impor- TO ELEMENT INPUTS TO SOIL tant pathways of cesium transfer to soil AND ELEMENT CYCLING based on concentration of '37Cs in soil at various depths. If in situ processes of Cs Much more limited than our knowledge of are comparable to those of the chemical root organic matter dynamics is our know- analog, potassium, large quantities of K ledge of the role of root production/turn- could be transferred to soil annually by over (sloughing) to element cycling. Of leaching-exudation processes. course, some assumptions about root element Very few data are available to compare content can be used to- estimate the flux of return of elements to the soil via above- elements to the soil. McGinty's (1976) ground and belowground processes. Table 1 work begins to place the contribution of summarizes a comparison for an extensively roots in perspective. In oak-hickory and studied yellow poplar forest at Oak Ridge, eastern white pine forests of Coweeta, Tennessee (Cox et al., 1978). In this North Carolina, roots comprised 28 percent analysis, consumption was assumed to be 10 of the forest biomass but contained 40 per- percent of root detritus. Root detritus cent of plant nutrients in hardwoods and 65 turnover was estimated by the large residual percent of plant nutrients in pines. Thus, CO2 efflux from soil unaccounted for after this dynamic root component is a nutrient- litter decomposition and autotrophic root rich substrate. Roots can return nutrients respiration were subtracted from total soil to the soil in several ways: death and CO2 efflux. decay, exudation and leaching, and, in- In this example (Table 1), annual re- directly, when consumed by grazers. turn of elements to soil by root processes Studies of leaching and exudation from was three times the combined aboveground roots are likewise limited. In a northern inputs (including atmospheric) for K and at hardwood forest ecosystem, Smith (1970) has least 1.5 times aboveground inputs for N. found root exudation (during growing sea- Of the total (aboveground and belowground) son) to account for 4 kg/ha of carbon, 8 Kg return to soil, root processes accounted K/ha, and 34.2 kg Na/ha for three princi- for turnover of 70 percent of organic mat- pal tree species (Betula alleghaniensis, ter, 62 percent of N, and 86 percent of K. Fagus grandifolia, and Acer saccharum). Some additional fraction (here assumed to Although the techniques employed (modified be about 10 percent of the total estimated axenic culture) risk introducing artifacts, detrital flux) was transferred to soil con- a considerable potential forcontribution sumer pools. of elements to the soil via exudation Estimates of total herbivory on roots exists. do not exist. Root-feeding nematodes and Direct exudation of mineral nutrients various larval stages (e.g., cicada) might to the soil may be of minor significance, be principal consumers (Ausmus et al., however, in comparison to the role of low 1978). Assuming consumption as 10 percent molecular weight organic acids contained in of the estimated turnover may be high for root oxidation. This small loss of reduced temperate forests. Schauermann (1977) re- carbon may have a major effect on pH regula- ported that rhizophagous Curculionidae con- tion in the rhizosphere and nitrogen meta- sumed 81 x iO kcal/ha/yr and comprised 12 bolism of the plant (Sollins et al., 1979), percent of the biomass of soil invertebrates. and the oxalate as a product of fungal Assuming comparable consumption rates per metabolism as well as higher plants could unit weight among all soil invertebrates, have a significant effect on weathering of total consumption might approach 800 x lO soil minerals, especially the availability kcal/ha/yr. In Schauermann's beech forest of phosphorus to plants (Graustein et al., H.F. HARRIS, D. SANTANTONJO, & 0. McGINTY 125 study, Curculionidae consumption was 0.1 SIGNIFICANCE OF ROOT SLOUCHING percent of net primary production (presumed TO FOREST ENERGY BALANCE to be aboveground only). Edwards (in Auerbach, 1974, p. 86) estimated the total Odum (1969) suggested a strategy of in- energy consumed by invertebrates to he 2 creasing conservation of nutrients in ele- percent of total amount fixed annually. ment cycling during forest ecosystem devel- Thus, evidence to date points to a small opment. The mechanism leading to a closed absolute flux of energy by consumption of cycle for nitrogen could be root sloughing root (or aboveground) biomass. Despite the and subsequent microbial mineralization. small absolute role of consumers, we cannot In temperate, deciduous forests at Oak Ridge, dismiss their importance to the functioning Tennessee, biomass and nitrogen accumulate of forest ecosystems. Schauermann regarded in roots during periods favorable for the Curculionidae as accelerators of the growth (summer) or just preceding growth mineralization processes because of physical (late winter); and winter growth occurs damage to roots and effects of their largely at the expense of stored photosyn- on microbial decomposition. He found that thate. During periods unfavorable for 87 percent of energy turnover in the growth (fall-winter) or when aboveground rhizophagous larval population occurred be- energy demands are high (spring-early sum- tween August and April a period generally mer canopy development), root biomass is coincident with high root turnover. sloughed, thus reducing the total energy Waldbauer (1968) reported a similar pattern demand on the temperate forest system at a for many insect populations. time when reserves are seasonally depleted and/or plant requirements for carbon are high elsewhere (e.g., canopy development).

Table 1. Annual aboveground and belowground orqanic matter and element returns to soil in a yellow poplar (Liriodendrori tulipifera L.) stand1

Biomass Nitrogen Potassium

kg/ha kg/ha kg/ha

Aboveground2

Dryfall/wetfall . .. 7.2 3.6 Canopy leaching ... 2.3 29.4 Litterfall 3,310 42.2 10.0

Total aboveground return 3,310 51.7 43.0

Be lowg round3

Root transfer processes4 Death and decay 6,750 76 128 Consumption 750 9 14 Exudation-leaching ...... 128

Total belowground return 7,500 85.0 270

Total return to soil 10,810 136.7 313

'From Coxet al., 1978. 2 Aboveground data from Edwards and Shanks (unpub. data); chemical determinations were made on fallen material. 3Root biomass estimates froma Liriodendron stand (>80% Liriodendron). 4Exudation-leachingdata are extrapolated from seedling studies of Cox (1975), assuming equivalent behavior of Cs and K. Element losses via root sloughing are based on amount of sloughed biomass times mean root N content; element flux via consumption assumed to be 10 percent of total belowground return. 126 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Nitrogen contained in sloughed organic because of the interactions of autot rophs matter is conserved as part of the soil and decomposers. detritus by those microbial processes which The energy expenditure to forest eco- immobilize it. systems represented by root sloughing is The cyclic pattern of photosynthate high. in the yellow poplar forest at Oak accumulation in a deciduous forest and the Ridge (Harris Ct al., 1975; Edwards and sustained productivity, which is in part HarrIs, 1976), Edwards (in Auerbach,197/4) dependent on available N, are closely estimated that lateral root growth, slough- coupled through activities of soil microbes ing, and maintenance respiration accounts on a large systematically replenished sub- for 44.8 percent of the total energy fixed strate rich in nitrogen. In this respect, annually in photosynthesis (1.88 x iO continuous maintenance of living roots in kcal/m2). Root slougbing, with subsequent temperate forests would impose energy limi- microbial immobilization, offers a parti- tations on by reducing periodic cularly attractive mechanism to explain re- influx of nitrogen-rich root organic matter. tention of essential elements in the uptake because this flux represents 70 percent of zone. In another context, maintenance and total detrital input. While data from other development of a fertile soil requires deciduous systems are scarce, we hypothesize significant input of energy (contained in that evolution of temperate forest species organic matter). For the yellow poplar has favored mechanisms which contribute to forest, energy requirements for maintenance systematic return of elements and organic of soil are on the order of 66 percent of matter through belowground sloughing. the energy fixed annually by photosynthesis Sloughing, therefore, stabilizes biogeo- (roots + 21% allocation to leaves). Many chemical cycles of potentially limiting ele- of man's activities which reduce both ments in an environment typified by season- energy fixed photosynthetically and/or ally limited photosymthate availability. energy input to soil are most severely Inani- As illustrated in Table 2, carbon (energy) fested by degradation of the soil with is rapidly metabolized within the ecosystem respect to humified soil organic matter and and lost (as CU2). Essential elements, on fertility. The energy inputs to soil the other hand, are retained effectively (dominated in temperate forests by root

Table 2. Comparison of turnover times for carbon, nitrogen and calcium in temperate deciduous forests (Tennessee)1

Turnover time(yrs)2

Component Carbon Nitrogen Calcium

Soil 107 109 32 Forest biomass 155 88 8 Litter (01 + 02) 1.12 5 <5 Total5 54 1,815 445 Decomposers 0.01 0.02

1From O'Neill et al., 1975. 2Carbon data basedon carbon metabolism of yellow poplar forest (Harris et al 1975; Reichie et al., 1973); nitrogen data based on nitrogen budget for mixed deciduous forest (Henderson and Harris, 1975); calcium data based on calcium budget from a Liriodendron itfera forest (Shugart et al., 1976). 3Turnover time basedon available Ca and assumes all losses of Ca from soil are from the pool of available Ca. 4Considers aboveground biomass pool. Cyclic renewal of structural roots (Kolesnikov, 1968) would lower turnover time. Tree mortality estimated from permanent plot resurvey (3-year interval) and likely underestimates the mortality rate over the duration of a forest generation. 5Total calculatedas sun of elements in living and dead components of the ecosystem; element loss based on sum of all losses from ecosystem. W. . HARPIS, D. SANTANTONTO, & 0. McGINTY127

sloughing) 'ontribute to maintenance of Cox, T. L., W. F. Harris, B.S. Ausmus, and soil fertility. N. T. Edwards. 1978. The role of A number of areas require additional roots in biogeochemical cycles in an study. First, the pattern of belowground eastern deciduous forest. Pedobiologia detritus contributions needs to be deter- 18: 264-271. mined for additional forest types, espe- cially forests of extreme climates. The Cromack, K., Jr., P. Sollins, W. Graustein, large photosynthate requirements for main- K. Speidel, A. Todd, G. Spycher, C. Li, tenance respiration of forests combined and R. Todd. 1979. Calcium oxalate with a large annual sloughing of root accumulation and soil weathering in organic matter may limit forest growth in mats of the hypogeous fungus (Hyster- climates severely limiting photosynthate ang4p crassun). Soil Biol. and Bio- production. In this same vein, the influence chem. (in press). of stresses (whether natural or of anthropo- genic origin such as air pollutants) on Devlin, R. M. 1966. Plant Physiology. photosynthate translocation needs to be New York: Reinhold Publishing Corp. examined in mature forests in order to eval- uate forest response to perturbations. The Edwards, N. T., and W. F. Harris. 1977. decay of root organic matter occurs rapidly. Carbon cycling in a mixed deciduous Are there biochemical changes in sloughed forest floor. Ecology 58:431-437. roots that promote decomposability or alter the behavior of fungal symbionts generally Fayle, D.C. F. 1968. Radial growth in associated with the rhizosphere?Answering tree roots. Univ. of Toronto, Fac. these and other questions about the dynamic For. Tech. Rep. No. 9 belowground component of forest ecosystems will provide an exciting challenge to for- Gbttsche, D. 1972. Verteilung von Fein- est ecology for the next several years. wurzeln und Mykorrhizen in Bodenpro- fileines Buchen- und Fichtenbestandes in Solling. Hamburg: Kommissions- LITERATURE CITED verlag Buchhandlung Max Wiedebusch.

Auerbach, S. I. 1974. Environmental Sci- Graustein, W. C., K. Cromack, Jr., and P. ences Division Annual Report for the Sollins. 1977. Calcium oxalate: period ending September 30, 1973. Oak Occurrence in soils and effect on Ridge National Lab. Rep. ORNL-4935, nutrient and geochemical cycles. Oak Ridge, Tenn. Science 198:1252-1254.

Ausmus, B. S., J. M. Ferris, D. E. Reichie, Grier, C. C., K. Vogt, M. Keyes, and R. and E. C. Williams. 1978. The role Edmonds. Above- and belowground pro- of belowgrourid herbivores in mesic duction in subalpine (Abies amabilis) forest root dynamics. Pedobiologia stands: Changes with ecosystem devel- 18: 289-295. opment. (Mans. in preparation).

Bazilevich, N. I., and L. E. Rodin. 1968. Harris, W. F., R. A. Goldstein, and G. S. Reserves of organic matter in the Henderson. 1973. Analysis of forest underground sphere of terrestrial phy- biomass pools, annual primary produc- tocoenoses, In International Symposium, tion and turnover of biomass for a USSR, Methods of Productivity Studies mixed deciduous forest watershed. In in Root Systems and Rhizosphere Organ- Proc. IUFRO Conference on Forest Bio- isms, pp. 4-8. (Reprinted for the mass Studies, edited by H. Young, International Biological Program by pp. 41-64. Orono: University of Maine Biddles, Ltd., Guildford, U.K.). Press.

Cox, T. L. 1972. Production, mortality and Harris, W. F., P. Sollins, N.T. Edwards, nutrient cycling in root systems of B. E. Dinger, and H. H. Shugart. Liriodendron seedlings. Ph.D. thesis, 1975. Analysis of carbon flow and University of Tennessee, Knoxville. productivity. In Productivity of World Ecosystems, Proc. .IP Stn Gen- Cox, T. L. 1975. Accumulation and mobility eral Assembly, edited by D.E. Reichie of cesium in roots of tulip poplar and J. F. Franklin, pp. 116-122. seedlings. In Mineral Cyc1ing Washington, D. C. : National Academy Southeastern Ecosystems, edited by of Sciences. F. G. Howell, J. B. Gentry, and M. H. Smith, pp. 482-488. ERDA Symp. Series (CONF-7405l3). 128 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Harris, W. F., R. S. Kinerson, and N. T. Lieth, H. 1968. The determination of Edwards. 1978. Comparisons of below- plant dry-matter production with ground biomass of natural deciduous special emphasis on the underground forest and loblolly pine plantations. parts. In Functioning of Terrestrial Pedobiologia 17:369-381. Ecosystems at the Primary Production Level, edited by F. E. Eckhardt, pp. Heikurainen, L. 1957. Uber Veränderungen 179-186. Proc. of Copenhagen Symp., in der Wurzelverhltnissen der Kiefern- Vol. 5. Paris: UNESCO. bestnde auf Moorböden in Laufe des Lyr, H., and G. Hoffmann. 1967. Growth Jahres. Act. For. Fenn. 62:1-54. rates and growth periodicity of tree roots. In International Review of Henderson, G. S., and W. F. Harris. 1975. Forestry Research, Vol. 2, edited by An ecosystem approach to the character- Romberger and Mikola, pp. 181-236. ization of the nitrogen cycle in a New York: Academic Press, Inc. deciduous forest watershed, In Forest Soils and Forest Land Management, McClaugherty, C. A. 1980. The role of fine edited by B. Bernier and C. H. Winget, roots in the organic matter and nitro- pp. 179-193. Quebec, Canada: Laval gen budgets of forest ecosystem. University Press. Unpub. M.S. thesis, University of Virginia, Charlottesville. Hermann, R. K. 1977. Growth and production of tree roots: A review. In The McGinty, D. T. 1976. Comparative root and Belowground Ecosystem: A Synthesis of soil dynamics on a white pine water- Plant-Associated Processes, edited by shed and in the hardwood forest in the J. K. Marshall, pp. 7-28. Range Coweeta basin. Ph.D. dissertation, Science Dept. Series No. 26, Colorado University of Georgia, Athens. State University, Fort Collins. Newbould, D. J. 1967. Methods for Esti- Jordan, C. L., and Gladys Escalente. 1979. mating the Primary Production of For- Root productivity in an Amazonian rain ests, IBP Handbook No. 2. Oxford: forest. Ecology (mans. submitted). Blackwell Scientific Pub.

1950. Manniköiden ja Kunsi- Kalela, E. K. Odum, E. P. 1969. The strategy of eco- koiden jurrisuhteista. I. Acta For. system development. Science 164:262- Fern. 57:1-79 (English summary). 270.

Kanazawa, S., T. Asami, and Y. Takai. O'Neill, R. V., W. F. Harris, B. S. Ausmus, 1976. Characteristics of soil organic and D. E. Reichle. 1975. A theoreti- matter and soil respiration in sub- cal basis for ecosystem analysis with alpine, coniferous forests of Mt. particular reference to element cycl- Shigayama. 3. Soil respiration under ing. In Mineral Cycling in South- field conditions. J. Sciences of Soil eastern Ecosystems, edited by F. G. and Manure 47(12):549-554. Howell, J. B. Gentry, and M. H. Smith, pp. 28-40. ERDA Symp. Series (CONF- Keyes, M. R. 1979. Seasonal patterns of 740513). fine root biomass, production and turn- over in two contrasting 40-year-old Ovington, J. D. 1962. Quantitative ecology Douglas-fir stands. M.S. thesis, and the woodland ecosystem concept. University of Washington, Seattle. Adv. Ecol. Res. 1:103-192. Kolesnikov, V. A. 1968. Cyclic renewal of Ovington, J. D., D. Heitkamp, and D. B. roots in fruit plants. In International Lawrence. 1963. Plant biomass of Symposium, USSR, Methods of Productivity prairie, savanna, oakwood and maize Studies in Root Systems and Rhizosphere field eocsystems in central Minnesota. Organisms, pp. 102-106. (Reprinted for Ecology 44:52-63. the International Biological Program by Biddies, Ltd., Guildford, U.K.). Persson, H. 1978. Root dynamics in a young Scots pine stand in Central Kozlowski, T. T. 1971. Growth and Develop- Sweden. Oikos 30:508-519. ment of Trees, Vol. 2. New York: Academic Press, Inc. Persson, H. 1979. Spatial distribution of fine-root growth, mortality and de- Physiological Plant Larcher, W. 1975. composition in a young Scots pine Ecology, trans. by M. A. Brederman- stand in Central Sweden. Oikos (in Thorson. New York: Springer-Verlag. press). W.F. HARRIS, D. SANTAHTONIO, & D. McGINTY 129

Pitman, M. G. 1976. Nutrient uptake by Sollins, P., K. Cromack, Jr., R. Fogel, and roots and transport to the xylem. In C. Y. Li. 1979. Role of low mole- Transport and Traufer Processes in cular weight organic acids in the in- Plants, edited by I.F. Wardlaw and organic nutrition of fungi and higher J.B. Passioura, pp. 85-100. New plants. In The Fungal Community, York: Academic Press, Inc. edited by 0. T. Wicklow and G. Carroll. New York: Marcel Dekker, Inc.(in Reichle, D. E., B. E. Dinger, N. T. Edwards, press). H. F. Harris, and P. Sollins. 1973. Carbon flow and storage in a forest Sollins, P., D. E. Reichie, and J. S. Olson. ecosystem. In Carbon and the Biosphere, 1973. Organic matter budget and model Proc. 24th Brookhaven Symp. on Biology for a southern Appalachian Lirioden- (AEC-CONF-720510), edited by G. M. dron forest. USAEC Rep. EDFB-IBP-73-2, Woodwell and E. V. Pecan, pp. 345-365. Oak Ridge National Lab., Oak Ridge, Springfield, Va.: National Technical Tenn. Information Service. Sutton, R. F. 1969. Form and development Rodin, L. E., and N.I. Bazilevich. 1967. of conifer root systems. Commonwealth Production and Mineral Cycling in For. Bull., Tech. Commun.7, Oxford, Terrestrial Vegetation, trans. by C. E England. Fogg. London: Oliver and Boyd. Waldbauer, G. 1968. The consumption and Sandberg, G. R., J. S. Olson, and E. E. C. utilization of food by insects. Adv. Clebsch. 1969. Internal distribution Insect Physlol. 5:229-288. and loss from roots by leaching of cesium-137 inoculater into Liriodendron Waller, H. D., and J.S. Olson. 1967. tulipifera L. seedlings grown in sand Prompt transfers of cesiurn-l37 to the culture. Oak Ridge National Lab. Rep. soils of a tagged Liriodendron forest. ORNL/TM-2660, Oak Ridge, Tenn. Ecology 48:15-25.

Santantonio, D., R. K. Herinann, and W. S. Whittaker, R. H., and G. M. Woodwell. 1968. Overton. 1977. Root biomass studies Dimension and production relations of in forest ecosystems. Pedobiologia trees and shrubs in the Brookhaven 17:1-31. Forest, New York. J. Ecol. 56:1-25.

Santantonio, D. 1979. Seasonal dynamics of Whittaker, R. H. 1971. Measurement of net fine roots in mature stands of Douglas- primary production of forests. In fir of different water regimes a Productivity of Forest Ecosystems, preliminary report. In Root Physiology edited by P. Duvigneaud, pp. 159-175. and Symbiosis, Proc. of IUFRO, Sept. Paris: UNESCO. 11-15, 1978, Nancy, France (in press).

Schauermann, J. 1977. Energy metabolism of rhizophagous insects and their role in ecosystems. In Soil Organisms as Components of Ecosystems, Ecol. Bull. NFR 25, edited by U. Lohm and T. Persson, pp. 310-319. Stockholm: Swedish Natural Research Council.

Shugart, H. H., D. E. Reichle, N. T. Edwards, and J. R. Kercher. 1976. A model of calcium cycling in an East Tennessee Liriodendron forest: model structure, parameters, and frequency response analysis. Ecology 57:99-109.

Smith, W. H. 1970. Technique for collec- tion of root exudated from mature trees. Plant and Soil 32:238-241. Vital Signs of Forest Ecosystems

B. H. Waring

INTRODUCTION much from autopsies but, so far, saved few patients. Some scientists who have observ- Forest ecosystems, like the human body, ed healthy ecosystems have charted probable are composed of many parts carrying on forest responses under a variety of environ- functions essential to the well-being of ments. Comparing predicted carbon dioxide the whole. Given sufficient fresh air, uptake for healthy Douglas-fir needles liquids, and balanced nutrition, most for- growing in a maritime climate with that ex- est ecosystems lead long, productive lives. pected in a more continental environment There are tines, however, when inflic- (Fig. 1), we find that a maritime forest tions of old age, environmental stress, or breathes more deeply. These predictions of unwelcomed visitors produce unhealthy eco- leaf activity correlate well with those of systems. In many cases, part of the system forest growth (Fig. 2). Thus, an observed dies and is replaced a sad but normal departure from predicted growth patterns is expectation. We should be concerned, how- casue for concern. ever, when critical functions become im- Similarly, the rate at which organic paired. In recognizing that forests and wastes decompose on the forest floor is other ecological systens provide irreplace- expected to differ with climate and the able services, when these systems are quality of material (Fogel and Cromack, threatened, we must administer aid. 1977; Bunnell et al., l977a,b).We can measure and compare the weight loss, after a year, of litter packaged in porous bags DIAGNOSTIC AIDS with that predicted.Where decomposition is unexpectedly suppressed, further analyses Diagnosing sick systems is a new sci- may show toxic pollutants are accumulating ence in which practitioners have learned (O'Neill et al., 1977).

Table 1. Redistribution of nitrogen (N,g m2) in leaves indicates the level of available nutrients on infertile and fertile sites-1

Infertile Fertile Species Fresh Fallen Fresh Fallen AT

Alder --- 8.26 7.88 5

Hornbeam 1.57 0.56 -64 1.76 1.11 -37

Oak 2.65 0.99 -63 1.14 0.63 -45

Pine 2. 32 0. 54 -77 ---

After Stachurski and Zimka, 1975.

1 31 132 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

MONTH 50 I I I I JAN FEB MAP APR MAY JUN JULAUG SEP OCT NOV 100 >- COASTAL 40 c'J E a 30 OAK TYPE - C') 50 U) 0Cu Lu 0 I U) CELL DIVIS PINE TYPE FULL U) LEAF w 100 z CASCADE MOUNTAIN >- U) 20 40 60 80 100 120 0 DAYS SINCE BUD SWELL 0I.- I °- Figure 3. Seasonal patterns of plant mois- 50 ture stress in Douglas-fir saplings growing Lu on progressively drier habitats (after I- Waring et al., 1972). -J

\ '_\ I

0 V

0 100 200 300 L1i1 YEAR DAY

Figure 1. The yearly predicted pattern of 40 photosynthesis for Douglas-fir growing in the Oregon Coast Range and the more contin- 30 ental Cascade Mountains (after Emmingham and Waring, 1977). 20 UJ 00

C', 0 10 U, UJ 400 I

12,00 0 100 200 300 SAPWOOD BASAL AREA

10,00 -J Figure 4. Projected leaf area of lodgepole 2 pine linearly related to sapwood cross- 8,00 sectional area at 1.3 m height (Waring, unpub.).

WOOD PRODUCTION, rn3 ha (100 yr(

Figure 2. A comparison of annual predicted photosynthesis and Douglas-fir wood pro- To tell whether plants are receiving a duction for a 100-year period for four sites balanced mineral diet, compare the nutrient in western Oregon (after Emmingham and content of fresh with fallen foliage (Table Waring, 1977). 1). Well-nourished leaves generally store and pass on more nutrients as they die. As a mineral becomes more scarce, plants ex- pend more energy translocating it before leaves are shed. Because the total weight of leaves varies seasonally, mobilization of nutrients is best perceived in analyses as weight per unit of leaf area. . H. A4RJNG 33

To see whether plants are receiving leaves was estimated by sun-doing::le suwis d sufficient liquid, measure the tension in basal area in all the trees In a sampled water columns by sampling twigs in a pres- area. sure chamber (Waring and Cleary, 1967; Ritchie and Hinckley, 1975). When water stress exceeds 40 to 50 atmospheres, notify the next of kin. Predictably different pat- 20 H terns of water stress are expected in differ- ent environments (Fig. 3), but when plants 15 depart from expected patterns, some infirm- ity or adverse condition has surely set In. 0 CO The general vigor of forest ecosystems ID 0 is reflected by how efficiently they accumu- S late carbohydrate reserves. Unfortunately, 5 keeping track of how much carbon dioxide is H assimilated by a forest and used to sustain We know life is a very complicated task. U that healthy forests generally grow larger 0 and develop denser canopies than forests in STAND LEAn SCEA more stressful situations (Waring et al., Figure 5. 1978). We also recognize that all forests Mean tree vigor of Douglas-fir, must allocate resources so that a balance is indicated by the ratio of basal area incre- maintained between the energy-capturing ment (BA1) to total cross-sectional area foliage and the mineral- and water-extract- (SA) of sapwood, decreases linearly as the ing roots (Gordon and Larson, 1968; canopy density increases (after Newman, Thornley, 1972; Rangekar and Forward, 1973; 1979). Values represent means of 30 trees Harris et al., 1978). Carbohydrate reserves with standard error bars. are available for making wood only after all essential needs are met. Because large trees generally grow more _o_iii_iiii-_ -- - -

- wood each year than small ones, we need a i_li_ill-lw means of comparing how efficiently wood is 150 111111 -- l5ilI_ being accumulated. Because leaves are the factories which produce carbohydrates, one 1l DIED measure of efficiency is the rate of wood iihllDhhhhllV accumulation per unit of leaf area (Waring UuJ et al., 1980). However, determining how S Lu__iJ±liiT5±iJuj5ii 0 many leaves a tree has is not simple. For- a (A tunately, a balance exists--not only be- S 0 tween leaves and roots, but also between the S -i cross-sectional area of vascular tissue con- 04 ducting water and nutrients through the stem C 0 CA and the amount of foliage (Fig. 4) (Dixon, (50 1971; Grier and Waring, 1974; Waring et al., F- 0 1977; Whitehead, 1978). Such a balance in CF- Cd symmetry often indicates additional rela- -J F- 0 tionships between functions still undis- Cd 0 -- covered. S Growth in volume or biomass is 0 o directly related to annual growth in basal area; leaf area is directly related to sap- 0 wood basal area which, if not immediately obvious, can be identified by stains (Kutscha and Sachs, 1962). Thus, extracting 0 a small core of wood from the stem may pro- Lion vide an estimate of the increment in both 0 biomass and leaf area. 0 5 IC In a particular forest, if the amount B1/S,% of light reaching the leaves can be con- trolled by modifying the density of the Figure 6. Trees growing more than 8 percent canopy, tree vigor (the efficiency with of their sapwood basal area (BA1) in one which wood is accumulated per unit of leaf year are unlikely to be killed, whereas less area) decreases linearly as the adjacent vigorous trees are killed by mountain pine canopy becomes more dense (Fig. 5). In this example, the number of layers of beetles attacking above critical levels (Waring and Pitrnan, 1980) 134 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

At times, the vigor of indIvidual Wrapped in soft clouds, the pampered trees trees within a stand dramatically differs. in the protected valleys of the Oregon For example, in an old lodgepole pine for- Coast Range are surrounded by companions est being attacked by mountain pine beetles, from birth. Not surprisingly, such intimacy only those trees with low vigor are attack- fosters many communicable diseases. Though ed, and only those attacked by a sufficient conifers, once established, reach for the number of beetles are actually killed (Fig. sky, a host of former playmates--salmon- 6). berry, sword fern, and the like--continue Yet the death of less efficient in- to survive in their shadow, often attending dividuals in a forest bequeaths additional the funerals of the giants. Recognizing resources to those surviving. Often, the these associates may aid us in selecting total productivity of the system increases seed for re-establishing a well-adapted (Mattson and Addy, 1975; Wickman, 1978). forest (Arno and Pfister, 1977). By monitoring both growth and mortality, Forest ecosystems, like the human body, we can assess the effect of thinning, are complex. We are only now discovering whether brought about by nature or by man. how to take their pulses and listen to In Figure 7, thinning a iorest to different their heartbeats. With the concern of a densities accelerated growth, although the general practitioner for his patients, we number of trees was reduced to a quarter of are beginning to make "field calls" to that in the original stand. check the development of young and the How large a forest may grow is ulti- malaise of old forests. We have a small mately determined by the amount of foliage bag of instruments but a growing confidence it can support (Fig. 8). In harsh environ- that the care of forests is a rewarding and ments, the canopy remains open; in favorable essential endeavor. environments, cathedral groves of giant trees capture almost all the light. In diagnosing the health of forest ecosystems, we need to know whether a young stand is a potential dwarf or giant. Environmental analyses provide such estimates (Grier and Running, 1978; Waring et al., 1978). The company trees keep in a forest often is a good indicator of the kind of environment in which they grew up (Franklin and Dyrness, 1973; Arno and Pfister, 1977). Trees associated with juniper and sagebrush are individualists that have struggled to 700 survive in harsh surroundings; they grow slowly and tolerate little crowding. 600

500

(n 400 - 1__

0 ______:___11111111111

300 0 w 200 - E /IIII_- I _____

_ I 0 4 8 12 0 0 5 10 LEAF AREA STAND LE2F AREA Figure 8. Maximum accumulation of stem'wood Figure 7. Stand growth in basal area fol- biomass is ultimately limited by the forest lows a parabolic function as the canopy canopy that can be supported (Waring, un- density increases (after Newman, 1979). pub.). S. H. i7RING 135

LITERATURE CITED Kutscha, N. P., and I.B. Sachs. UJ62. Color tests for d ifferntiating eart- Arno, S. F., and R.D. Pfister. 1977. wood and sapwood in ertain softwood Habitat types: an improved system for tree species. USDA Forest Service classifying Montana's forests. Western Pubi. No. 2246, Madison, Wisconsin. Wildlands 4:6-11. Mattson, W. H., and N. D. Acldy. 1975. Bunnell, F. L., D. E. N. Tart, P. W. Phytophagous insects as regulators of Flanagan, and K. Van Cleve. 1977a. forest primary production. Science Microbial respiration and substrate 190:515-522. weight loss. I. Soil Biol. and Bio- chem. 9:33-40. Newman, K. 1979. Sapwood basal area as an estimator of individual tree growth. Bunnell, F. L., D. E. N. Tart, P. W. M.S. thesis, Oregon State University, Flanagan, and K. Van Cleve. 1977b. Corvallis. Microbial respiration and substrate weight loss. II. Soil Biol. and Bio- O'Neill, R. V., B. S. Ausnus, D. R. Jackson, chem. 9:41-47. R. I. Van Hook, P. Van Voris, C. Wash- burne, and A. P. Watson. 1977. Moni- Dixon, A. F. G. 1971. The role of aphids toring terrestrial ecosystems by in wood formation. I. The effect of analysis of nutrient export. Water, the sycamore aphid, Drepanosiphum Air, and Soil Pollution 8:271-277. platanoides (Schr.) (Aphidae), on the growth of sycamore, Acer pseudoplatanus Rangnekar, P. V., and 0.F. Forward. 1973. (L.). J. Applied Ecol. 8:165-179. Foliar nutrition and wood growth in red pine: effects of darkening and Emmingham, W. H., and R. H. Waring. 1977. defoliation on the distribution of An index of photosynthesis for compar- C-photosynthate in young trees. ing forest sites in western Oregon. Can. J. Bot. 51:103-108. Can. J. Forest Res. 7:165-175. Ritchie, G. A., and T. M. Hinckley. 1975. Fogel, R., and K. Cromack, Jr. 1977. The pressure chamber as an instrument Effect of habitat and substrate quality for ecological research. In Advances on Douglas-fir litter decomposition in in Ecological Research, Vol. 9, edited western Oregon. Can. J. Bot. 55:l632 by A. Macfayden, pp. 165-254. London: 1640. Academic Press, Inc.

1968. Gordon, J. C., and P. R. Larson. Stachurski, A. ,and J. R. Zimka. 1975. Seasonal course of photosynthesis, Methods of studying forest ecosystems: respiration, and distribution of 1C leaf area, leaf production, and with- in young Pinus resinosa trees as re- drawal of nutrients from leaves of lated to wood formation, Plant Physiol. trees. Ekologia Poiska 23:637-648. 43: 1617-1624. Thornley, J. H. M. 1972. A balanced Franklin, J. F., and C. T. Dyrness. 1973. quantitative model for root:shoot Natural vegetation of Oregon and ratios in vegetative plants. Ann. Washington. USDA Forest Service Ceo. Bot. 36:431-441. Tech. Rep. PNW-8, Pacific Northwest Forest and Range Expt. Sta., Portland, Waring, R. H., and B. D. Cleary. 1967. Oregon. Plant moisture stress: evaluation by pressure bomb. Science 155:1248-1254. Grier, C. C., and S. W. Running. 1978. Leaf area of mature northwestern coni- Waring, R. H., W. H. Emmingham, H. L. ferous forests: relation to a site Gholz, and C. C. Grier. 1978. Varia- water balance. Ecology 58:893-899. tion in maximum loaf area of coni- ferous forests in Oregon and its 1974. Grier, C. C., and R. H. Waring. ecological significance. Forest Sri. Conifer foliage mass related to sap- 24:131-140. wood area. Forest Sci. 30:205-206. Waring, R. H., H. L. Gholz, C.C. Crier, Harris, W. F., R. S. Kinerson, and N. T. and M. L. Plummer. 1977. Evaluatinq Edwards. 1978. Comparison of below- stem conducting tissue as an estimator ground biomass of natural deciduous of leaf area in four woody angio- forest and loblolly pine plantations. sperms. Can. J. Sot. 55:1474-1477. Pedobiologia 17:369-381. 136 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Waring, R. H., and G. B. Pitman. 1980. A simple model of host resistance to bark attack. Forest Research Labora- tory Res. Note 65, Oregon State Uni- versity, Corvallis.

Waring, R. H., K. L. Reed, and W. H. Emming- ham. 1972. An environmental grid for classifying coniferous forest eco- systems. In Research on Coniferous Forest Ecosystems, Proc. Symp. North- west Scientific Assoc., edited by J. L. Franklin, L. J. Dempster, and R. H. Waring, pp. 79-91. USDA Forest Service, Pacific Northwest Forest and Range Expt. Sta., Portland, Oregon.

Waring, R. H., W. G. Thies, and D. Muscato. 1980. Stem growth per unit of leaf area: a measure of tree vigor. Forest Sci. (in press).

Whitehead, D. 1978. The estimation of foliage area from sapwood basal area in Scots pine. Forestry 51:137-149.

Wickman, B. E. 1978. A case study of a Douglas-fir tussock moth outbreak and stand conditions 10 years later. USDA Forest Service PNW-244, Pacific North- west Forest and Range Expt. Sta., Portland, Oregon.

I Interpretation of Nutrient Cycling Research in a Management Context: Evaluating Potential Effects of Alternative Management Strategies on Site Productivity

Wayne T. Swank and Jack B. Waide

INTRODUCTION This objective is strongly guided by our underlying philosophy that resource manage- One of the fresh perspectives alluded ment is synonymous with ecosystem manage- to in the title of this volume is the in- ment. creased emphasis on understanding the bio- In this paper we evaluate the effects geochemistry of forest ecosystems (Bormann of various harvesting practices and alter- and Likens, 1967; Jorgensen et al., 1975; native levels of wood fiber utilization on Waide and Swank, 1976). Understanding the sustainable productivity of forests. nutrient cycling processes in forests is Such evaluations are now mandated by the needed not only to explain forest eocsystem Forest and Rangeland Renewable Resources dynamics in space and tine, but also for the Planning Act of 1974 and by the National wise husbandry of forest resources. The Forest Management Act of 1975. The latter circulation of essential elements in forest Act specifically requires demonstration ecosystems integrates biological populations that management systems used on land admin- with a variety of physicochemical processes istered by the Forest Service "will not (Hutchinson, 1948). Thus, nutrient cycling produce substantial and permanent impair- research is amenable to holistic interpreta- ment of the productivity of the land. tion and provides an essential means of Accelerated demands for wood products and evaluating the environmental consequences of derivations have led to such intensified resource management. forest management practices as site prepara- Our research program in forest biogeo- tion (Balmer and Little, 1978), short rota- chemistry at the Coweeta Hydrologic Labora- tion forestry (Ribe, 1974) and whole-tree tory, North Carolina, was initiated in 1968 utilization (Koch and McKenzie, 1975). The with a cooperative study between the Insti- economic benefits of these practices will be tute of Ecology, University of Georgia, and much reduced if soil fertility and producti- the U.S. Forest Service. This research vity decline because of altered nutrient program has descriptive, predictive, and cycles (Waide and Swank, 1976). Thus, there conceptual objectives (Monk et al., 1977). is urgent need for information and analyti- We are trying to describe the biogeochemical cal tools which can be used to address these behavior of forested watersheds in the difficult questions. Answers now are tenta- southern Appalachians. By measuring net tive because we still have much to learn nutrient budgets of experimental watersheds, about forest ecosystems, but we must attempt we can hypothesize mechanisms of nutrient to provide relevant answers. Wood has been recycling and conservation internal to the viewed as eventually supplying up to 20 per- systems. Our watershed-level measurements cent of our current energy needs (Ripley and indicate responses that can be related to Doub, 1978), and the Forest Service has mechanistic process studies. initiated a program to increase the use of Our research results also permit devel- wood for energy fourfold within 10 years opment of both a conceptual framework and (Wahlgren, 1978). specific methods for evaluating the environ- In this paper, our analysis includes mental consequences of alternative land three steps or phases: 1) characterization management practices. We have been con- of ecosystem budgets (input minus output) of cerned with effects on both water quality selected nutrients for several contrasting and sustainable productivity of forests. forest ecosystems located in different physiographic regions of the United States;

137 138 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

2) examination of nutrient pools contained ranging from 130 to 233 cm with both wet and within ecosystem compartments, and annual dry growing seasons and the absence or transfer rates among compartments for these dominance of a snowpack. same ecosystems; and 3) elaboration of the Although N inputs to these systems conceptual framework which has guided eco- differ by a factor of 10 and outputs by a system research at Coweeta, and illustration factor of 2, net budgets are similar, with of how specific data sets can be used to all systems showing an accumulation of N determine important management needs. (Table 1). Organic N is an important com- Proceeding from a general to a more detailed, ponent of input at all sites where this complex analysis, we will attempt to inte- form of N has been measured. The N budget grate theory, data, and modeling in a is most nearly balanced for the old-growth management context. conifer forest at H. J. Aridrews, largely because of small inputs in bulk precipita- tion. The remoteness of Andrews from in- NUTRIENT BUDGETS OF dustrial sources may account for the lower FOREST ECOSYSTEMS deposition of N than at eastern sites, which are in the vicinity of heavy indus- Nutrient budgets of forest ecosystems trial or agricultural activity. This com- are an integrated measure of biogeochemical parison of N budgets includes only hydro- behavior and are thus useful in character- logic constitutents; large gains and losses izing the net result of many interacting which occur in gaseous form will be dis- physical, chemical, and biological process- cussed later. es. Input-output data taken at ecosystem In contrast to N budgets, those for Ca boundaries are valuable for characterizing and K show net losses for all ecosystems undisturbed ecosystems (Likens et al., (Table 1). The wide range of values for Ca 1967), for generalizing across ecosystems discharge reflects differences in bedrock located in diverse physiographic or climatic mineralogy and solubility (Henderson et al., regions (Henderson et al., 1978), and for 1978). The dolomitic bedrock at Walker documenting changes produced by human Branch and the andesitic bedrock at Andrews activities (Likens et al., 1970; Johnson and contribute to especially large stream loss- Swank, 1973; Swank and Douglass, 1975, es of Ca. Gains and losses of K, a rela- 1977). Budgets are derived by monitoring tively mobile cation, are small. Net quantities of precipitation and streamfiow, budgets reflect the combined effects of as well as concentrations of elements in weathering rates and conservation mechanisms water entering and leaving catchments retaining K within ecosystems. Smaller (Bormann and Likens, 1967). The elements losses of this ion from Andrews and Hubbard nitrogen (N), calcium (Ca), and potassium Brook may reflect lower rates of K release (K) have been selected for discussion here from bedrock. based on their importance in tree nutrition, These baseline data are useful in eval- their origin, and their contrasting mobility uating impacts of management activities on in biogeochemical cycles. nutrient cycling only when compared with Average annual inputs and outputs of similar data for manipulated catchments. N, Ca, and K for four contrasting baseline Data in Table 2 were derived by measuring ecosystems representing different physlo- nutrient inputs and outputs for several graphic regions of the United States are altered, young, successional forest eco- shown in Table 1. These four systems pro- systems at Coweeta and comparing them with vide major contrasts in vegetation, bedrock budget data for adjacent undisturbed hard- geology, soils, and hydrology (Likens et wood-covered watersheds. Both white pine al., 1977; Henderson et al., 1978). The and hardwood coppice forests at this site three eastern sites contain deciduous for- show small losses of nitrate nitrogen ests (oak-hickory or northern hardwoods), (NO3-N), no change in ammonium nitrogen while the western site is characterized by (NH4-N), and either no change or small an old-growth coniferous forest. Soils and accumulations of K and Ca, relative to un- bedrock underlying these forests vary wide- disturbed forests. Thus, except for NO3-N, ly among sites, ranging from typic paleu- biogeochemical cycles during developmental dults derived from dolomite bedrock at Oak stages of successional forests at Coweeta Ridge, soils derived from volcanic tuff appear as conservative as cycles for more overlying andesitic bedrock at H. J. mature hardwoods. This conclusion agrees Andrews, typic hapludults derived from with predictions of Vitousek and Reiners granodiorite, gneiss, and schist at Coweeta, (1975). These results suggest that in- to spodosols overlying highly metamorphosed creased losses of nutrients in stream dis- mudstones and sandstones at Hubbard Brook. charge from regrowirig stands are not suff 1- The amount, form, and seasonal distribution cient to deplete site productivity, at of annual precipitation are also variable, least for the time period covered in Table 2. inTable streamflow 1. for four watershed ecosystems in different physiographic regions of the United States Comparison of nitrogen (organic and inorganic) , calcium, and potassium inputs in precipitation and outputs Site Organic N Inorganic N Nutrient Ca K vegetationtype ------Input kg/ha/yr ------Output budget Net Input Output budget Net Input Output budget Net and______-Input Output budget Net Walker Branch, Oak-HickoryTennessee1- 3.7 1.6 +2.1 9.3 1.5 +7.8 12.0 148.0 -136.0 3.0 7.0 -4.0 Hubbard Brook, HardwoodsNorthernNew Hampshire 2 6.5 3.9 +2.6 2.2 13.7 -11.5 0.9 1.9 -1.0 Coweeta, Oak-HickoryNorth Carolina 3 4.3------3.1 +1.2 4.5 0.1 +4.4 4.8 7.7 -2.9 2.1 5.6 -3.5 H. J. Andrews, Douglas-firOregon4 1.5 1.8 -0.3 0.7 0.1 +0.6 2.3 50.3 -48.0 0.1 2.2 -2.1 2Likens'Henderson and Harris, 1975; Henderson et al., 1977; data not available for organic N et al., 1978 4Fredriksen,3Swank and Douglas,1975; Grier 1975; unpublished data for organic N et al., 1974 U) C-2" ri 140 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Table 2. Net loss (-) or gain (+) of selected nutrients in treated watersheds at Coweeta as compared with adjacent hardwood-coveredwatersheds1

Nutrient Treated vegetation, type and age NO3-N NH4-N Ca K

------kg/ha/yr

Eastern white pine (ages 14 through 20 yrs) -0.6 0.0 +2.3 +1.7

Hardwood coppice regrowth (ages 7 through 13 yrs) -2.2 0.0 +0.1 -0.3

'Each value in this table represents the net budget for the treated watershed minus the associated net budget for an adjacent control watershed.

Table 3. Annual change in net nitrogen budget in the first 2 years after road construction and clearcutting on WS 7 at Coweeta-

Years after treatment

Nutrient 1 2

kg/ha/yr ------

NO3-N -0.01 -0.60

NH4-N -0.08 -0.11

Dissolved organic N -0.18 -1.31

2 Particulate organic N -6.16 -1.55

Totals -6.43 -3.57

1Each value in this table is calculatedas the net budget for the treated watershed (WS 7) minus the net budget for the adjacent control watershed (WS 2). 2Suspended solids plus weir pond sediments.

Before this conclusion can be accepted, logging roads. Insignificant changes were however, nutrient losses immediately follow- observed in inorganic and dissolved organic ing logging must be considered. N discharges; however, a net loss of 6.2 As demonstrated in a recent experiment kg/ha was observed for organic N associated at Coweeta (Table 3), elevated losses of N with the elevated discharge of suspended can be expected during and immediately fol- particulates and sediments. This large loss lowing logging activity. Following the of particulate organic N was associated with construction of roads on an experimental two large storms (precipitation amounts of watershed, which disturbed only 5 percent 25 and 15 cm) during the period of road of the area, the mixed oak-hickory forest construction. During the second year of was clearcut and cable logged. Response in treatment and following road stabilization, the first year of treatment was primarily altered N dynamics due to cutting were evi- influenced by the construction and use of dent in the measured ecosystem response. W. T. SWANK & J. B. WAIDE 141

Increased losses of NO3-N and dissolved NUTRIENT DISTRIBUTION AND CYCLING organic N were observed and, when combined WITHIN FOREST ECOSYSTEMS with a reduction in losses of particulate organic N, resulted in a total net loss of A more detailed analysis of potential 3.6 kg/ha in the second year. Taken col- impacts of forest management strategies on lectively, budget data at Coweeta indicate biogeochemistry and sustainable producti- that annual N losses attributable to clear- vity may be obtained by examining processes cutting and natural regrowth via hydrologic of nutrient recycling and conservation vectors are rather small, but may persist internal to forest ecosystems. Such an for at least 20 years (Swank and Douglass, analysis will reveal the major pools of 1975, 1977). The cumulative net N loss is nutrient storage in forests, significant approximately 55 kg/ha. pathways for nutrient transfer among Effects of cutting and harvest activi- storage pools, and mechanisms that regulate ties on nutrient discharge have also been biogeochemical responses to forest altera- documented at the other sites shown in tion. Table 4 summarizes information on Table 1, except for Walker Branch. Modest nutrient distribution and cycling for the increases in losses of NO3-N have been ob- same ecosystems considered in analyses of served following clearcutting and slash nutrient budgets. Values again are given burning in conifer forests of the Cascades for N, Ca, and K. and Coast Range of Oregon (Fredriksen, For all ecosystems, the majority of N 1975). Responses appear to be only slightly is found in the soil organic matter fraction. greater than at Coweeta. On the other hand, Values for the four sites are comparable, in northern hardwood stands hydrologic with the amount of N stored in this compart- losses of N have been substantially greater, ment at Coweeta being slightly higher than both at Hubbard Brook following clearcutting at the other three locations. The second and herbicide treatment (Likens et al., largest N storage pool for the two oak- 1970) and elsewhere in New Hampshire fol- hickory forests is in vegetation. Again, lowing clearcutting alone (Pierce et al., the Coweeta value is higher than those for 1972). However, stream concentrations of the other sites, largely due to higher con- NO3-N at Hubbard Brook appear to return to centrations of N in the roots (McGinty, baseline levels in only 4 to 6 years, per- 1976; Henderson et al., 1978). Vegetation haps due to the depletion of readily miner- pools at all four sites contain between 8 alizable forms of N in litter and soil and 12 percent of the total N in the forest. horizons (Likens et al., 1978). In contrast with the oak-hickory forests, Hence, it appears that increased hydro- ecosystems at Andrews and Hubbard Brook logic losses of nutrients may persist for have the second largest N storage in the varying periods following cutting, but that forest floor compartment. Such a large such losses are not of sufficient magnitude accumulation of N in litter at these sites alone to cause significant reductions in is related to slower decomposition rates site productivity. This conclusion seems (e.g., Gosz et al., 1973; Cromack and Monk, justified, despite the tremendous range in 1975; Fogel and Cromack, 1977) due to nutrient losses after cutting (especially climatic differences (dry summer at Andrews, for NO3-N), and in the underlying mechanisms cold winter with snow at Hubbard Brook). regulating nutrient loss, among forest eco- Stone (1973) has suggested that enhanced systems in the United States (Vitousek et microenvironmental conditions following al., 1979). For northern hardwood forests, clearcutting of northern hardwoods greatly hydrologic losses of N approach the amount accelerate decay rates for these large of N removed in wood products (Likens et litter pools, and that such increased decay al., 1978). But when hydrologic losses rates may explain why these forest eco- from these systems are averaged over normal systems lose so much N in streamwater after rotation lengths of 110 to 120 years, they forest removal. Soil exchangeable N (i.e., do not appear to be severe (approx. 2 kg inorganic mineral N) is the smallest pool N/ha/yr). Thus, if we are searching for in all four forests. Amounts of N in this sources of potential major reductions of pool are highest at Coweeta and Walker site quality following forest cutting, we Branch, perhaps due to more rapid microbial must look beyond increased losses of turnover and mineralization at these sites.

V nutrients (especially N) in streamwater. Table 4 also reveals that litterfall In particular, we must examine in detail is the major aboveground transfer pathway processes of nutrient recycling and conser- in the N cycle. Values for this N transfer vation internal to experimental forested are highest at Hubbard Brook, intermediate watersheds. in the two oak-hickory forests, and lowest at Andrews. Woody increment and uptake (aboveground only) values for the three hardwood forests are fairly similar, and are potassiumTable 4. in four forest ecosystems in contrasting physiographic regions of the United States1 Summary and comparison of compartment sizes and transfer rates for the cycles of nitrogen, calcium, and Z Nitrogen Nutrient and site Calcium Potassium (I)fl-I Compartment sizes (kg/ha) WB HB CIIL HJA WB HB CHL HJA WB HB CHL HJA U)-n'i Vegetationand belowground) (aboveground 470 532 995 560 980 484 830 750 340 218 400 360 -orn MineralForest floorsoil 310 1,256 140 740 430 372 130 570 20 66 20 90 Cd, Total3Exchangeable 4,700 75 4,890 26 6,800 117 4,500 5 3,800 710 9,600 510 2,500 940 4,450 38,000 170 --- 124,000 510 ---860 Percentin vegetation of system total 8.4 8.0 12.4 9.6 16.6 4.4 18.9 Ci..) m1enIf) Transfer rates (kg/ha/yr)Litterfall 39 54 33 21 55 41 44 41 19 18 18 9 I- WoodyCanopy increment leaching 15 3 93 13 4 -2 4 3114 84 23 8 -4 8 19 8 29 6 1331 -115 (1) Uptake4 2.1Data from Bormann et al., 1977; Likens et al., 1977; and Henderson et al., 1978. 57 66 50 23 100 53 75 45 46 53 62 23 Laboratory, North Carolina; HJA, H. J. Andrews,4Hubbard3Values Oregon. BrookSite codesvalues as exclude follows: to 94.5 cm depth at Hubbard Brook, to 60 cm depth at other sites. WB, Walker Branch, Tennessee; HB, Hubbard Brook, New uptakeHampshire; that CHL,is recycled Coweeta in Hydrologic root litter/root exudates. W. T. SWANK & 3. B. WAIDE 143

considerably higher than for the old-growth leaves to woody tissues has been noted at conifer forest, where mortality exceeds all four sites (Henderson and Harris, 1975; growth. Nitrogen leaching is uniformly Mitchell et al., 1975; Bormann Ct al., low at all four sites. 1977; Waring and Franklin, 1979; Franklin, For the Ca cycle, the dominant storage this volume). Such internal redistribution pool is in the soil, either in bound mineral of N may account for more than 50 percent form for the three deciduous forests or in of annual requirements at all sites and may exchangeable form for the conifer stand. be even more important in the Douglas-fir The high total Ca pool at Hubbard Brook may stand than in the three deciduous forests. reflect the fact that the glaciated soils A similar redistribution of K, about one- there are developmentally younger. The third as large as for N, occurs at Coweeta, high exchangeable Ca value for Andrews is although not for the less mobile element associated with the high cation exchange Ca (Waide and Swank, unpub. data). capacity of soils there (Henderson et ml., Several tentative conclusions emerge 1978). Storage of Ca in vegetation is low- from these analyses of nutrient distribution est at Hubbard Brook, and higher and quite and cycling in the four forest ecosystems similar at the other sites. These vegeta- relative to potential management impacts. tion pools represent 4 to 19 percent of the First, much greater amounts of all three total Ca found in these forests. Litter nutrients are stored and recycled within pools of calcium are again lowest at Coweeta, these forests than are lost annually in where decay rates are rapid and immobiliza- drainage waters. This is especially true tion of Ca in litter is low. Indeed, water for N, the cycle of which is more strongly passing through the litter layer at Coweeta biologically regulated, than for the cations becomes enriched in Ca (Best and Monk, 1975). Ca and K, for which cycles and especially Litterfall is also the major mechanism losses are more strongly regulated by geo- for transfer of Ca. Values for this path- chemical factors (Henderson et al., 1978). way are quite similar across all sites. This result reinforces the importance of The aboveground uptake of Ca, and its in- examining internal recycling mechanisms. corporation as annual woody increment, are Second, quantities of N, Ca, and K stored highest for the two oak-hickory forests in vegetation and removed in wood fiber from and lowest for Hubbard Brnok and Andrews. the site do not appear sufficient to cause The latter site shows a negative increment major reductions in site quality. This is value for Ca as it did for N. especially true if nutrient removals are For the K cycle, the overwhelmingly expressed as rates (e.g., kg/ha/yr) averaged dominant storage pool is in bound form in over reasonable rotation lengths. Third, of the soil. Exchangeable K pools are also the pools considered here, the most suscept- quite high and vary across sites in relation ible to management disruptions appears to to soil cation exchange capacities, being be the exchangeable soil pool, as compared especially high at Andrews (Henderson et to annual uptake requirements of vegetation. al., 1978). Vegetation pools are compar- This relationship appears to be more import- able and appear to represent less than 1 ant for N than for Ca or K. For the latter percent of the system total. Storage of K two ions, exchangeable soil pools represent in litter is quite low, reflecting differ- 400 percent to 10,000 percent of annual up- ences in decay rates among sites. take. Comparable values for N range from In contrast to the cycles of N and Ca, 20 percent to 200 percent. Thus, the transfers of K via canopy leaching are amount of N mineralized annually, relative large. Values for K increment and uptake to nutritional requirements of vegetation, are reasonably similar for the deciduous may be the key to a forest ecosystem's forests and are much higher than comparable response to management actions. values for the old-growth Douglas-fir Two components of the N cycle not yet forest. considered may also be especially susceptible Analyses presented so far have excluded to cutting disturbance. These are the two additional mechanisms important in re- microbially mediated gaseous transformations cycling nutrients within forest ecosystems --N fixation and denitrification. Data pre- --root mortality and internal redistribu- sented in Table 5 for Coweeta and Andrews tion. Root mortality may be more important show that for undisturbed forests these than litterfall in returning elements to gaseous inputs and outputs of N are much soil pools at both Walker Branch (Henderson larger than hydrologic components of eco- and Harris, 1975) and Coweeta (Mitchell et system budgets (Todd et ml., 1975; Todd et al., 1975; McGinty, 1976). Such a transfer ml., 1978). Moreover, because these pro- mechanism must also be important at the cesses are mediated by microbial populations, other two sites, although comparative data they may change drastically following for- are currently lacking. Additionally, the est cutting. Microbial populations have importance of retranslocation of N from extremely high growth rates and can respond 144 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS rapidly to changes in forest microenviron- How can we best utilize such data on ments, availability of requisite substrates, undisturbed ecosystems to predict environ- and energy sources. mental consequences of man's resource Thus, our analyses suggest that under- management activities? In a management standing the following three processes in context, it is both impractical and unrea- the N cycle is central to evaluating the sonable to expect precise, quantitative effects of forest management alternatives predictions over millions of hectares of on site productivity: mineralization, in- forest land. Instead, a methodology is puts via biological fixation, and outputs needed to rank or scale one ecosystem rela- via denitrification. Changes in these tive to another based on theoretical and three processes may, in large measure, known behavior. Our approach in attempting regulate the response of the forest eco- to couple ecosystem theory and nutrient system to forest cutting and removal. cycling research with management needs has proceeded within the framework of a con- EVALUATION OF IMPACTS OF MANAGEMENT ceptual model of ecosystem relative ALTERNATIVES ON SITE PRODUCTIVITY stability. Stability is an important con- cept in scientific ecology as well as an We have attempted to use specific data intuitive concept in human experience that both on forest ecosystem nutrient budgets can be related to solving resource manage- and on nutrient distribution and recycling ment problems. The incorporation of within forests to identify possible causes stability concepts into ecosystem analysis of reductions in productivity on intensive- has been discussed by many investigators ly managed forests. We have demonstrated (Child and Shugart, 1972; Waide et al., points at which nutrient cycles, especially 1974; Patten, 1974; Botkin and Sobel, 1975; the nitrogen cycle, may be sensitive to O'Neill et al., 1975; Waide and Webster, management disruptions. These results are 1975; Webster et al., 1975; Van Voris, specific to the sites considered here, and 1976; Botkin, this volume). We have pre- generalization to a wide variety of manage- viously detailed extensions of stability ment situations becomes tenuous. Similar analysis to questions of forest management empirical data are unavailable for a (Waide and Swank, 1976, 1977). variety of forest types because costs and manpower requirements are high for large ecosystem studies.

Table 5. Estimated rates of nitrogen fixation and denitrification for an undisturbed oak-hickory forest at Coweeta, and of nitrogen fixation in several components of an old-growth conifer forest at H. J. Andrews

Site Ecosys tern Process component Coweeta H. J. Midrews

------kg/ha/yr

Nitrogen fixation Phyllosphere 0.22 5.02

Bole 1.00

Woody litter 1.66 2.6

Leaf litter 0.63

Soil 8.55

Total 12.04

Denitrification Soil 10.70

'Todd et al., 1975; Todd et al., 1978; Waide and Swank, 1976. C. Dennison, pers. comm. 3Larsonet al., 1978. W. T. SWANK & J. B. WAIDE 145

Conceptual Model of Resistance deviation, the greater the resistance of the and Resilience ecosystem. The second component of response to We begin by considering the general disturbance is the resilience of the eco- nature of an ecosystem's response to dis- system--i.e.. the rate at which the eco- turbance. Illustrated in Figure 1 are system recovers or returns to within a several hypothetical responses to an eco- definable range of pre-disturbance function. system disturbance such as clearcutting, The faster the system recovers, or the fire, or major windstorm. The vertical shorter the time required to return to a axis in this diagram represents the devia- previous level of function, the more tion of some (unspecified) functional pro- resilient the ecosystem. The several curves perty or measure of the state of the eco- depicted in Figure 1 were chosen to illus- system from a nominal or pre-disturbance trate different possible combinations of level. The horizontal axis represents time, resistance (extent of displacement) and in any appropriate units. Such curves are resilience (rate of recovery) meant to be quite general and could repre- The curve forms shown in the graphical sent, for example, changes in streamfiow model of ecosystem disturbance and recovery volumes, NO3-N concentrations in stream- (Fig. 1), as well as many other similar water, or total losses of K following for- curves, may be generated by the following est cutting. If the curves were inverted equation for a second-order damped oscilla- (i.e., were mirrored across the horizontal tor (i.e., a pendulum): axis in Fig. 1), they might represent total forest biomass or productivity over the y + 2e + w2y = w2z. period of post-disturbance succession. A similar conceptual approach was taken by In this equation, y and z represent outputs Trudgill (1977) in his analyses of terres- and inputs of the system of interest, the trial nutrient cycling. dot and double-dot notations indicate first As illustrated in Figure 1, two com- and second derivatives with respect to time, ponents of ecosystem disturbance and an is the undamped natural frequency of the recovery may be recognized (Table 6). The system, and is the damping coefficient. first is the maximum extent of system dis- This second-order equation is used only as placement from a pre-disturbance functional an analogy to an ecosystem's response to level, or the resistance of the ecosystem. disturbance, and as a means of quantifying The smaller the deviation from a nominal the concepts of resistance and resilience. functional level for a given amount or type As will be shown below, we associate of disturbance, or the greater the distur- quantitative indices of resistance and bance required to produce a given maximum resilience with the magnitudes of and .

Ui F- U) >- 0 0

I I- 0 F-LU

2 0 0I- z S

Figure 1. Hypothetical response of an ecosystem following a specific disturbance (fire, windstorm, clearcutting). The vertical axis represents the deviation of some unspecified functional property or measure of the state of the ecosystem from its nominalor pre- disturbance level. The horizontal axis represents time, in unspecified units. Several possible responses to disturbance are shown, each differing in the magnitude of deviation from the pre-disturbance level of function (resistance) and in the rate ofrecovery or return to the previous state (resilience). 146 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Previous analyses of hypothetical variability in functional processes during models of ecosystem nutrient cycles times of environmental stress. Also re- (Webster et al., 1975) indicated that eco- lated to ecosystem resistance is the con- system resistance is related to the presence cept of a "big-slow" component in terres- of organic components having large standing trial ecosystems (O'Neill et al., 1975; stocks with slow turnover. However, O'Neill and Reichle, this volume). The resilience is high when biotic components term big-slow refers to large storage pools have low mass but high turnover cr metabolic of organic matter and elements which turn rates. These general conclusions agree well over slowly. Such big-slow components are with current understandings of functional believed to buffer ecosystems against properties of forest ecosystems. For environmental extremes and serve as an al- example, Waring and Franklin (1979) and ternate energy base during times of stress. Franklin (this volume) suggest that the Again, such a functional component contri- large size of dominant trees in coniferous butes to the resistance property of eco- forests of the Pacific Northwest "provides systems. a buffer against environmental stress Similarly, we interpret the functional (especially for nutrients and moisture)" role of pin cherry in disturbed forests at (Waring and Franklin, 1979, p. 1380). By Hubbard Brook (Marks, 1974) in terms of storing large amounts of water and nutrients resilience. The high rate of growth and (especially N) internally, conifers are elemental uptake by pin cherry, and its buffered against extremes of water and rapid accretion of biomass and leaf area, nutrient availability in the climate typical contribute to the recovery of northern of the region. This is certainly directly hardwood forests following severe distur- related to the concept of ecosystem re- bance. Webster and others (1975) suggested Sistence--massive trees storing large that successional species regulate the quantities of water and N, thereby reducing resilience of ecosystems following distur- bance.

Table 6. Definition of resistance and resilience as two complementary components of ecosystem relative stability1

Component Analogous terms Meaning

Resistance Inertia 1. Inversely proportional to the amount by Rigidity which some functional property or measure of the State of the ecosystem deviates from a nominal level in response to a specific disturbance.

2. Directly proportional to the extent of disturbance required to produce a certain magnitude of deviation in some ecosystem functional property.

Resilience Elasticity 1. Directly proportional to the rate at which Restoration time some functional measure of the state of the Classical stability ecosystem recovers or returns to a pre- disturbance or nominal level.

2. Inversely proportional to the time required for ecosystem recovery following disturbance.

1See Figure 1 for diagrammatic illustrations of these concepts. W. T. SWANK & J. B. WAIDE 147

Because this conceptual model of eco- regulated mechanisms of ecosystem homeo- system disturbance and recovery Is central stasis exist in response to environmental to our analyses in the remainder of the oscillations acting at a wide variety of paper, and because it has been criticized frequencies (Schindler et al., in press). both generally (Botkin and Sobel, 1975; Therefore, the concepts of resistance Botkin, this volume) and specifically and resilience are appropriate at two quite (Harwell et al., 1977), several additional different levels of analysis. At one level points must be made about the sense in of analysis, the concepts of resistance and which we are using the model. First, we resilience relate to the persistence of are in no way suggesting that an ecosystem ecosystems within temporally variable behaves like a pendulum. We are using the environments. The physicochernical environ- equation of a second-order damped ment impinging on any natural ecosystem oscillator, and specifically the curve forms varies, often substantially, over time. in it generates, as an analogy or general model this sense, resistance and resilience relate of ecosystem responses following some man- to the integrated sets of responses of the induced or natural environmental distur- biotic components of ecosystems for per- bance. We are taking advantage of the well- sisting in the face of environmental accepted engineering approach (Shinners, oscillations (Webster et al., 1975). At 1972) of using a second-order model to quite another level of analysis, ecosystems approximate the behavior of a higher-order exhibit functional responses to specific system. This approach allows us to quantify disturbances, both natural disturbances and or derive indices for the concepts of eco- those induced by man. The nature of the system resistance and resilience. But response to a specific disturbance allows these indices are of value only in a com- us to recognize the ecosystem as being parative sense, and only in the context of highly resistant or not (extent of displace- specific theoretical or applied questions. ment from previous level of function) and Second, we are not considering forest highly resilient or not (rate of recovery disturbances severe enough to cause a new to previous level of function). ecosystem to appear on site. For example, It is at the first, more theoretical following the clearcutting of WS 2 at level of analysis identified above that the Hubbard Brook, WS 7 at Coweeta, or WS 10 at concepts of resistance and resilience were H. J. Andrews, one would expect the regrowth first defined explicitly (Webster et al., of northern hardwoods, oak-hickory, and 1975). It is also at this level that Douglas-fir forests to be similar in all Watson and Loucks (1979) recently analyzed quantifiable functional properties to the the turnover times of organic matter, N, pre-cut forests, differing mainly in details and P in Lake Wingra. However, it is at of species composition. the second, more applied level of analysis Third, in these analyses we are mea- that the concepts of resistance and resil- suring the state of the ecosystem in terms ience have been previously applied to pro- of functional variables, not in structural blems of forest management (Waide and Swank, terms. Species composition is not used as 1976, 1977; Huff et al., 1978) and in which a measure of the state of the ecosystem. they will be employed here. Within this context, the curve forms depicted in Figure 1 correspond well to responses documented in a variety of water- Resistance, Resilience, and the shed manipulation experimerjts throughout Nitrogen Cycle this country, for many types of functional variables: total streamflow, total evapo- The concepts of resistance and resil- transpiration, net production, total forest ience will now be quantified for models of blomass, litterfall, stream nutrient con- the N cycle for two forest ecosystem types centrations. Thus, our approach is based important in the southeastern United States, upon a reasonable general model of eco- a natural oak-hickory forest and a loblolly system disturbance and recovery. pine plantation. Details of parameter Finally, rather than using this con- estimation for the second-order model are ceptual approach to analyze the static given elsewhere (Waide and Webster, 1975; stability (Botkin, this volume) of eco- Webster et al., 1975; Waide and Swank, systems, we argue that the context in which 1976). this model is used is consistent with a Figure 2 depicts a compartment model stochastic view of both ecosystems and of the N cycle in an undisturbed hardwood environments. The apparent resistance and forest at Coweeta (see Mitchell et al., resilience of forest ecosystems following 1975, for details of model construction). cutting results from the evolution of biotic The model provides estimates of pool sizes components of forests within continuously (kg N/ha), vegetation increments (kg N/ha/ variable environments. Thus, biotically yr), and transfers of N among compartment 148 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

(kg N/ha/yr). For comparison, a compart- Swank, 1976, 1977). Hence, direct compari- mental model for the N cycle in a 16-year- son of results for the two systems is old loblolly pine plantation in the Duke difficult. Forest, North Carolina, is shown in Figure Results of relative stability analyses 3. Values shown are from studies by Wells for these two nitrogen models are shown in and Jorgensen (1975) and by Wells and Table 7. Resistance of the ecosystem models others (1975). Inspection of these figures is inversely related to the natural fre- shows that both forests are dominanted by quency, w (Webster et al, 1975). In fact, large storage pools of N which turn over for these systems, it can be shown analyti- slowly. The loblolly stand, in comparison cally (Waide, unpub.) that resistance is with the oak-hickory forest, has a smaller directly proportional to Values in proportion of the total N in the system con- Table 7 thus suggest that the oak-hickory N tained in vegetation pools, with nearly cycle is more resistant to displacement than twice as much N in the litter and only about the loblolly cycle. half as much soil N. Interpretations of resilience values The most dynamic portion of the N cycle depend on whether one is interested in a for the oak-hickory forest at Coweeta (Fig. relative (Webster et al, 1975) or an 2) is in the soil, with high rates of absolute (Harwell et al., 1977) index. transfer between microbial and mineral N Given two ecosystems, the value oftalone poois. Similar data were unavailable for provides a good measure of resilience if the loblolly plantation; thus, the two values of the natural frequency (u) for nitrogen models are conceptualized at the two systems are within one order of grossly different levels of resolution. magnitude: the closer is to 1.0, the The importance of level of resolution to more resilient the system. However, if systems analyses has previously been docu- values of wfor the two systems differ by mented for these two mbdels (Waide and at least an order of magnitude, resilience

0 Litt.r 3.797 2.738 34.58 x7

40.27 r:u I 1x9 3873.

8628 IlirbivoregI1 I 02 L.it$ir

.388 I I I 62.47 lx" )1 Soil Founo xa 3.377 l.201j2.033

6432I I______113.80 xe x14 I 0 Litti, NO3-N 34.58 33.60 Woody Litis, 957 242 I

194.2 I I 40.27 th773 45U0 4.214

[X$4 10.81 Mic rot

I NO3-N 131.3 15G7 I 33.6 78I x9 11282.0 A$5 11.181 )j I__i N144-N 1 orrhlSo. Mottr NH4-N 1195.6 IJOrgO 62.41 I 52.92 I 94.9 3873 k.I 52.92

Figure 2. Compartment model of the nitrogen cycle in an undisturbed oak-hickory forest at Coweeta. Shown in the left half of the diagram are storage pools and flows associated with N uptake from and return to soil pools.Compartments and flows associated with decomposition and N mineralization are depicted in the right portion. Values in boxes represent the magni- tudes of nitrogen storage pools (kg/ha). Numbers within rectangles in vegetation compart- ments represent annual increments (kg/ha/yr). Rates of nitrogen transfer among storage pools are shown on arrows, in units of kg/ha/yr (see Mitchell and others, 1975, for details of model construction; figure modified from Mitchell and others, 1975). W. T. SWANK & J. B. WAIDE 49

is proportional toC.w. The absolute time nearly identical. Clearly, this is not the required for recovery (the inverse of case for the two forest types considered absolute resilience) is proportional to here. Thus, the relative index of resil- Thus, relative and absolute indices ience is more appropriate for our analyses. of resilience provide different interpreta- idso, we are largely concerned here with tions in this case (Table 7), suggesting questions of forest resistance to various that the oak-hickory nitrogen cycle is more management strategies, for which the resilient (relative) or less resilient analyses (Table 7) give unambiguous results. (absolute) than the loblolly pine cycle. Finally, we again emphasize that the N However, from a practical standpoint, the cycle in the two forests is conceptualized absolute index (l/w) is useful only if at different levels of resolution, compli- the allowable recovery times (i.e., the cating interpretations of results. rotation lengths) of the two systems are Nonetheless, relative stability analy- ses indicate that management impacts on the N cycle would be greater in the loblolly pine plantation than in the oak-hickory for- est. This conclusion will be examined in light of specific simulation predictions 52.2 New I Old below. Leaves Leaves 55.0 27.0

Simulations of Alternative 55.0\ /17.0 Management Strategies

The previous discussion provides an 4.5 Branches LItter operational framework for predicting com-- 60.0 307.0 parative biogeochemical responses of differ- ent forest ecosystems to manipulation. In this section, we consider specific manage- 49.1 ment alternatives and use the compartmental models (Figs. 2,3) to simulate changes in N pools and associated impacts on pro- Stems ductivity. In related papers, we have dis- 115.0 cussed a wider variety of simulations (Waide and Swank, 1976) and have predicted changes in several compartments of the N 54.41 125.2 cycle (Waide and Swank, 1977). Here, for illustrative purposes, we discuss only a 48.7 few representative forest alterations and Roots their simulated effects on the soil N pool. SoIl I 64.0 1753.0 104.6 I Details of simulation models may be found in our earlier papers. Management practices simulated for Figure 3. Compartment model of the nitro- oak-hickory and loblolly pine forests are gen cycle in a loblolly pine plantation in shown in Table 8. These alternatives focus the Duke Forest. Labeling terms same as in on rotation length and degreeof tree Figure 2 (see Waide and Swank, 1976, for utilization, two practical decisions faced details of model construction; figure modi- by managers today. Changes in soil N for fied from Waide and Swank, 1977).

Table 7. Comparison of relative stability indices for the nitrogen cycle in southeastern oak-hickory and loblolly pine forest ecosystems

Indicesof Resistance Indices ofResilience Ecosystem type Wn 1/a2 1kw

Oak-hickory 0.106 89.0 0.906 10.4 loblolly pine 0.167 35.9 0.850 7.0 150 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

CD CD

CD

d

0.00 TIME (TERFiS)

CD CD 0

00 TIME (YERFiS)

Figure 4. Simulated changes in total soil nitrogen (kg/ha) for (A) oak-hickory and (B) loblolly pine forest ecosystems following several types of forest alteration. All simula- tions begin at time = 0 with a recently cut, regrowing forest. Cutting alternatives in part (A) are: a. uncut forest; b. merchantable harvest, 90-yr rotation; c. merchantable harvest, 50-yr rotation; d. complete-tree harvest, 90-yr rotation. Cutting alternatives in part (B) are: a. uncut forest; b. merchantable harvest, 30-yr rotation; c. merchantable harvest with residue removal, 30-yr rotation; d. complete-tree harvest with residue removal, 30-yr rotation. 8. T. SWANK & 3. B. WAIDE 151 each management alternative (Table 8) are sidered typical for each site, it is clear compared with values for an uncut oak- from values in Table 9 that increased levels hickory forest over four successive rota- of wood fiber utilization are predicted to tions in Figure 4(A). For all simulated have a greater impact on the loblolly pine alternatives, depletion of soil N increases than on the oak-hickory forest. This re- with each succeeding harvest. The merchant- sult is consistent with the relative able harvest with 90-year rotation length stability comparisons of the two sites, produced the least impact, with a 405 kg/ha specifically the resistance component (11%) depletion in soil N at the end of the (Table 7). However, even for the oak-hickory first rotation. Shortening the rotation forest, increased levels of wood utilization length to 50 years produced large addition- from a merchantable to a complete-tree har- al decreases in soil N, as did the simulat- vest nearly doubled the predicted reduction ed complete-tree harvest with a 90-year in yield in subsequent rotations. Hence, rotation. increasing the frequency or the level (or Simulation results from the loblolly both) of wood fiber harvest may lead to pine model are shown in Figure 4(B). The significant reductions in productivity. merchantable tree harvest with no residue Such reductions may be quite severe, removal showed little difference from the especially for the pine site. uncut forest, but increased removal of These simulated reductions in yield plant material associated with the other are consistent with experimental evidence alternatives produced substantial reduc- from other areas such as Australia (Keeves, tions in soil N. As suggested previously 1966), New Zealand (Whyte, 1973), and (Waide and Swank, 1976, 1977), if suffi- Europe (Troup, 1928), where reduced pro- cient soil dynamics data were available to ductivity of conifer plantations has been provide an expanded pine model, simulated documented over several successive rota- changes in soil N might be even larger. tions. With specific reference to N, We are Interested not only in changes Weber (1978) concluded that fertilization in soil N for these two forests, but also in would be needed to sustain productivity of changes in yield of forest products associ- Pinus radiata in New Zealand under intensi- ated with any reductions in soil N. Data fied management practices such as shorter for all management alternatives considered rotations, closer utilization, and slash here (Table 9) are based on assumptions that burning. Nutrient cycling studies in a yield of wood fiber is directly proportional variety of forest ecosystems in North to standing crops of nitrogen in vegetation America have similarly led investigators to compartments (Figs. 2, 3). If the merchant- express concern about impacts of intensi- able stem harvest, without residue removal fied management on nutrient removals, soil and for a "standard" rotation length (90 impoverishment, and site degradation yrs for hardwood, 30 yrs for pine) is con- (Boyle et al., 1973; Kimins, 1977; Patric and Smith, 1975; Pritchett and Wells, 1978;

Table 8. Summary of management alternatives considered in model simulations of the nitrogen cycle in eak-hickory and loblolly pine forest ecosystems1

Rotation length Ecosystem type Type of cut Residue removal (years)

Oak-hickory Merchantable No 90

Merchantable No 50

Complete-tree No 90

Loblolly pine Merchantable No 30

Merchantable Yes 30

Complete-tree Yes 30

1See Figures 2 and 3. 152 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Aber et al., 1979). Based on findings at specific, and both ecosystems analyzed here Hubbard Brook, Likens and others (1978) are of average or better quality. There- concluded that conventional rotation lengths fore it is not unreasonable to expect even (110-120 years) for even-aged hardwood in greater impacts on sites which are less the White Mountains of New Hampshire would fertile initially. We feel that the not seriously affect nutrient replenish- strength of our analyses lies in the over- ment and long-term productivity. However, all approach taken, and we submit that the these authors pointed out that such ques- qualitative, comparative aspects of our tions must be reexamined for intensified predictions are useful. Refined stability management practices. Indeed, other analyses and simulation models incorporat- analyses (Hornbeck, 1977; Aber et al., ing improved data might be utilized to rank 1978) indicate that replenishment of avail- expected responses of specific ecosystems, able N in such ecosystems could be a pro- areas, or entire regions to intensified blem following whole-tree utilization or management. Energy plantations, more com- shortened rotations. Simulated changes in plete fiber utilization, or shorter rota- available N pools (NO3-N and NH4-N) in oak- tions might be evaluated in this manner. hickory forests at Coweeta (Fig. 2) parallel Another appealing aspect of the modeling changes shown in total soil N in Figure approach is that data from many sources can 4(A). Hence, a consistent conclusion is be used in a framework that is consistent drawn from our simulation predictions, from with theoretical treatments of ecosystem our earlier analyses of storage pools and dynamics. With the need to provide transfer rates in the N cycle for several immediate answers to problems that may forest ecosystems, and from the results of evolve over long periods of time, this gen- Aber and others (1978). Mineralization of eral approach appears to be the only viable N may be insufficient to meet uptake recourse. requirements of successional vegetation We have also used our modeling approach following intensive forest management in to identify specific research needs. For the Southern Appalachians. example, the partitioning of N losses and It is important to recognize limita- accretions for the hardwood simulations tions in our simulation results. The models (Table 10) provides a basis for placing of N cycling (Figs. 2,3) are incomplete; priorities on future studies. In terms of improved information is needed for certain losses, increasing levels of fiber removal processes, particularly belowground N can double the N loss rate in wood products, dynamics. Also, our results are site but denitrification still appears to be the

Table 9. Predicted changes in yield of forest products after three simulated rotations for several forest management alternatives for southeastern oak-hickory and loblolly pine forest ecosystems

Predicted change in Ecosystem type Type of cut yield (%)

Oak-hickory Merchantable, 90-year -10.3 rotation

Merchantable, 50-year -12.7 rotation

Complete-tree, 90-year -16.8 rotation

Loblolly pine Merchantable, 30-year rotation +6.9

Merchantable with residue removal, 30-year rotation -24.9

Complete-tree with residue removal, 3O-year rotation -29.5 W. I. SWANK & 3. B. WAIDE 153

dominant reason for simulated reductions in Youngberg and Wollum (1976) estimated fixa- soil fertility and fiber yield. Thus, tion by this species to be about 1,000 large errors in estimating losses via fiber kg/ha over a 10-year period. Significant N removal and stream discharge are greatly fixation by other woody species in forest overshadowed by minor inaccuracies in ecosystems in Oregon has also been docu- denitrification estimates. Yet, we know mented (Dyrness and Youngberg, 1966; Dalton little about denitrification in forest eco- and Zobel, 1977; Newton et a]., 1968). systems. Improved field techniques are Lichens are another important biological urgently needed to provide estimates of rates symbiont; Pike and others (1972) found large of deriitrification in forest soils. accretions of nitrogen in the phyllosphere Similarly, biological fixation of N is of older Douglas-fir stands by Lorbaria viewed as the primary mechanism of accre- oregana. Major research is needed to quanti- tion, but quantitative information for a fy gaseous nitrogen transformations in un- variety of forest ecosystems is lacking. At disturbed and managed forest ecosystems. Coweeta, rates of N fixation have increased roughly sevenfold in the first 18 months after cable logging (Todd and Waide, unpub. CONCLUSIONS data), but the duration of such elevated N inputs is unknown. In the southern At Coweeta we plan to continue study- Appalachians, black locust (Robinia pseudo- ing the problems discussed in this paper by acacia L.), a legume, is a ubiquitous early improving our current techniques of measure- successional tree species on disturbed ment, and by more intensified sampling of N sites. Ike and Stone (1958) estimated an fixation, immobilization, mineralization, accumulated N increase of nearly 700 kg/ha denitrification, and N availability associ- in the soil of a 16- to 20-year-old black ated with forest management practices in- locust plantation. In the Pacific North- volving traditional and increased levels of west, snowbrush (Ceanothus velutinus) is an wood utilization. Recently initiated early successional, nonleguminous plant; research in this area is part of a coopera-

Table 10. Simulated components of total gains and losses for the nitrogen cycle in a southeastern oak-hickory forest ecosystem subjected to alternative management strategies1

Component Merchantable Merchantable Complete-tree of loss harvest, 90-yr harvest, 50-yr harvest, 90-yr Uncut or gain rotation rotation rotation forest

------kg/ha/yr------

Nitrogen losses

Fiber removal 2.0 3.4 5.3 0.0

Stream discharge 0.5 0.7 0.5 0.3

Denitrification 16.1 18.8 15.5 11.2

Total 18.6 22.9 21.3 11.5

Nitrogen gains

Fixation ------10.9

Precipitation ------3.4

Total ------14.3

'Values sho are averaged over the indicated rotation length. 154 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

tive project that includes similar studies Best, G. R., and C. D. Monk. 1975. Cation at H. J. Aridrews, Hubbard Brook, Oak Ridge, flux in a hardwood forest watershed Clemson University in the South Carolina and an eastern white pine watershed at Piedmont, and the University of Washington. Coweeta Hydrologic Laboratory. In Our goal is to couple extensive nutrient Mineral Cycling in Southeastern Eco- cycling data with specific process-level ystem, edited by F. C. Howell, J. B. research for the purpose of filling gaps in Gentry, and M. H. Smith, pp. 847-861. our ability to evaluate alternative manage- ERDA Symp. Series (CONF-7405l3). ment practices. We also intend to improve the nitrogen simulation models described Bormann, F. H., and G. E. Likens. 1967. here and to test or validate our approach Nutrient cycling. Science 155:424-49. with experimental data on yield and pro- ductivity for pine plantations with various Bormann, F. H., C. E. Likens, and J. M. rotation lengths. Melillo. 1977. Nitrogen budget for Specific simulation studies within the an aggrading northern hardwood forest context of our conceptual model of eco- ecosystem. Science 196:981-983. system resistance-resilience will remain an integral component of our total research Botkin, D. B. 1980. Perturbation frequency effort. Modeling activities serve to focus and ecosystem stability. In this research initiatives and to integrate pro- volume. cess-level information in the context of system-level hypotheses. Such activities, Botkin, D. B., and N. J. Sobel. 1975. however, become disoriented and inefficient Stability in time-varying ecosystems. unless an overall conceptual model is re- Amer. Natur. 109:625-646. tained. Thus, both conceptual and simula- tion models serve as evolving hypotheses Boyle, J. R., J. J. Phillips, and A. R. Ek. about the dynamical behavior of forest eco- 1973. "Whole tree" harvesting: nutri- systems, useful at any instant to make ent budget evaluation. J. For. 71: specific predictions, but also malleable as 760-762. new data or interpretations become avail- 1972. able. Child, G. I., and H. H. Shugart, Jr. We submit that the integration of Frequency response analysis of magnes- empirical research and modeling in the con- ium cycling in a tropical forest eco- text of a general theory is the only viable system. In Systems Analysis and method of answering the serious questions Simulation in Ecology, Vol. 2, edited concerning sustainable productivity facing by B. C. Patten, pp. 103-135. New managers of forest resources. The only York: Academic Press, Inc. alternatives are piecemeal studies or wait- and-see attitudes. Neither will suffice in Cromack, K., Jr., and C.D. Monk. 1975. the multi-demand environment within which Litter production, decomposition, and resource management decisions must currently nutrient cycling in a mixed hardwood be made. watershed and a white pine watershed. In Mineral Cycling in Southeastern Ecosystems, edited by F. G. Howell, LITERATURE CITED J. B. Gentry, and M. H. Smith, pp. 609-624. ERDA Symp. Series Aber, J. D., D. B. Botkin, and J. M. Melillo. (CONF-740513). 1978. Predicting the effects of dif- ferent harvesting regimes on forest Dalton, D. A., and D. B. Zobel. 1977. Eco- floor dynamics in northern hardwoods. logical effects of nitrogen fixation Can. J. Forest Res. 8:306-315. by Purshia tridentata. Plant Soil 48: 57-80. Aber, J. D., B. B. Botkin, and J. M. Melillo. 1966. 1979. Predicting the effects of dif- Dyrness, C. T., and C. T. Youngberg. ferent harvesting regimes on producti- Soil-vegetation relationships within vity and yield in northern hardwoods. the ponderosa pine type in the central Can. J. Forest Res. 9:10-14. Oregon pumice region. Ecology 47: 122-138. Balmer, W. E., and N. G. Little. 1978. Site preparation methods. In Proceed- Fogel, R., and K. Cromack, Jr. 1977. ings: A Symposium on Principles of Effect of habitat and substrate quality Maintaining Productivity on Prepared on Douglas-fir litter decomposition in Sites, edited by T. Tippen, pp. 60-64. western Oregon. Can. J. Bot. 55: Starkville: Mississippi State Univer- 1632-1640. sity Press. W. T. SWANK & J. B. WAIDE 155

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Youngberg, C. T., and A. T. Wollum. 1976. Nitrogen accretion in developing Ceanothus velutinus stands. Soil Sci. Soc. Amer. J. 40:109-112. Geomorphology and Ecosystems

Frederick J. Swanson

INTRODUCTION system and on a variety of time scales. Hack and Goodlett (1960) argue that the Natural ecosystems develop through the landscape and vegetation development models interplay of physical and biological fac- of Davis and Clements are incorrect in tors. Biological factors have traditionally their application to the Appalachian Moun- been emphasized because most ecologists have tains where they were initially developed. life science backgrounds. The purpose of A model involving steady state in an open this paper is to explore the significance system has greater explanative power and of earth science perspectives in under- heuristic value in Hack and Goodlett's standing ecosystems. Particularly in moun- view. A system nay be shifted from steady tain landscapes and along streams and state by a variety of disturbances ranging rivers, geomorphic processes and landforms from short-term events such as flash floods have important roles in the development and to long-term changes in climate or relief. geographic distribution of plant and animal Those components of the system, whose rate communities. Geomorphologists and ecolo- of response is fast relative to disturbance gists working in these dynamic landscapes frequency, react to produce a new steady have long relied on insights from each State. other's discipline to interpret causes and This view of a dynamic landscape-eco- patterns of ecologic and geomorphic change. system with the potential for biotic-geomor--- The full richness of geomorphic-biologic phic interaction over a broad range of time interactions really emerges from programs scales is the subject of this paper. First, of ecosystem analysis where earth and life I will discuss time scales of geomorphic and scientists work closely together on com- ecosystem variation and consider the impor- mon topics, sites, and tLne frames. tance of a broad time perspective in analyz- In the pre-twentieth century of ing landscape and ecosystem development. naturalists, the mixing of earth and life From this perspective,I will briefly science perspectives was common. In this examine an array of interactions among century, there has been parallelism and fauna, flora, landforms, and geomorphic interchange in the evolution of general processes, concluding with a more detailed models in geoinorphology, plant ecology, and analysis of soil and sediment movement animal ecology (Drury and Nisbet, 1971). through forest watersheds and the role of William Morris Davis' cyclical model of vegetation in regulating material transfer long-term (l07_108 years) landform develop- and storage. ment set the stage for the views of vege- tation development put forth by Clements (1936) and Braun (1950). The interpreted TEMPORAL PERSPECTIVES vegetation and landforms as progressing to- gether toward a common end point--the pene- How one perceives interactions between plain with deep mature soils and "climax" geomorphic and ecosystem factors depends not vegetation on a nearly level landscape. only on the particular landscape and eco- Gilbert (1880), Gleason (1926), and system in question, but also on the time Hack and Goodlett (1960) put forth alter- scale used for viewing the system. Types native concepts of landform-vegetation and intensities of interactions between relations based on dynamic short-term plants and landforms, for example, on the (immediate) interactions among vegetation, long-time frame of landform development and soils, water, and landforms in an open

159 160 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

biologic evolution contrast with the short- scales, landforms of intermediate spatial term interaction of daily operation of geo- scale, such as terraces, fans, and moraines, morphic processes and growth response of form in response to exogenous events.On individual plants. Thus, in order to still longer time frames, landform elements examine physical-biotic relationships in of greater geographic extent develop as the natural ecosystems, it is useful to recog- Sum of all higher frequency geomorphic nize the full range of temporal scales of responses to exogenous events. variation in both physical and biological Vegetation also responds in various parts of the system and then compare system ways across this broad time range. Indivi- behavior at appropriate time scales. dual plants have physiological response to To help clarify this point, let us daily and seasonal fluctuation of moisture look at an example from the Douglas-fir! and temperature regimes. On the scale of western hemlock forest ecosystem in the centuries, vegetation (secondary) succession Cascade Mountains of Oregon (Table 1). This occurs following major ecosystem distur- charting of temporal scales of landscape- bances such as fire, landslides, and ex- ecosystem change is an outgrowth of the pro- tensive blowdown events. Primary succes- cess of earth scientists and biologists sion, shifts in the range of species and learning to work together in an interdisci- plant communities, and microevolution plinary research team, the Coniferous For- occur, in part, in response to and on the est Biome (CFB) of the U.S.,'International time scale of major climatic change. Most Biological Program. In early 1970, I began significant macroevolution takes place over working with CFB as a geologist mapping bed- still longer time periods. rock in the H. J. Andrews Experimental For- To some extent, Table 1 is arranged in est, a primary CFB study site. Although a hierarchical structure. Geomorphic and working side by side with terrestrial and vegetative changes on each time scale in- aquatic ecologists, we had little in com- volve response to exogenous events at that mon, because our time frames were disjunct. time scale as well as to the sum of all I was mapping formations no younger than higher frequency variation in that system. 3.5 million years old; the time period of For example, formation of terraces and major concern to the ecologists was the alluvial fans may be facilitated by climate annual scale of nutrient budgets and physio- change and glaciation on the scale of logical behavior of plants and animals. to lO years, but the actual constructional These differences in time perspective raised processes occur as more frequent "base questions about the sorts of geomorphology- flow" erosion and pulses of accelerated ecosystem interactions that occur over the sedimentation at the scales of decades and full range of time scales from days to mil- centuries. lions of years. Where is the common ground One aspect of hierarchially organized for interaction between geomorphologists systems is that system behaviors are "nearly and ecologists? decomposable," such that system behavior at Major exogenous events affect eco- one level or frequency may be isolated from systems and landscapes over a broad range scales of variation of higher and lower of frequencies of occurrence (Table 1). frequencies (Simon, 1973; Monk et al., These events include climatic and geologic 1977). Many studies of natural systems processes as well as major disturbances of focus on one organizational level, assuming vegetation such as fire for which ignition that lower frequency variations of the may be considered exogenous, but intensity system are so slow that they can be consider- and areal extent of burns may be controlled ed constant and higher frequency behaviors by endogenous vegetation and landscape are so rapid "that only their steady state factors. Some of these events are regular properties appear in the system description" and cyclical in occurrence, while others (Monk et al., 1977). However, CFB research are episodic and their frequency would be in natural systems has revealed many pro- considered here in terms of average return blems with this common assumption. A not- period. able example arose when aquatic ecologists Geomorphic factors vary over this time began to compile an annual carbon budget scale, ranging from relatively frequent for a small stream ecosystem. After sampl- changes in rates of geomorphic processes to ing two successive years and finding two the long-term development of the physio- very different budgets, they quickly graphic province as a whole. Development realized that the annual scale of behavior of progressively larger landforms occurs on of this system depended strongly on stream- progressively longer time scales. Geo- flow characteristics for the sample period. morphic response to the most frequent exo- Inputs exceeded output by about 40% in a genous events listed does not lead to dry year, but were nearly balanced in the development of landforms attributable to an wetter year, although no major peak flows individual event. At intermediate time occurred (Triska et al., in press). Table I. Geonr3rphic and vegetative variation and exogenous events affecting ecosystems and landscapes on an Eventarray frequencyof time scales (yrs) (example from Douglas-fir/western hemlock forests in Cascade Mountains, Oregon) txogenous events eomorpnic variation Vegetation variation 10-2 to 10-1 Precipitation- discharge event "Base-flow" erosion by Physiologic response 102100 to 101 ExtremeAnnual water storms, budget, majormoderate storms Periods of acceleratednoncatastrophic processes of individual plants l0 to l0 Climate change, tationdisturbances (e.g., offire) vege- Intermediate-scale land-erosion--slidechannel changes, scars, etc. Secondary succession 106 Episodes of volcanismglaciation Gross morphology of majormoraineS,forms; terraces, etc. fans, Primary Succession,microevolutiorimigration, l0 to 108 Development of physiographicprovincedrainagetional (volcanic)asand a construc-whole landforms Macroevolution -n (y)(5 162 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Furthermore, the system had a good memory GEOMORPHOLOGY ECOLOGY for detrital input and channel flushing events in earlier years. It is necessary to place annual budgets in the context of IA I FAUNA broader temporal variability of the system LANDFORMS (the 102 yr scale of Table 1). Geomorphology-ecosystem interactions are most dramatic on intermediate time scales--decades and centuries (Table 1). On longer and especially shorter time frames, geomorphic setting is commonly viewed as a GEOMORPHIC FLORA passive, invariant stage on which evolution PROCESSES F

and plant physiologic behavior take place. I But on the intermediate scale of secondary succession, change in plant community com- Figure 1. Relationships among landforms, position, vigor, and structure can profound- geomorphic processes, fauna, and flora. ly affect rates of geomorphic processes. A. Define habitat, range. Effects through Geomorphic events may, in turn, set the flora. B. Define habitat. Determine dis- stage for succession by creating fresh sub- turbance potential by fire, wind. C. strates and may determine to some extent Affect soil movement by surface and mass the rate and type of plant community erosion. Affect fluvial processes by dam- development that follows a major ecosystem ming, trampling. D. Sedimentation pro- disturbance. cesses affect aquatic organisms. Effects The detailed character of geomorpho- through flora. E. Destroy vegetation. logy-ecosystem interactions vary from one Disrupt growth by tipping, splitting, ston- This landscape-ecosystem type to another. ing. Create new sites for establishment interaction is particularly dynamic in the and distinctive habitats. Transfer nutri- coniferous forest ecosystems of the steep ents. F. Regulate soil and sediment Cascade terrain, where vegetation is impor- transfer and storage. tant in regulating soil and sediment move- ment down slopes and streams. Historically, these forests and landscapes experienced morphology benefit from biological informa- widespread wildfire, floods, landslides, tion derived by methods such as dendrochron- and windstorms, which caused profound ology that have been exploited to only a fluctuations in sedimentation. Today, the limited extent. Fields of ecology center major process of stand and landscape dis- on relations between fauna and flora, in- turbance is clearcut logging and associated cluding herbivore, habitat structuring, and road construction and slash disposal. the like. Ecologists have a long tradition Over the course of CFB and subsequent of using information on the physical envi- research projects, earth scientists and ronment to interpret biological factors, biologists in our group have developed a but there are still many instances where common focus on questions at the inter- ecological understanding would be enhanced mediate time scale of system behavior such by improved appreciation for the role of as ecosystem response to disturbances like physical factors in ecosystems. logging, wildfire, and geomorphic events. Linkages among geomorphic processes, The overriding concern is to understand how landforms, fauna, and flora are manifold. nature has "managed" forests, streams, and Figure 1 shows interactions of major impor- landscapes on a variety of time scales to tance in forest and stream ecosystems in set a basis for evaluating and directing geomorphically active landscapes. Many of man's management programs. the following examples of these interactions have emerged as a result of interdiscipli- nary ecosystem research. We begin with GEOMORPHIC-BIOTIC INTERACTIONS landform effects on flora and fauna, then move to flora and fauna interactions with Interactions between physical and bio- geomorphic processes, ending with regulation logical realms of ecosystems offer many un- of geomorphic processes by vegetation, the explored but interesting and fruitful latter probably having greatest signifi- research topics that tend to fall between cance to land managers. disciplines (Fig. 1). Much of geomorpho- logy concerns the long-term effects of geo- morphic processes in sculpting landforms Effects of Landforms on Flora and the ways that landforms determine spa- tial distribution of geomorphic processes On the time scale of secondary suc- in the short term. Many studies in geo- cession and related major disturbances of vegetation, landforns are relatively F. J. SWANSON 163

invariant templates on which mosaics of Frequency and intensity of fire at a vegetation develop. Actual patterns of vege- site is also regulated by landforms in tation types and age classes over landscapes several ways (Swanson, in press). In many are determined by the interplay of landforms landscapes and storm types, topography in- and flora. Effects of landforms on vegeta- fluences geographic distribution of lightn- tion development at a site are generally ing strikes. Once ignition has occurred, mediated by microclimatic, edaphic, and type and rate of fire spread are determined hydrologic factors. Elevation slope, and by fuel conditions, wind, and topography aspect, for example, are elements of land- (Brown and Davis, 1973). Faster, more in- form whose main effects on vegetation are tense burning occurs on steeper slopes in through microclimate. Slope steepness, the response to convective winds and preheating product of long-term landform development, of fuels uphill of a fire front. Steep, influences erosion potential of soil and sunny slopes have dryer fuels than flatter soil texture and nutrient capital. Narrower slopes or slopes of other aspect. The role ridge tops and steeper slopes generally of topography in channeling winds also experience greater soil turnover and nutrient affects the geographic patterns of fire depletion by physical processes than more regime. gentle topography. These effects can often Landforms also influence fire pattern be recognized in chlorotic condition of by creating natural firebreaks. Completely young conifer stands on these physiograph forested but sharp ridges may be effective sites. Both slope steepness and soil tex- firebreaks where upslope mountain winds pre- ture determine drainage characteristics of vent fire from moving down lee slopes. a soil. Lakes, streams, talus fields, snow ava- Soil properties are profoundly influ- lanche, and landslide tracks form more con- enced by geologic factors, mainly bedrock spicuous firebreaks. Effectiveness of type, and geomorphic factors that control these landscape elements as firebreaks de- accumulation, redistribution, and mixing of pends on fire intensity and direction of soil. In the Pacific Northwest, volcanic fire spread relative to the "grain" of ash falling from the sky is an important, topography (Swanson, in press). Landforms widespread type of soil parent material that are more effective as firebreaks during can blanket diverse landscapes from distant lower intensity fires burning perpendicular sources. More typical depositional soils to drainage pattern or other potential fire- (alluvial, colluvial, and aeolian) commonly breaks. form the deepest, most fertile soils. The net effects of landforms on soil Landforms also influence vegetation by formation, geomorphic processes, vegetation affecting the potential for disturbance of disturbance regime, and light, water, and vegetation at a site. This vegetation- nutrient availability at a site result in physical process-landform set of relation- systematic variation in vegetation with ships is obvious where recurrences of the respect to topographic position, slope, and physical process have shaped the landform aspect. These effects are most pronounced as well as the vegetation community. An in steep terrain where topographic shading example is the role played by floodwater in and ridgetop to channel soil moisture inundation and sediment deposition, which gradients are important. Resulting vegeta- form floodplain features and associated tion patterns include more mesic communi- vegetation patterns. Both the magnitude of ties along streams, more xeric types on flood impact on channel form and time for ridges, and greater extent of mesic types recovery of channel form depend strongly on on slopes facing away from the afternoon the character of streamside vegetation sun. Hack and Goodlett (1960) interpret (Wolman and Gerson, 1978). this pattern at a site in the central Landforms play a more subtle role in Appalachians principally in terms of varia- determining vegetation conditions where the tion in soil water-holding capability as vegetation disturbance mechanisms are wind determined by soil texture and soil-forming and fire rather than geomorphic processes. geomorphic processes. A similar vegetation Slope position and valley configuration are pattern in the Cascade Range of Oregon has important variables affecting windthrow been interpreted more in terms of micro- potential of a site (Ruth and Yoder, 1953). climate and topographic shading (Hawk, Topograjihy can channel and funnel winds and 1979) create intense turbulence on the lee side of ridges. Since windthrow potential is a function of tree size and shape and stand Effects of Landforms on Fauna structure, topography and wind may conspire at some sites to repeatedly blow down Landforms affect fauna by determining stands as they reach a certain stage of the geographic distribution of habitats and development. by forming special habitats. The major 164 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS influence of landform on fauna is a result Effects of Fauna on Geomorphic of landform effects on vegetation patterns, Processes since vegetation structure and distribution determine habitat and range for most forest- Animal activities increase the rate of dwelling animals. Many examples come to geomorphic processes by directly moving mind, especially with respect to migratory soil or by altering soil properties, hydro- large mammals whose annual ranges cover logy, or vegetation with the result of diverse vegetation types. Distribution of accelerating subsequent erosion at a site. this vegetation, associated snow conditions, Soil that is moved by burrowing animals and other habitat factors are commonly ranging in size from to small strongly influenced by landforms. Flood- mammals can be a significant component of plains and valley bottom vegetation, for soil creep (Carson and Kirlcby, 1972). Ex- example, provide winter range, connectors cavation of burrows usually involves down- between diverse terrestrial habitat types, slope soil movement, as does subsequent and corridors for migration (Thomas et al., burrow collapse and erosion of bare soil on 1979). Vegetation analysis of the type done burrow mounds (Imeson, 1976; Imeson and by Whittaker (1956) in the Smokies and else- Kwaad, 1976). Charles Darwin (1881) ob- where illustrate strongly the multiple served in detail downslope movement of effects of landform on community pattern. castings during dry, rainy, and In a more special sense, distinctive windy periods and attempted to quantify the landforms provide special habitat oppor- role of earthworms in overall landscape tunities, termed "geomorphic habitats" by denudation. Few studies since have care- Maser and others (in press). Caves, talus, fully documented rates of soil movement by and cliff faces may be utilized by animals animals, but qualitative observations are of a great variety of sizes and habits de- common. Evidence of downslope soil move- pending on size, stability, and accessibility ment by large mammals, particularly elk, is of nesting, denning, perching, and other conspicuous where population densities are types of sites (Maser et al., 1979). In the high. Grazing livestock accelerates ero- Basin and Range physiographic province sion especially where stock concentrate in cliffs and associated talus slopes formed streams and riparian zones, trampling banks along rivet canyons, glaciated valley walls, and stirring up sediment. Fluvial geomor- and fault scarps support rich fauna in phic processes are also affected by dam terrain with little other large-scale construction, harvest of riparian vegeta- habitat density. The character of these tion, and bank burrowing by beaver. geomorphic habitats is determined in part Many impacts of animals on geomorphic by rock type, overall topography, and mode processes are the result of indirect effects of origin. Type of bedrock influences the of altered vegetation, soil properties, and size of talus blocks shed from a cliff and hydrology. Reduced litter due to shape and size of cavities in cliffs. and increased compaction as a result of Cliff height, shape, and aspect affect trampling can cause accelerated surface localized wind currents and utilization by erosion, but these effects are not likely birds, particularly raptors (Craighead and to occur in forest ecosystems where grazing Craighead, 1969). Canyon walls cut by intensities are low. Other subtle effects rivers provide less talus and more cliff of animal activity may occur. Pierson types of habitats, because the river carries (1977) suggested that mountain beaver away many of the talus blocks. Proportion (pdontia ruf a) burrows in areas of the of talus to cliff habitat is higher on Oregon Coast Ranges may pipe water rapidly fault scarps and walls of U-shaped glaciated into mass movement prone areas, thereby valleys where talus accumulates for long increasing the potential for soil mantle periods of time. failure. Kelsey (1978) and others have These examples of rather obvious in- discussed the possibility that introduction fluences of landforms on flora and fauna with livestock of short-rooted, annual suggest an infinite complex of more subtle grasses to prairies and oak savanna, earth- physical-biological interactions running f low areas of northwestern California may through all large-scale natural ecosystems. have led to accelerated earthf low movement At successional and higher frequency time since the late 1880's. They hypothesize scales most landforms can be viewed as the that earthf low activity was less when stage or template on which geomorphic- native deep-rooted, perennial species pro- biologic process interactions occur. vided greater evapotranspiration and root strength. Although these examples are of a very anecdotal nature, collectively they indi- cate that effects of fauna on geomorphic F. J. SWANSON165

processes are probably significant in many a surprisingly snail, short-lived impact on forest ecosystems. aquatic organisms (Hoopes, 1974). Organisms survive major floods by finding protected sites in gravel, behind logs, amongst roots Effects of Geomorphic Processes on and flooded vegetation, and in the lower Fauna portions of low gradient tributary streams. Many insects have life cycles with terres- Most effects of geomorphic processes trial phases during periods of high poten- on fauna occur indirectly as a result of tial for major flooding. Streams are influences of geomorphic processes on flora rapidly recolonized following a major flood and landforms, discussed in other sections. by organisms from these terrestrial and Direct effects in terrestrial environments aquatic refugia. are minimized in part by the mobility of Thus, the mobility of animals is a animals. In stream ecosystems, on the cause of weaker linkage between geomorphic other hand, sedimentation processes can have processes and fauna than between geomorphic immediate and direct impacts on aquatic processes and flora, the latter being very organisms. Microenvironments within a important. stream reach are shaped by the interplay of hydraulic processes, sediment characteris- tics, organic debris, and bedrock. Result- Effects of Geomorphic Processes ing channel geometry at the scales of on Flora gravel fabric, pool-riffle sequences, and downstream decreases in gradient provide a Geomorphic processes affect vegetation great variety of microhabitats. The many in all stages of development. In the con- species and functional groups (Cummins, text of succession on bare mineral soil, 1974) of aquatic organism are precisely geomorphic processes may initially "filter" distributed over this physically defined the species of plants established on a array of microhabitats (1-lynes, 1970). site. Surface erosion processes may move Stream water velocity, for example, is seeds of some species off the site, while a critical factor in determining distribution species with other seed characteristics or of organisms (Hynes, 1970). Leaf and needle reproductive strategies may become esta- processing organisms such as caddis flies blished. Established seedlings may be reside in the relatively quiet water of lifted out of the soil by frost heaving and eddies behind boulders and logs and in pools growth of needle ice. Geomorphic processes where organic detritus collects. Many col- disrupt growth of established trees by lector organisms (Cummins, 1974) build their tipping, splitting, and moving soil and tiny nets on stable substrates like large stones against them. Disrupted growth of pieces of wood or in interstices between trees that form regular annual rings com- rocks where the current carries sufficient monly provides excellent records of geo- organic detritus to support the organisms, morphic activity at a site (e.g., Potter, but does not flow at such high velocity that 1969; Schroder, 1978; Carrara, 1979). it destroys the nets. These disturbances to individual plants Increased sediment availability, alter overall stand composition and struc- transport, and deposition causes a variety ture. On an earthflow in a coniferous for- of disruptions of aquatic organisms in est (Swanson and Swanston, 1977), for these habitats. A thin film of clay and example, areas of open ground cracks mdi- silt-sized sediment deposited over organic cative of differential ground movement have detritus can render this food and case- complex stands with numerous holes in the building material unusable by clogging canopy where many of the heavily leaning mouths and gills of shredder organisms. trees have been blown down. Opening of the The nets of organisms collecting fine canopy has resulted in extensive develop- organic detritus from the water column may ment of understory vegetation and a multi- become filled with inorganic sediment. layered forest. Adjacent stands not subject Accumulation of fine sediment in intersti- to recent earth movement have complete, tial areas of spawning sites restricts flow single-level canopies and no significant of oxygenated water to eggs and decreases understory due to heavy shading. the opportunity for alevins to move through Geomorphic processes such as stream- the gravel to open stream water once they bank cutting and landslides completely re- have hatched. move vegetation, but in the process create Extremely high streamflow events can fresh sites for establishment of new plant reshape stream channels and change the dis- communities. Less destructive events such tribution of aquatic microhabitats. Major as overbank deposition of fine sediment abrupt geomorphic disruptions commonly have may suppress herbs for a period of time, 166 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS but also allow establishment of species a few years or less. Such studies run the which root on disturbed bare mineral soil. risk of failing to account for episodic Geomorphic disturbances can selectively events with return periods of many years, affect specific components of a plant com- but which accomplish in a few or munity like other disturbance processes days the results of many "average" years such as fire and harvest. (Swanson et al., in press). Debris ava- At the whole ecosystem level physical lanches and windthrow are two potentially processes have important roles in nutrient dominant processes that are readily over- cycling regimes. This is most clearly recog- looked in short-term studies. nized in the case of stream eocsystems where the biota resides in flowing water--the principal sediment transport medium. The Effects of Flora on Geomorphic analogous transience and mobility of the Processes physical environment of terrestrial eco- systems are not so easily recognized be- Vegetation regulates the movement and cause soil movement is accomplished by a temporary storage of soil and sediment on mix of slow and episodic processes. But on hillslopes and in small to intermediate- a broad time perspective and in steep sized streams. To appreciate the importance terrain the soil mantle and its accompany- and variety of vegetation effects it is use- ing are moving in- ful to first describe a soil/sediment rout- exorably downslope. Consequently, nutrient ing system typical of forested mountainous capital of a site reflects the long-term terrain (Fig. 2). This model is simplified balance of nutrient input and output pro- from systems defined by Dietrich and Dunne cesses. Physical transport of nutrients in (1978) and Swanson and others (in press). steep terrain is an important factor in Soil moves down hillslopes by a variety nutrient cycling and may limit accumulation of mass movement and surface erosion pro- of nutrients in an ecosystem (Sollins et cesses. Once in the channel, this material, al., in press). now termed sediment, is moved downstream by The importance of geomorphic processes another set of transfer processes. A single as nutrient transfer vectors needs further particle of material moves through a water- consideration in analysis and comparison of shed from one temporary storage site to nutrient cycling regimes of diverse eco- another in a series of steps by different systems. Nutrient cycling studies typically transfer processes, and it may move by assess storage sites and transfers for only several processes simultaneously.

HILLSLOPE CHANNEL

SLUMP EARTHFLOW COLLUVIUM MOVEMENT DEPOSITS AVA I LABLE TO CHANNEL PROCESSES BE D LOAD OUTSIDE OF SURFACE LAIN EROSION TRANSPORT HOLLOWS

TO DOWNSTREAM REACHES

ALLUVIAL OWSO SUSPENDED ATHERI HOLL TRANSPORT FAN

ROOT DEBRIS IN-CHANNEL BEDROCK THROW AVALANCHE TORRENT STORAGE

Figure 2. A model of soil and sediment movement through steep, forested watersheds. Transfer processes are circled. Storage areas are denoted by rectangles. F. J. SWANSON 167

The soil mantle, for example, has As a result of these and other effects several components subject to different of vegetation on geomorphic processes, sedi- sets of processes. All the soil surface is ment yield from snail steep watersheds susceptible to surface erosion processes, typically increases dramatically, but tem- and the entire soil mantle moves by the porarily, following severe disturbance of subtle group of processes termed "creep," vegetation by processes such as wildfire and including rheological soil deformation and clearcutting. Accelerated sedimentation root throw. Portions of a landscape sub- commonly results more from increased avail- ject to slump and earthflow movement also ability of sediment for transport than from experience creep and surface erosion. increased availability of water to transport These processes move soil directly to sediment. Clearcut logging, for example, streams, where it may reside temporarily in can trigger increased sediment yield by deposits of coiluvium until it is eroded (1) input of soil and organic detritus to during high streamflow events. Surface channels during timber felling, bucking, and erosion, root throw, and creep also move yarding operations, (2) release of sediment soil into "hollows," linear depressions in stored in channels by removing large organic the bedrock surface oriented downslope debris that trapped sediment prior to log- (Dietrich and Dunne, 1978). Periodically ging, and (3) reduction of ground cover, during conditions of extremely high soil nutrient uptake, evapotranspiration, and moisture, soil stored in hollows fails and root strength, all of which accelerate soil moves rapidly downslope as debris avalanches. erosion following logging. Debris avalanches that enter small steep Erosion rates from disturbed sites re- channels may maintain their momentum and cover to pre-disturbance levels partly continue to move rapidly downstream, pick- as a result of revegetation and re-establish- ing up alluvium, colluvium, and organic ment of the various controls of vegetation material along the way. on geomorphic processes. Because each ero- Bedload and suspended sediment trans- sion process is regulated by a different port processes move particulate matter set of vegetation factors, recovery rates through channels. Sediment is stored in differ from process to process (Swanson et floodplains, alluvial fans, and a variety al., in press). On many sites, for example, of in-channel sites, including point bars invading herbs and residual vegetation and deposits associated with large organic rapidly reduce nutrient losses in solution, debris, such as logjams. Storage behind but redevelopment of a substantial network large organic debris is most important in of woody roots may take a decade or more. headwater channels, whereas floodplain and Consequently, erosion, sediment yield, non-debris-related storage sites are pro- and soil/sediment routing in steep forest gressively more significant in larger land must be viewed in terms of succession channels (Swanson and Lienkaemper, 1978). and stand history, since the relative Forest vegetation strongly influences importance and absolute rates of geomorphic nearly all elements of the soil/sediment processes vary significantly on this time routing system on slopes and in small scale. In evaluating the geomorphic streams (Swanson et al., in press). Organic effects of man's activities in forest eco- litter protects the soil surface by dissi- systems, it is essential to contrast the pating the energy of throughfall and rain- frequency and erosion consequences of major drops and increasing the infiltration rate, vegetation disturbances in natural and thus decreasing the potential for overland managed systems. flow. Evapotranspiration functions of vegetation reduce soil moisture which may significantly affect seasonal rates of SUMMARY AND CONCLUSIONS creep and slump-earthflow movement (Gray, 1970). At many sites root throw associated Geomorphic factors, both processes and with blowdown of trees is the major mechan- landforms, play important active and ism of soil movement. Roots increase soil passive roles in forest ecosystems. Many strength, thereby decreasing the potential influences of geomorphic processes and for shallow rapid soil mass movements landforms on vegetation are mediated by (Swanston, 1969, 1970; O'Loughlin, 1974). physical, nutritional, and hydrologic Root systems contribute up to 40% of soil properties of soils. Landforms principally shear strength in some key landslide-prone determine the geographic distributions of areas (Dietrich and Dunne, 1978). Removal fauna and flora. Landform effects on of material in solution in ground and terrestrial fauna are mainly the result of stream waters is regulated in part by rate landform-fiora interactions. Geomorphic of nutrient uptake by vegetation (Likens et processes and flora interact strongly in al., 1977). Sediment storage capacity of steep terrain and along streams and rivers. small channels is greatly influenced by the presence of large organic debris. 168 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Live and dead vegetation regulates rates of Drury, W. H., and I. C. T. Nisbet. 1971. geomorphic processes, which, in turn, Inter-relations between developmental destroy vegetation, create new opportunities models in geomorphology, plant ecology, for establishment, and influence the and animal ecology. In Yearbook, Soc. development of plant communities. Gen. Syst. Res., edited by L. von En considering the evolution of con- Bertalannfy and A. Rapoport, pp. 57-68. cepts of ecosystem development, a major contribution of geomorphology has been to Gilbert, G. K. 1880 (2nd ed.) Report on provide time limits and temporal perspec- the geology of the Henry Mountains, tives on ecosystem change. Clearly, forest U.S. Dept. Interior, Geographical and ecosystem development on many time scales Geological Survey of the Rocky Moun- involves the interplay of physical and bio- tain Region. Washington, D.C.: U.S. logical factors, particularly in mountainous Govt. Printing Office. regions. The physical sciences should be well represented in any major ecosystem Gleason, H. A. 1926. The individualistic study. concept of the plant association. Bull. Torrey Bot. Club 53:7-26.

LITERATURE CITED Gray, D. H. 1970. Effects of forest clear- cutting on the stability of natural Braun, E. L. 1950. Deciduous Forests of slopes. Bull. Assoc. Eng. Geol. 7: Eastern North America. Philadelphia, 45-66. Pa.: Blackiston. Hack, J. T., and J. C. Goodlett. 1960. Brown, A. A., and K. P. Davis. 1973. For- Geoinorphology and forest ecology of a est Fire Control and Use, 2nd ed. mountain region in the central New York: McGraw-Hill Co. Appalachians. U.S. Geol. Surv. Prof. Paper 347. Carrara, P. E. 1979. The determination of snow avalanche frequency through tree- Hawk, C. M. 1979. Vegetation mapping and ring analysis and historical records community description of a small at Ophir, Colorado. Geol. Soc. Amer. western Cascade watershed. Northwest Bull., Pt. 1, 90:773-780. Sci. 53:200-212.

Carson, M. A., and M. J. Kirkby. 1972. Hoopes, L. 1974. Flooding as a result of Hillsope Form and Process. London: hurricane Agnes and its effect on a Cmabridge University Press. macroinvertebrate community in an infertile headwater stream in central Clements, F. E. 1936. Nature and structure Pennsylvania. Limnol. Oceanogr. 19: of the climax. J. Ecol. 24:252-284. 853-857.

Craighead, J. J., and F. C. Craighead. Hynes, H. B. N. 1970. The Ecology of Run- 1969. Hawks, Owls, and Wildlife. ning Waters. Ontario: University of New York: Dover Publ., Inc. Toronto Press.

Cuinmins, K. W. 1974. Structure and func- Imeson, A. C. 1976. Some effects of bur- tion of stream ecosystems. BioScience rowing animals on slope processes in 24:631-641. the Luxemborg Ardennes, Part 1: The excavation of animal mounds in experi- Darwin, Charles. 1881. The formation of mental plots. Geografiska Ann. vegetable mould through the action of 58A: 115-125. with observations on their habits, reprint (1945). London: meson, A. C., and F. J. P. M. Kwaad. 1976. Faber and Faber, Ltd. Some effects of burrowing animals on slope processes in the Luxembourg Dietrich, W. E., and T. Dunne. 1978. Sed:t- Ardennes, Part 2: The erosion of ment budget for a small catchment in animal mounds by splash under forest. mountainous terrain. Zeit. für Geomor- Geografiska Ann. 58A:3l7-328. phol. Suppl. Bd. 29:191-206. F. 3. SWANSON 169

Kelsey, H. M. 1978. Earthflows in Schroder, J. F. 1978. Dendrogeomorphologi- Franciscan melange, Van Duzen River cal analysis of mass movement on Table basin, California. Geology 6:361-364 Cliffs Plateau, Utah. Quat. Res. 9: 168-185. Likens, G. E., F. H. Bormann, R. S. Pierce, J. S. Eaton, and N. M. Johnson. 1977. Simon, H. A. 1973. The organization of Biogeochemistry of a Forested Eco- complex systems. In Hierarchy Theory, system. New York: Springer-Verlag. edited by H. D. Pattee, pp. 3-27. New York: George Braziller. Maser, C., J. M. Geist, D. M. Concannon, R. Anderson, and B. Lovell. Geomor- Sollins, P., C. C. Crier, F. M. McCorison, phic and edaphic habitats in managed K. Cromack, Jr., R. Fogel, and R. L. rangelands--their importance to wild- Fredriksen. The internal element life. In Wildlife Habitats in Managed cycles of an old-growth Douglas-fir Rancelands--The Great Basin of South- stand in western Oregon. Ecol. Monogr. eastern Oregon, edited by J. W. Thomas (in press). and C. Maser. USDA Forest Service (in press). Swanson, F. J. Fire and geomorphic pro- cesses. In Fire Regime and Ecosystem Maser, C., J. E. Rodick, and J. W. Thomas Properties, edited by H. A. Mooney, 1979. Cliffs, talus, and caves. In T. M. Bonnicksen, N. L. Christensen, Wildlife Habitats in Managed Forests J. E. Lotan, and W. A. Reiners. the Blue Mountains of Oregon and USDA Forest Service Gen. Tech. Rep. Washington, edited by J. W. Thomas, (in press). pp. 96-103. USDA Handbook 533. Swanson, F. J., R. L. Fredriksen, and F. M. Monk, C. D., D. A. Crossley, Jr., R. L. McCorison. Material transfer in a Todd, W. T. Swank, J. B. Waide, and western Oregon forest ecosystem. In J. R. Webster. 1977. An overview of The Natural Behavior and Response to nutrient cycling research at Coweeta Stress of Western Coniferous Forests, Hydrologic Laboratory. In Watershed edited by R. L. Edmonds. Stroudsburg, Research in Eastern North America, Pa.: Dowden, Hutchinson, and Ross, edited by D. L. Correll, pp. 35-50. Inc. Washington, D. C.: Smithsonian Institu- tion. Swanson, F. J., and C. W. Lienkaemper. 1978. Physical consequences of large O'Loughlin, C. L. 1974. A study of tree organic debris in Pacific Northwest root strength deterioration following streams. USDA Forest Service Gem. clearfelling. Can. J. Forest Res. Tech. Rep. PNW-69. 4:107-113. Swanson, F. J., and D. N. Swanston. 1977. Pierson, T. C. 1977. Factors containing Complex mass-movement terrains in the debris flow initiation on forested western Cascade Range, Oregon. Geol. hillslopes in the Oregon Coast Range. Soc. Amer. Rev. Engineering Geol., Ph.D. thesis, University of Washington, Vol. 3, pp. 113-124. Seattle. Swanston, D. N. 1969. Mass wasting in Potter, N., Jr. 1969. Tree-ring dating of coastal Alaska. USDA Forest Service snow avalanche tracks and the geomor- Res. Paper PNW-83. Pacific Northwest phic activity of avalanches, northern Forest and Range Expt. Sta., Portland, Absaroka Mountains, Wyoming. In United Oregon. States Contributions to Quaternary Research, edited by S. A. Schumm and Swanston, D. N. 1970. Mechanics of debris W. C. Bradley, pp. 141-165. Geol. avalanching in shallow till soils of Soc. Amer. Spec. Paper 123. southeast Alaska. USDA Forest Service Res. Paper PNW-103. Pacific Northwest Ruth, R. H., and R. A. Yoder. 1953. Re- Forest and Range Expt. Sta., Portland, ducing wind damage in the forests of Oregon. the Oregon Coast Range. USDA Forest Service Paper No. 7. Pacific North- Thomas, J. W., C. Maser, and J. E. Rodick. west Forest and Range Expt. Sta., 1979. Riparian zones. In Wildlife Portland, Oregon. Habitats in Managed Forests--the Blue Mountains of Oregon and Washington, edited by J. W. Thomas, pp. 40-47. USDA Handbook 533. 170FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Triska, F. J., J. R. Sedell, and S. V. Gregory. Coniferous forest streams. In The Natural Behavior and Response to Stress of Western Coniferous For- ests, edited by R. L. Edmonds. Stroudsburg, Pa.: Dowden, Hutchinson, and Ross, Inc. (in press).

Whittaker, R. H. 1956. Vegetation of the Great Smoky Mountains. Ecol. Monogr. 26:1-80.

Wolman, M. G., and R. Gerson. 1978. Rela- tive scales of time and effectiveness of climate in watershed geomorphology. Earth Surface Processes 3:189-208. The Role of Wood Debris in Forests and Streams

Frank J. Triska and Kermit Cromack, Jr.

In the Pacific Northwest, old-growth WOOD BIOMASS AND ACCUMULATION forests and their associated streams con- tain large quantities of coarse wood debris. As we have indicated, debris accumula- To date, such debris has been considered an tion must be considered over a period of impediment to reforestation and stream about 500 years. Accumulation over such a quality. Consequently, it has been virtu- cycle of secondary succession--from a nearly ally ignored in ecological studies, partly bare forest floor to the debris beneath a because man's need for wood fiber has re- 450-year-old stand of Douglas-fir--is sulted in the removal of debris from for- depicted in Figure 1. The diagram, which ests throughout the world but also because is a composite of data from three sites on the extended period necessary for wood to the H. J. Andrews Forest near Eugene, decay makes it difficult to study nutrient Oregon, is not intended to represent any recycling from such a process. In this particular site. It does, however, reflect paper, we shall attempt to correct that the fact that accumulations of debris are omission by exploring how wood debris is greater in the Pacific Northwest than else- utilized in forest and stream ecosystems. where because of the larger biomass of the Such an exploration is timely in view region's tree boles (Grier and Logan, of the diminishing amount of pristine for- 1977). In most cases, natural catastrophes est. In the Pacific Northwest, the greatest would result in greater accumulations than accumulation of wood debris occurs from depicted here (Franklin and Waring, 1980), natural mortality and blowdown in such for- but those that would result from clearcut- ests. Now that forests are being cut every ring followed by yarding and burningare 80 years instead of standing 250 to 500 adequately portrayed. years (the interval between natural cata- In Figure 1, event 1 represents an in- stropic fires), it is crucial that we crease in wood debris as a result of natural determine the role of wood debris in pris- thinning following canopy closure. The in- tine habitats and then incorporate that crease in wood biomass is slight because knowledge into existing management strate- such debris is finely divided and readily gies for our forests and watersheds. susceptible to decomposition. Event 2 rep- Our exploration will begin with deter- resents a long period of accumulation as mining the amounts of wood debris in various low branches are shed and thecanopy in- forest and stream ecosystems and its rates creases in height. Event 3 represents a of accumulation in each. We shall then decrease in wood debris because ofa litter examine how debris modifies existing brush fire. If trees were killed by such habitats and creates new ones. Next, we a fire, however, the accumulation of woody shall determine how rapidly coarse wood debris would increase. debris breaks down into its component ele- Event 4 represents windthrow in a large ments and how its carbon and other elements old-growth stand. Event 5 represents the are recycled. Finally, we shall discuss accumulation of large individual treeson what implications these data have for the the forest floor over an extended period. managers of forested watersheds in the Toward the end of succession, evena single Pacific Northwest. tree can introduce a large amount of organic matter. For example, the biomass of a tree 100 cm in d.b.h. equals 10 metric tons.

171 172FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

As the foregoing sequence implies, This distribution results because the deep wood carbon entering the detritus pooi of incisions in the basin cause trees to roll both the forest and its stream varies in downhill toward the stream. decomposition rate according to stand age Quantities ranging from 55 to 580 and history. For example, woody debris in metric tons per hectare represent a large young stands is finely divided and highly pool of organic carbon. We now know that susceptible to microbial attack, whereas an such pools of refractory (decomposition- equal amount of large woody debris with its resistant) carbon and other elements pro- low surface-to-volume ratio may have a de- vide a nutrient source throughout secondary composition period of hundreds of years. succession of ecosystems (O'Neill et al., Furthermore, the wood component in litter- 1975). Estimated wood debris in old fall is less than 10 percent in young stands Douglas-fir forests (Grier and Logan, 1977; but 70 percent in old-growth forests MacMillan et al., 1977; Waring and Franklin, (Grier and Logan, 1977). 1980) represents a larger aboveground pool Few estimates exist of the quantity of of organic matter than the entire above- wood debris in forests and their watershed ground biomass of most current eastern streams. One site where data are available deciduous forests (Day and Monk, 1974; from both ecosystems is Watershed 10, a Sollins and Anderson, 1971). 450-year-old stand of Douglas-fir in the Although large wood debris (>10 cm in H. J. Andrews Forest. Biomass estimates of diameter) is more visible, fine wood debris downed logs were made for the forested also represents a substantial input and de- watershed by Grier and Logan (1977) and for composes more rapidly both in streams and the watershed streams by Froehlich et al. on land. Fine wood debris in Watershed 10 (1972). Log debris for the forest was constituted only 13 percent of the biomass estimated at 55 to 580 metric tons per in the streams but decomposed faster, on hectare, whereas that for the stream the average, than coarse wood debris. The channel was estimated at 298 metric tons various litter inputs into the forest floor per hectare. Plotting of these data on a and streams of Watershed 10 are shown in map of standing and downed vegetation on Table 1. Watershed 10 indicates a general decrease in Tables 2 and 3 indicate the biomass of wood debris from stream channel to ridgetop. wood debris in streams and on the forest

240

0

0, /NO/V/OC/AL LOG fNPUT- WS 10 C 200 0 0

160

(I) 4-W/NO STORM 2I- o 120 4

LU > 80 : RS 9 3-GROUND F/RE I-4 -J Ui :2-BRANCH /NPUT £t 40

:1-TREE )H/NNf/VG 100 200 300 400 450 YEARS

Figure 1. Accumulation of wood debris during the life of a hypothetical stand of Douglas-fir. The solid line indicates the overall increase of wood debris over time; included as reference points are data from the Thompson Site (TS), Washington Reference Stand 19 (RS 19), and Watershed 10 (WS 10), all on the H. J. Andrews Forest near Eugene, Oregon. The dotted line depicts major events (discussed by number in text) that affect debris accumulation. F. J. TRISKA & K. CROMACK, JR.173

floor of various old- arid young-growth for- been dendrochronological, prfmarily the es Ls. By far the largest amount of wood interpretation of tree scars (MacMillan debris occurs in Streams draining old-growth et al., 1977; Swanson ot al., 1976) or the redwoods and Douglas-fir/western hemlock. assessment of dated successional sequences Even second-growth Douglas-fir/hemlock has such as fir waves (Sprugel, 197b) in balsam more wood in its streams than do some old- fir forests (Lambert et al., in press). growth sites in other parts of the country, Permanent plots set aside for studies of partly because of the carryover of wood tree growth and mortality afford another debris from the primeval forests. In old- method of dating wood debris. While falling, growth forests in the Great Smoky Mountains trees may scrape against adjacent trees, re- of Tennessee, both spruce/fir and mixed sulting in the removal of bark and the de- hardwood stands have large quantities of composition of callus tissue in annual in- wood debris in their streams. crements in the surviving trees. These in- Comparison of old- and second-growth crements or shock rings permit dating of the forest types indicates that even in primeval events (Shigo and Marx, 1977). Unfortunate- forests, the amount of wood debris in the ly, only a few trees leave such records of streams varied with species composition and their deaths. environmental conditions. Regardless of Dating the accumulation of large debris these two factors, however, the quantity of is especially difficult in third-order or such wood was probably much greater in larger streams. In first- and second-order many primeval forests than can be observed streams, wood remains essentially where it today. It follows that the biota of for- falls. In the larger streams, however, it ested ecosystems and streams draining them tends to be clumped by high water prior to evolved in a system where wood debris play- decomposition, making it especially diffi- ed a far larger role than it does today. cult to date the accumulations or to esti- Thus, wood debris has been removed in many mate decomposition rates or nutrient re- parts of the world before man has fully cycling. One can conclude that wood debris understood its role. tends to exert a greater impact, in terms One of the major difficulties in of amount, on the stream than on the sur- assessing the input rate of wood debris is rounding forest and that this impact the episodic mature of its accumulation. gradually diminishes as one proceeds down- To date, the most successful methods have S t ream.

Table 1. Leaves and coarse and fine wood debris entering the forest floor and watershed stream at Watershed 10, H. J. Andrews Forest, prior to clearcutting1

Leaf litter Wood debris Method of measurement Deciduous Coniferous Fine Coarse

g/m2 /day

Litterfall 0.070 0.346 0.244 --

Lateral movement .096 .143 .728 --

Scaling 0.548

Total .166 .489 .972 .548

Percent composition 7.6 22.5 44.7 25.2

'Unpublished data from F. J. Triska, Dept. of Fisheriesand Wildlife, Oregon State Univ., 1978. 174FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

MODIFYING AI'TD CREATING channel as intact boles after catastrophes NEW HABITATS such as windthrow and localized earth move- ments or after bankcutting or erosion. On both land and in water, wood serves More highly decomposed wood may enter the as more than a large pooi of refractory forest floor or stream as snags. carbon. Its very presence in large quanti- To differentiate various states of ties modifies habitats on the forest floor wood decay and their effects on habitat, we and in streams and creates new ones. have devised a classification system based As habitat, wood debris represents an on the findings of previous researchers alteration in the physical structure of the (Table 4). The system is based on physical forest, changing the nature of light re- characteristics such as texture, shape, flection to the canopy and providing new color, the presence or absence of bark or types of habitat on the forest floor. Be- twigs, and propotion of the bole in contact cause wood accumulates irregularly, many with the ground. Trees alive when they fell different states of decay are present at a to the forest floor or stream would usually particular time. In natural stands, logs be grouped in decay class 1, while snags may be added to the forest floor and stream would probably be in decay class 2 or 3.

Table 2. Estimated wood debris on the forest floor of selected old-growth and young-growth temperate forests.

Location Forest type and age (years) Logs1 Branches2

metrictons/hectare

Oregon3 Douglas-fir > 450 218

New York4 Spruce/birch > 300 42 -

New Jersey5 Mixed oak > 250 21.3 2.1

New Hampshire6 Mixed hardwoods > 170 34

New Hampshire7 Subalpine balsam fir 80 71 33

North Carolina8 Mixed oak/hickory > 60 11.8 .7

Great Britain9 Mixed oak - 2.0

10 Denmark Mixed oak 5

Poland11 Mixed spruce/basswood 200-400 22 -

1Logs assumedto include coarse woody debris > 7.5 cm in diameter. 2Branches assumedto range from 2 to 7.5 cm in diameter. 3NacMillanet al. (1977). 4McFee and Stone (1966). 5Lang and Forman (1978). 6Bormann and Likens (1979). 7Lambertet al. (in press); peak log biomass (> 8 cm in diameter) occurs at stand age 33 years. 8Cromack (1973). 9swiftet al.(1976). 10 Christensen (1977). 11Falinski (1978);assumes a density of 0.35 for 63 m3 of logs. F. U. TRISK4 & K. CROMACK, JR. 175

The role of large wood debris as habi- small animals (Maser et al. ,1978) and to tat depends on its decay class (F1g. 2). capture soil and organic debris, which Fof example, cover ond nesting sites for slows erosion and maximizes nutrient reten- terrestrial vertebrates depead on seen fac- ti an. tors as shape, texture, and presence of Physical distribution is also impor- branches and twigs. Elton (1966), Winn tant. Generally, the more even the overall (1976), and Maser et al.(1979) outlined distribution, the greater the habitat di- some of the important features of coarse versity and utilization (Winn, 1976; Maser wood debris and noted how habitat role Ct al., in press). Large blowdowns may shifts with decay class. provide excellent cover and concealment for Other factors which affect the role of smaller animals such as porcupines (Taylor, wood as habitat for wildlife include size 1935) while interfering with the passage of and orientation. Obviously, large logs larger wildlife such as deer (Lyon, 1976) provide greater cover for small vertebrates and wild boar (Falinski, 1978). On the than do small ones (Ruben, 1976; Maser et other hand, large areas devoid of wood al., 1979). Large logs are also more per- debris lead to reduction or elimination of sistent features of the environment because those species dependent on it for some they decompose slowly as a result of a low stage of their life cycle. surface-to-volume ratio (MacMillan et al., In addition to serving as animal habi- 1977). The orientation which logs take tat, downed wood debris also serves an also influences their capacity to serve as important function for the plant community. habitat. Logs oriented along a contour As log debris decomposes, its internal are most likely to serve as runways for moisture and nitrogen concentration in-

Table 3. Estimated coarse wood debris in first- and second-order streams draining old- and young-growth temperate forests.

1 Lo cat ion Forest category Wood

2 OLD-GROWTh kg/rn

Oregon2 Douglas-fir/hemlock 25-40 Idaho2 Spruce/lodgepole pine .2 7 New Hampshire Spruce/fir 4 Tennessee3 Spruce/fir 10

Tennessee3 Mixed hardwoods 13

Southeastern Alaska4 Spruce/hemlock 5 .4 California Redwoods 45-80

YOUNG-GROWTH

Michigan5 Mixed hardwoods 4-8

Oregon5 Douglas-fir/hemlock 20-2 5

1> 10 cm in diameter 2Unpublished data from J.R. Sedell and F. J. Swanson, Dept. of Fisheries and Wildlife and Dept. of Forest Engineering, Oregon State Univ., 1978. 3Unpublished data from S. V. Gregory,Dept. of Fisheries and Wildlife, Oregon State Univ., 1978. 4Unpublished data of F. J. Swansonand C. W. Lienkemper, Dept. of Forest Engineering, Oregon State Univ., 1978. 5Unpublished data of J. R. Sedell,Dept. of Fisheries and Wildlife, Oregon State Univ., 1977. 176 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Table 4. Decay classes of Douglas-fir, after Fogel et a1. (1973), MacMillan et al. (1977), and Maser et al. (1979).

Class

Characteristic 1 2 3 4 5

Bark Intact Intact Sloughing Detached or Detached or absent absent

Structural Sound Sound Heartwood Heartwood None integrity sound, rotten, does supports not support own weight own weight, branch stubs pull out

Twigs < 3 cm Present Absent Absent Absent Absent

Texture of Intact Mostly intact, Hard, large Soft, small Soft, rotten portions sapwood pieces blocky powdery partly soft pieces when dry

Color of wood Original Original Reddish Reddish or Red-brown to (except in color color brown or light brown dark brown portions with original white rot) color

Invading roots Absent Absent Sapwood only Throughout Throughout

Vegetation None None Conifer Tsuga < 15 cm Tsugup to surviving seedlings DBH; smaller 200 cm DBH: shrubs, moss shrubs, some large; moss

Fungal fruiting Fungal Cyathus, Polyporus, Cortlnarius, Cortinarius, colonization, Tremella, Polyporel- Mycena, Collybia, few large Mycena, lus, Pseudo- Marasmius Cantharellus fruiting Collybia, hydnum, bodies Polyporus, Fomitopsis Fomitopsis, Ps eudohydnum

Mycorrhizae1 Absent Absent Mycorrhizal Boletus, Boletus, colonization Corticium, Corticium, Hydnotria, Hydnotria, Lacaria, Lacaria, Piloderma, Piloderma, Rhizopogon Rhizopogon

1J. M. Trappe, USDA Forest Service, Pacific Northwest Forest and Range Experiment Station, Corvallis, Oregon, 1979. F. J. TRISKA & K. CROMACK, JR. 177

crease (Place, 1950; Rowe, 1955). In the burned logs on a clearcut in western Pacific Northwest, decomposing logs even- Washington. accumulation tually serve as nursery sites for hemlock, In watershed streams, the of coarse wood debris also modifiesthe the climax species in moist Douglas-fir specialized habitat (Franklin and Dyrness, 1973). stream channel and provides The anount and rela- Thus, by serving as plant habitat, downed habitat (Figs. 3-5). tive role of wood increases dramatically as logs influence forest succession (Jones, For example, in the 1945; Rowe, 1955). one proceeds upstream. Besides providing habitat, wood debris first-order stream called Devil's Club Creek on the H. J. Andrews Forest (Table5), also modifies the forest floor. If cover- wood completely inundates the channel. In age of the forest floor is extensive, a fact, at summer low-flow there is more large area may be taken out of production water in the decaying wood tissuethan is for extended periods. If wood is in con- free-flowing in the stream channel. Under tact with the ground, some physical and these circumstances, wood plays a strong biological properties of the soil beneath role in directing water flow and sediment may be modified significantly. Ausmus (1977) reported that soil under logs in a storage. In the smallest streams, wood debris is deciduous forest increased 4-fold in organic especially valuable in creating habitat, matter, 8-fold in adenosine triphosphate or where, because of high streambed gradients, ATP (which is a measure of microbial bio- Small, steep mass), 18-fold in nematode density, more it might not otherwise exist. watershed streams have extensive areas of than 2-fold in root biomass, and 5-fold in bedrock except where sediment is entrained In the Pacific calcium concentration. At these sites, Northwest, preliminary data by K. Cromack, by wood debris (Figs. 4-5). small riffles and pools are formed behind Jr., and D. H. McNabb (Dept. of Forest debris, thus facilitating the establishment Science, Oregon State Univ., 1978, personal of a biological community. Because small communication) indicate that Ceanothus streams do not have enough hydrologic force velutinus undergoes a significant increase to remove debris, wood-created habitat in in nodulation (for fixation of nitrogen) in these streams is most often formed by indivi- soil under old logs. B. Bormann (Dept. of dual pieces of debris or minor accumulations. Forest Science, Oregon State Univ., 1979, The biological community in these small personal communication) has reported that modulation of red alder occurred beneath

SNAG: NESTING SITES INSECT HABITAT INSECTIVOROUS BIRDS LIMITED BY DECAY CLASS A SIZE

LOGS ALONG CONTOUR - PROVIDE BETTER -. FEEDING AND LOOKOUT MAMMAL RUNWAYS SITES FOR SMALL MAMMALS THAN 00 THOSE ACRO CON TOU INSECT HABITAT BENEATH BARK BIRD PERCHING ROOT WADS SERVE SITES AS PERCHING I DUSTING AND NESTING SITES

- SUITABILITY A / HIGHLY DECOMPOSED ( WOOD USED BY SQUIRRELS NURSERY SITE FOR WOOD STORAGE AND DEPENDS ON BY DEERMICE FOR DECAY CLASS ITTERACCUM CONSTRU TING BURROWS UPSLOPE SIDE, IN PHYSICAL ELEVATED LOGS WITH LITTLE DECAY PROVIDE MORE COVER AND CON- CONCEALMENT THAN HIGHLY DECAYED LOGS - © FUNGAL FRUITING BODIES SERVEAS FOOD RESOURCE TO BOTH SMALLAND CR COVER LARGE MAALS

LIMITS BASED ON SIZE CLASS

Figure 2. Role of coarse wood debris as habitat on the forest floor. Habitat role is dependent on decay class, size, amount, and orientation of debris. Circled numbers indicate decay classes. 178FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS streams, although not tremendously produc- of organic particulates. Retention is tive, is effective at processing particulates particularly important for litter process- and even at altering certain nutrient con- ing because microbial colonization is a centrations of the water before it reaches a prerequisite to invertebrate consumption of second-order stream (S. Gregory, Dept. of wood arid other litter (Triska, 1970; Fisheries and Wildlife, Oregon State Univ., Anderson and Grafius, 1975). 1978, personal communication). Although most extensive in first-order First-order streams in old-growth for- streams, wood-created habitat is most ests are thus effective ecosystems because visible in third- to fifth-order streams. of the retentiveness of wood-created habitat. In these larger streams, heavy discharges Time gained by slowing and directing water exert enough hydrologic force to clump flow and by increasing biologically debris. These clumps entrain large amounts and chemically active surfaces facilitates of organic matter and sediment, which form chemical exchange with organic and mineral areas of rich biological habitat. In surfaces, as well as promoting microbial streams larger than fifth-order, coarse colonization and invertebrate consumption

2 2

THIRD-ORDER HRST-ORDE\ STREAM STREAM HIGH RETENTION HIGH RETENTION, WOOD- CONTROL tED WOOD-CONTROLLED LOCALIZED HABITAT

Figure 3. Role of wood in the various watershed streams of a drainage network. Note that the azw3unt of wood-created habitat decreases as one proceeds downstream. Circled numbers indicate stream order. F. J. TRISKA & K. CROMACK, JR. 179

FORESTED STREAM HABITATS

)12 ORDER) (3-4 ORDER) VERY SMALL STREAMS SMALL INTERMEDIATE STREAMS N S REDOC S S ZE S /,pJ :\

COLLECTORS PREDATORS

SPR(ODERS

TORS

4ç3R \\GOERSJ

MINERAL SUBSTRATE EDftOCo, BOULDERS. COBBLES, GRAOEL.ETC I

HABITAT CREATED BY WOOD DEBRIS

WOOD HABITAT

Figure 4. Formation of wood-created habitat and its influence on the invertebrate community of first- through fourth-order streams. Life functions of various invertebrate groups based on Curtanins (1974) and Anderson et al. (1978). Size of segments in each chart based on proportional role of indicated functional group.

Table 5. Estimates of coarse and fine wood debris from selected streams of increasing watershed area within and adjacent to the H. J. Andrews Forest.

Coarse Fine Stream Watershed wood wood Stream order area Gradient debris' debris

km2 percent kg/rn2------

Devil's Club Creek 1 0.05 35 40.89 1.11

Mack Creek 3 5.35 20 28.50 0.61

Lookout Creek 5 60.20 12 11.65 .08

McKenzie River 7 1,642.00 9 .07 .08

1> 10 cm in diameter. 180 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS wood debris is found along banks or deposit- density was higher in the stretch draining ed in the riparian zone and thus plays a the old-growth area, where litter had been minor role in habitat formation. retained among pieces of coarse wood debris. Although the smallest streams have the There were 15 times more larvae behind the most extensive wood-created habitat, they debris dam, however, because the coarse also have the lowest invertebrate biomass. wood had captured large amounts of litter, Anderson et al. (1978) describe 38 taxa of thus facilitating microbial conditioning invertebrates, mostly insects, associated and expanding the amount of available with wood in Oregon streams. However, only habitat. Thus, wood debris sometimes plays a few of these insect species are truly an important role completely unrelated to xylophagous (wood-consuming): Lara anova its own utilization as an energy or nutrient (gouging), Heteroplectron californicum source. (boring), and Lipsothrix spp. (tunneling). The effect of coarse wood debris on For the others, wood serves an incidental fish habitat (Fig. 5) has been summarized by role--for example, as an attachment site Hall and Baker (1977) and Baker (1979). for feeding or pupation; for oviposition; Overall, wood debris seems to have a direct as a nursery area for early instars; or influence on the size of fish populations for nesting, molting, or emergence (Fig. 5). but only an indirect influence on their These incidental associations can have metabolisms. Actual habitat value of debris a direct influence on the structure of the dams is dependent on such factors as the stream's invertebrate community, as evi- stability of the structure and the diversity denced by Grafius's (1977) population esti- of habitat created behind it. The most mates for the leaf-consuming caddis, important function of wood debris is to pro- Lepidostoma unicolor, in various aquatic vide cover and protection from predation. habitats. L. unicolor consumes Douglas-fir For underyearling salmon and trout, debris needles after they have been conditioned by provides not only cover but also protected microbial colonization (Sedell et al., rearing areas (Hartman, 1965; Coulter, 1975). To test the suitability of various 1966; Sheridan, 1969; Meehan, 1974), parti- habitats, Grafius determined larval densi- cularly during overwintering (Hartman, 1965; ties of Lepidostoma in three stretches of a Bustard and Narver, 1975). Adult salmon often inhabit pools formed by coarse wood clearcut, one draining an area of old- debris (James, 1956; Larkin et al., 1959; growth Douglas-fir, and one behind a debris Sheridan, 1969). At two sites in the dam (Fig. 6). In the clearcut stretch, Oregon Coast Range, Baker (1979) found that Lipidostoma larvae were scarce because of fish biomass was significantly higher be- the absence of suitable litter. Larval hind debris dams than either upstream or downstream.

REARING AND HIDING AREAS FOR UNDER-YEARLING SALMON AND OVERWINTER PROTECTION FOR NATIVE TROUT SJRFACZ'(II) EMERGENCE

ANADROMOUS REST AREAS PUPATION SITE - 'S. ---

SURFACE GOUGING GRAZING OVIPOSITION /

BORING

SHREDNG -

COVER

SEDIMENT CAPTURE

FILTERING OF FINE FOOD ORGANISM FINE PARTICILATE ORGANIC MATTER SEDIMENTS ENHANCES HABITAT QUALITY OF DOWNSTREAM SPAWNING AREAS

Figure 5. Role of coarse wood debris as habitat in a watershed stream.Habitat role is dependent on decay class, size, amount, and orientation of debris. F. J. TRISKA & K. CROMACK, JR.181

Accumulations of coarse wood debris cellulolytic and lignin-decomposing fungi also function as filtering devices (Hail are aerobic, decomposition of aojor struc- and Baker, 1975). Bishop and Shapley (n.d.) tural tissue is retarded. found that the amount of fine sediments Because decomposidon of mod in was significantly reduced and oxygen con- streams begins on the periphery, physical centration was increased in gravel areas processes such as scouring play a more downstream from such accumulations. As important role than on land. Decomposition pointed out previously, this filtration can from the outside inward is also evident in increase the production of fish food the action of invertebrates within water- organisms. logged debris. Of the 38 insect taxa reported by Anderson et al. (1978) in such debris, only two were tunneling as opposed WOOD DECOMPOSITION AND to surface species. Of these, only Lipso- NUTRIENT CYCLING thrix spp. were present in substantial numbers, which were described as occurring As mentioned at the outset, decomposi- "in tunnels in decayed alder wood that was tion of coarse wood debris requires several so soft it could be broken apart by hand." hundred years. This persistence of debris Unlike the decay process in streams, is related to its size, shape, and nutrient wood decay on land can occur both from the composition (Fogel and Cromack, 1977; outside inward and from the center to the MacMillan et al., 1977; Lambert et al., in press). Because of the extended periods involved, investigators have devised broad

F I I classifications for wood decay, such as the I one outlined previously in Table 4. A 1400- OPTIMAL HABITAT major problem with such schemes, however, is that a single log can contain wood in various stages of decay. This condition 200- often arises because of (1) greater soil contact at one end than the other, (2) z 1000- partial decomposition prior to contact with 0 the forest floor, (3) distinct decay zones Cr) related to plant, animal, and microbial E activity, (4) waterlogging of debris in the 800- stream channel, and (5) significantly dif- ferent diameters at the base and the tip. w CLEARCUT By later stages of log decomposition, wood 2600- OOLO GROWTH texture is so soft that increased stream- DESRIS DAM flow will disintegrate the softest portions and sweep them downstream as fine particles. 400- - On land, logs with advanced decay can exist for more than 500 years (MacMillan et al., 1977). 200- The process of water logging is depict- ed in Figure 7, which represents 50 years

of decomposition in a single log whose cJ length spans three distinct habitats-- 300- SLJITA8LE HABITAT streams, riparian, and terrestrial. This ujm 200 log exhibits five stages of decay resulting >1 from the varying environmental factors to I0- which it has been subjected. zo In streams, the decay of intact logs APR MAY JUNE JULY AUG seems to occur primarily from the periphery of the log toward the interior, and the MONTH process is slower than on land. In small streams, for example, logs do not always Figure 6. Density of Lepidostoma unicolor have permanent contact with the water. If this contact occurs only during the rainy larvae in three stretches of Mack Creek seasons or when the stream is at its high- one stretch draining a clearcut, one drain- est, decay is likely to be retarded. And ing an old-growth area, and one behinda even when the log is submerged or has con- debris darn--within the H. J. Andrews Forest. tinuous contact with the water, waterlogging Upper graph depicts larval density along a prevents oxygen diffusion deep within the 10-rn span, whereas the lower graph depicts woody tissue. Consequently, because most larval density per square meter of suitable habitat. (From Grafius, 1977). 182 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS outside. On land, moisture content of de- tion and aeration as their roots penetrate composing coarse debris increases with age the decomposing wood. (Fig. 8), but logs rarely achieve the water- As log decay advances, there is a pro- logged, spongy state observed in the final gressive increase in the concentration of stages of decomposition in water. The essential nutrients such as nitrogen and greater moisture content in wood debris on phosphorus (Fig. 8). This is due primarily land in fact facilitates decomposition by to the fact that carbon is mineralized at preventing drying out during the warm, a greater rate than most other essential droughty summers characteristic of the elements during initial stages of decay. Pacific Northwest. Thus, the terrestrial The net result is that other essential ele- log acts as a perched water table, en- ments are conserved for recycling within couraging not only decomposition but also the forest ecosystem. invasions by burrowing mammals and tunnel- As log decay advances, there is a pro- ing invertebrates. Common invertebrates gressive decrease in wood density. In a such as , carpenter ants, and wood- study on the H. J. Andrews Forest (MacMillan boring beetles are well known for their et al., 1977), Douglas-fir logs were esti- ability to operate within the wood matrix mated to lose about 75 percent of their (Elton, 1966). This activity in turn density after about 220 years. As such logs further enhances aeration. become less dense, their habitat value for Because wood on the forest floor re- tunneling invertebrates and small mammals mains permanently in place with ever- increases. Unfortunately, similar estimates increasing soil contact as time progresses, are not available for logs in stream mycorrhizal associations sometimes act as channels. sources of nutrients to promote wood decay. Although large debris is the most Harvey et al. (1976) demonstrated the visible wood component on land and in importance of decaying logs as sites for streams, fine wood contributes substantially colonization by ectomycorrhizal fungi. to energy flows and nutrient cycling Such fungal activity promotes carbon miner- throughout the course of secondary succes- alization and the immobilization and fixa- sion. Average decomposition periods for tion of nitrogen (Larsen et al., 1978; fine wood are faster than those for coarse Silvester, 1978), thereby decreasing the debris (Fogel and Cromack, 1977; MacMillan carbon/nitrogen ratio of decomposing tissues et al., 1977; Grier, 1978; Sollins et al., and providing sources of nutrients and in press). The large nutrient pool provided water for the establishment of nursery hem- by fine wood is intermediate in availability locks on decaying logs. These colonizing between those of leaf litter and coarse seedlings in turn lead to further fraginenta- wood debris.

', 'I

CLASS CLASS CLASS /OTAL SOIL 0 \\,,/\\// ç)1/ D CONTACT ROOT WAD BARK LARGELY BARK SMALL INTACT BREAKING HEMLOCK 1/ UP COLONIZATION - (O3n' HIGH

'0 c., -CERTER, INTACT MAJOR SOIL 8-20n,0AMP CONTACT FIRST 5eC,WATERLOGGED

BOULDER BOULDER CONTACT CONTACT CHAN MAJOR SOIL CONTACT BASE FLOW ONTERMITTENT) WATER LINE

LTREAM CHANNELRIPARIAN ZONE HILL SLOPE I

Figure 7. Decomposition over a 50-year period in a single log whose length spans three habitats. Note that five decay classes are represented within the log. F. J. TRISKJ\ & K. CROMACK, JR. 83

Branches and twigs also play an impor- source of carbon and other nutrients varies tant role in providing habitat and a food not only be debris size but also by debris source, particularly in aquatic environ- species. Tunneling invertebrates which use ments. Anderson et al. (1978) report that rotten wood as a nutrient source prefer the majority of invertebrate organisms they intermediate-sized debris (1 to 10 cm in collected frm seven streams in Oregon were diamter) of deciduous species. When wood found on woo.. 1 to 10 cm in diameter. Be- is intermediate in size, waterlogging in cause most of the aquatic invertebrates on streams apparently does not cause an acute wood are associated with surfaces, it is diffusion problem, as it does in large reasonable that they would be associated debris. with debris providing a large surface-to- Little is known about how wood of volume ratio as well as ample Sites for small to intermediate size is decomposed in attachment. the terrestrial environment. Accordingly, The role of wood as habitat and as a this process is being studied at Mack Creek and on the forest floor of the H. J. Andrews Forest. Five types of fine wood rue substrates of Douglas-fir have been placed both on the forest floor and in the stream. Data analyzed to date indicate that fine 500 wood debris decomposes faster in the aquatic than in the terrestrial environment (Fig. 9). The largest difference between decom- 500 position in the two habitats was observed in chips, which have the largest surface- a' E to-volume ratio. The next greatest differ- 00 ence was in twigs, which are sapwood and LiJ therefore the second most decomposable sub- strate. Bark and heartwood sticks, which one would expect to be the least susceptible 500 to microbial breakdown, exhibited the smallest differences between decomposition on land and in water and also the lowest 100 incidence of decay. As noted previously, in large wood debris decomposition is accompanied by an 3 increase in nitrogen concentration. The 3.0 0 30 same process was observed in the fine wood substrates (Fig. 10). As with weight loss, the greatest increase in nitrogen concen- 2.5 0.25 tration and the largest difference between reactions in the terrestrial and aquatic environments were observed in the least - 20 020 refractory substrates--chips and twigs. AR Because the data analyzed to date cover a' E only 220 days, long-term trends, or even seasonal trends related to temperature, are Is 015 not yet known. a' One of the major obstacles to the de- composition of wood debris is its extremely I07 0 0 a- high carbon/nitrogen ratio (322 for twigs, 357 for bark, 1,175 for heartwood chips, and 1,382 for heartwood blocks of Douglas- 0.5 005 fir). Nitrogen fixation could play an important role in the early stages of de- composition by initially decreasing the

0 I carbon/nitrogen ratio. Therefore, acetylene 0 50 100 50 200 reduction, as a chemical assay of nitrogen GE (years) fixation (McNabb and Geist, 1979), was studied in the five substrates to determine Figure 8. Water, nitrogen, and phosphorus if fixation contributes to the observed in- contents in relation to age of wood debris crease in nitrogen concentration. Acetylene at a raid-elevation stand of Douglas-fir in reduction was observed at some time in all the H. J. Andrews Forest. (From MacMillan five substrates. As one might expect from et al., 1977). previous data, acetylene reduction was 184 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

WOOD SUBSTRATE INCUBATED INMACK CREEK WOOD SUBSTRATE INCUBATED IN MACK CREEK

0 w UJ z z

I.- H w w t:r:

F- I.-I I w w z z w w

30 39 228 334 458 565 30 139 228 334 458 565

DAYS IN PLACE DAYS IN PLACE

Figure 9. Weight loss in five fine wood substrates of Douglas-fir placed on the forest floor and in Mack Creek on the H. J. Andrews Forest. Each point is the mean of three samples - F.3. TRISK3 & K. CPOMCK, JR. a5

greateSt in the at ream in he east ref rae- tory samples--eli I pe and ta i ga--and lowest among samples on the forest floor (Fig. I I) Factors such as temperature and mois- ture arc important in influencing the nitro- gen fixation rate and the rates of di ffui-i on 0.2 of nitrogen and oxygen to nitrogen-fixing bacteria. A general relationship between temperature and nitrogen fixation rates has 0.1 been noted in the literature (Cromack et aT., 1979; Kallio et al., 1972; Paul, 1975). z C Acetylene reduction has also been detected in large log debris and in small-sized wood 0 (Cornaby and Waide, 1973; Sharp and Mill- 0.3 bank, 1973; Sharp, 1975; Roskoski, 1977; Larsen et al., 1978). Through nitrogen fixation, logs may not only serve as an - 02 II important source of habitat but may also z facilitate their own decomposition and per- uJ C) haps even contribute significant quantities z 0.1 io_10 of nitrogen to the forest floor. 0 () 0 z BARK MANAGEMENT IMPLICATIONS 0.3 MACK CREEK Wood debris functions as an integral component of forest ecosystems. Concerted 0 FORES7 FLOOR efforts to conserve wood debris will be needed if managed forests are to maintain the diversity of plant, animal, and micro- bial habitats currently present in un- managed, primeval forests. On forest land, woody debris (slash) should be maintained

C I I I over approximately 10 percent of clearcut 50 100 150 200 250 areas (Maser et al., 1979). It would be desirable to leave several logs of decay classes 1 and 2 per hectare; these could be DAYS culled from logs of less desirable timber quality. As many logs as possible of Figure 10. change in nitrogen concentration classes 3, 4 and 5 (which have little or no In in three fine wood substrates placed on the commercial value) should be retained. some instances, a portion of the woody forest floor and in Mack Creek on the H. J. Andrews Forest. debris could be utilized locally as fire- wood. Logs could be physically rearranged on the landscape to ensure optimal density and physical stability as part of the routine logging operations and site pre- paration (Maser et al., 1979). The removal of natural, stable woody debris from streams can damage both the stream channel and streamside riparian habitat. Consequently, such material should be left in place when possible. In cases where massive accumulations occur, either as a result of logging or catastrophic events such as debris avalanches, signifi- cant wood removal nay be necessary. In such cases, the advice of competent stream ecologists and geomorphologists should be sought before removal of massive debris jams are attempted. The general goal for wood management in streams should be to maintain well-established debris so that it can continue to function both as habitat and as a long-term nutrient source to stream organisms. 186 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

FOREST FLOOR TWIGS BLOCKS I 500 flBARK STICKS 000 9 CHIPS isis NOT SAMPL ED

_i-L_fl_ 13° 40 ' 6° U 5° I 6° ' 2°

4,000 47,000 7000 LU MACKCREEK

4500 " z 2 4000 I- 3500 O :-' LU 3000- :-

lU z 2500

> 2000- - I-

-. -- 0 500- -..

000 50 Ij DAYS IN PLACE: 30 139 228 334 458 508 565 699 DATE: 514/77 8/31/77 11/28/77 3/14/78 7117/78 9/6/78 11/1/78 3/14/79 450 40 TEMPERATURE (°C) 4° 11° 5,5° 2.50 20 00

Figure 11. Rates of acetylene reduction in five fine wood substrates placed on the forest floor and in Mack Creek on the H. J. Andrews Forest. F. J. TRISKA & K. CRO1ACK, JR.187

ACKNOWLEDGE1ENTS Custard, 0. R., and C. H. Narver. i975. Aspects of the winter ecology of We acknowledge National Science Founda- juvenile collo salmon (Oncorhynchus tion Ecosystems Grants No. DEB-76-2l402 and kisutch) and steelhead trout (Salmo DEB-77-06075 for support of our work. We girdneri). J. Fish. Res. Board Can. appreciate the help of the following people 32:667-680. from Oregon State University: for techni- cal assistance, J. Anders, B. Buckley, C. Christensen, 0. 1977. Estimation of Hawk, P. MacMillan, C. Mallonie, S. Phillip, standing crop and turnover of dead and L. Roberts; for the use of unpublished wood in a Danish oak forest. Olkos data, C. Baker, B. Buckley, T. Dudley, R. 28:177-186. Fogel, F. Grafius, G. Hawk, G. Lienkaemper, P. MacMillan, M. Ogawa, J. R. Sedell, F. Cornaby, B. W., and J. B. Waide. 1973. Swanson, and J. Trappe. Additional sug- Nitrogen fixation in decaying chestnut gestions and assistance in this work have logs. Plant and Soil 39:445-448. come from P. Sollins, Oregon State Univer- sity, and from J. Means and J. F. Franklin, Coulter, M. W. 1966. Ecology and manage- USDA Forest Service, Pacific Northwest ment of fisheries in Maine. Ph.D. Forest and Range Experiment Station. thesis, State Univ. College of For- estry at Syracuse, N.Y.

LITERATURE CITED Cromack, K., Jr. 1973. Litter production and decomposition in a mixed hardwood Anderson, N. H., and E. Grafius. 1975. watershed and a white pine watershed Utilization and processiisg of alloch- at Coweeta Hydrologic Station, North thonous materials by stream Trichop- Carolina. Ph.D. thesis, Univ. of tera. Verb. Internat. Ver. Limnol. Georgia, Athens. 19:3083-3088. Cromack, K., Jr., C. C. Delwiche, and D. H. Anderson, N. H., J. R. Sedell, L. M. McNabb. 1979. Prospects and problems Roberts, and F. J. Triska. 1978. of nitrogen management using symbiotic Role of aquatic invertebrates in pro- nitrogen fixers. In Symbiotic Nitro- cessing wood debris in coniferous f or- gen Fixation in the Management of est streams. Am. Midl. Natur. 100: Temperate Forests, edited by J. C. 64-82. Gordon, C. T. Wheeler, and D. A. Perry, pp. 210-223. Forest Res. Lab., Ausmus, B. 5. 1977. Regulation of wood Oregon State Univ., Corvallis. decomposition rates by arthropod and annelid populations. In Soil Organisms Cummins, K. W. 1974. Structure and func- as Components of Ecosystems, edited by tion of stream ecosystems. BioScience U. Lohm and T. Persson. Proc. 6th 24:631-641. Int. Colloq. Soil Zool., Ecol. Bull. (Stockholm) 25:180-192. Day, F. P., Jr., and C. D. Monk. 1974. Vegetation patterns on a southern Baker, C. 0. 1979. The impacts of logjam Appalachian watershed. Ecology 55: removal on fish populations and stream 1064-1074. habitat in western Oregon. M.S. thesis, Oregon State Univ., Corvallis. Elton, C. 5. 1966. The Pattern of Animat Communities. New York: John Wiley Bishop, D. M., and S. P. Shapley. n.d. and Sons, Inc. Effects of log debris jams on south- eastern Alaska salmon streams. Unpub- Falinski, J. B. 1978. Uprooted trees, lished report, Inst. of Northern For- their distribution and influence in estry, Pac. Northwest Forest and Range the primeval forest biotope. Vegetatio Experiment Sta., Juneau, Alaska. 38:175-183.

Bormann, F. H., and C. E. Likens. 1979. Fogel, R., and K. Cromack, Jr. 1977. Patterns and Processes in a Forested Effects of habitat and substrate Ecosystem. New York: Springer- quality on Douglas-fir litter decom- Verlag. position in western Oregon. Can. J. Bot. 55:1632-1640. 188 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Fogel, R., M. Ogawa, and J. M. Trappe. Jones, E. W. 1945. The structure and re- 1973. Terrestrial decomposition: a production of the virgin forests of New Phytol. synopsis. Conif. For. Biome Rep. 135. the north temperate zone. 44:130-148. Franklin, J. F., and C. T. Dyrness. 1973. Natural vegetation of Oregon and Kallio, P., 5. Suhonen, and H. Kallio. Washington. USDA Forest Service Pac. 1972. The ecology of nitrogen fixation Northwest Forest & Range Experiment in Nephroma arcticum and Solorina Stn. Gen. Tech. Rep. PNW-8. crocea. Rep. Kevo. Subarctic Res. Stn. 9:7-14. Franklin, J. F., and R. H. Waring. 1980. Distinctive features of the north- Lambert, R. L., G. E. Lang, and W. A. western coniferous forest: develop- Reiners. 1980. Weight loss and ment, structure and function. (In this chemical change in boles of a subalpine volume). balsam fir forest. Ecology (in press).

Froehlich, H. A., D. McGreer, and J. R. Lang, G. E., and R. T. Forman. 1978. Sedell. 1972. Natural debris within Detrital dynamics in a mature oak for- the stream environment. Univ. of est: Hutcheson Memorial Forest. Eco- Washington, USIBP Internal Rep. 96, logy 59:580-595. Conif. For. Biome. Larkin, P. A., and others. 1959. The Grafius, E. J. 1977. Bioenergetics and effects on freshwater fisheries of strategies of some Trichoptera in pro- man-made activities in British Colum- cessing and utilizing allochthonous bia. Can. Fish. Cult. 25:27-59. materials. Ph.D. thesis, Oregon State Univ., Corvallis. Larsen, M. J., M. F. Jurgensen, and A. E. Harvey. 1978. N2 fixation associated Grier, C. C. 1978. A Tsuga heterophylla- with wood decayed by some common fungi Picea sitchensis ecosystem of coastal in western Montana. Can. J. Forest Oregon: decomposition and nutrient Res. 8:341-345. balances of fallen logs. Can. J. Forest Res. 8:198-206. Lyon, L. J. 1976. Elk use as related to characteristics of clearcuts in Grier, C. C., and R. S. Logan. 1977. Old- western Montana. In Proceedings of the growth Pseudotsuga menziesii communi- Elk-logging-roads Symposium, edited by ties of a western Oregon watershed: S. R. Hieb, pp. 69-72. Univ. of biomass distribution and production Idaho, Moscow. budgets. Ecol. Monogr. 47:373-400. MacMillan, P. C., J. E. Means, G. M. Hawk, Hall, J. D., and C. 0. Baker. 1975. Bio- K. Cromack, Jr., and R. Fogel. 1977. logical impacts of organic debris in Douglas-fir log decomposition in an Pacific Northwest streams. In Logging old-growth Douglas-fir forest. North- Debris in Streams, Workshop II.Oregon west Sci. (abstr.), p. 13. State Univ., Corvallis. Maser, C. J. M. Trappe, and D. C. Ure. Hartman, C. F. 1965. The role of behavior 1978. Implications of small mammal in the ecology and interaction of mycophagy to the management of western underyearling coho salmon (Oncorhyn- coniferous forests. In Trans. 43rd chus kisutch) and steelhead trout North An. Wildi. and Nat. Resour. Conf. (Salmo gneri). J. Fish. Res. Wildlife Manage. Inst., pp. 78-88. Board Can. 22:1035-1081. Washington, D. C.

Harvey, A. E., M. J. Larsen, and M. F. Maser, C., R. G. Anderson, K. Cromack, Jr., Jurgensen. 1976. Distribution of J. T. Williams, and R. E. Martin. ectomycorrhizae in a mature Douglas- 1979. Dead and down woody material. fir/larch forest soil in western In Wildlife Habitats in Managed For- Montana. Forest Sd. 22:393-398. ests the Blue Mountains of Oreg and Washington, edited by J. W. Thomas, James, G. A. 1956. The physical effect of pp. 78-95. USDA Forest Serv. Agric. logging on salmon streams of southeast Handbook 553. Alaska. USDA Forest Service, Alaska For. Res. Cent. Stn. Pap. 5. F. J. TRISKA & K. CRON1ACK, JR. 189

McFee, U. U., and E. L. Stone. 1966. The Sharp, R.F. 1975. Nitrogen fixotion in persistence of decaying wood in the deteriorating wood: The incorporation layers of northern forests. of and the effect of environmental Proc. Soil Sci. Soc. Amer. 30:512-516 conditions on acetylene reduction. Soil Biochem. 7:9-14. McUabb, D. H., and J. M. Geist. 1979. Acetylene reduction assay of symbiotic Sharp, R. F., and J. U. Milibank. 1973. N2 fixation under field conditions. Nitrogen fixation in deteriorating Ecology 60:1070-1072. wood. Experientia 29:895-896.

Meehan, U. R. 1974. The forest ecosystem Sheridan, U. L. 1969. Effects of log of southeast Alaska. 3. Fish habitats debris Jams on salmon spawning riffles USDA Forest Serv. Pac. Northwest For- in Saginaw Creek. USDA Forest Service, est & Range Exp. Stn. Gen. Tech. Rep. Alaska Region. PNW-l5. Shigo, A. L., and H. G. Marx. 1977. Com- O'Neill, R. V., U. F. Harris, B. S. Ausmus, partmentalization of decay in trees. and D. E. Reichle. 1975. A theoreti- USDA Forest Service Agric. Inf. Bull. cal basis for ecosystem analysis with 405. particular reference to element cycl- ing. In Mineral Cycling in South- Silvester, W. B. 1978. Nitrogen fixation eastern Ecosystems, edited by F. G. and mineralization in Kauri (Agathis Howell, J. B. Gentry, and M. H. Smith, australis) forest in New Zealand. In pp. 28-40. ERDA Symp. Series (CONF- Microbial Ecology: Proceedings in Life 740513). Sciences, edited by M. W. Loutit and J. A.R. Miles, pp. 138-143. Berlin: Paul, E. A. 1975. Recent studies using Springer-Verlag. the acetylene reduction technique as an assay for field nitrogen fixation Sollins, P., and R. M. Anderson, eds. 1971. levels. In Nitrogp Fixation by Free- Dry weight and other data for trees living Micro-organisms, edited by and woody shrubs of the southeastern W. D. P. Stewart, pp. 259-269. New U.S. ORNL-IBP-71-6 Rep., Oak Ridge York: Cambridge University Press. Natl. Lab., Oak Ridge, Tenn.

Place, I. C. M. 1950. Comparative moisture Sollins, P., C. C. Grier, F. M. McCornison, regimes of humus and rotten wood. K. Cromack, Jr., R. Fogel, and R. L. Can. Dep. Resour. & Dev., Forestry Fredriksen. 1980. The internal ele- Branch, For. Res. Div., Silvicultural ment cycles of an old-growth Douglas- Leaflet 37. fir forest in western Oregon. Ecol. Monogr. (in press). Roskoski, J. 1977. Nitrogen fixation in northern hardwood forests. Ph.D. Sprugel, D. G. 1976. Dynamic structure of thesis, Yale Univ., New Haven, Conn. wave-generated Abies balsamea forests in the northeastern U.S. J. Ecol. Rowe, J. S. 1955. Factors influencing 64:889-912. white spruce reproduction in Manitoba and Saskatchewan. Can. Dept. of Swanson, F. J., G. U. Lienkaemper, and J. R. Northern Affairs and Nat. Resour., Sedell. 1976. History, physical Forestry Branch, For. Res. Div. Tech. effects and management implications of Note 3. large organic debris in western Oregon streams. USDA Forest Service Pac. Ruben, J. A. 1976. Reduced nocturnal heat Northwest Forest & Range Exp. Stn. loss associated with ground litter bur- Gem. Tech. Rep. PNW-56. rowing by the California red-sided garter snake, Thamnophis sirtalis in- Swift, M. J., I. N. Healey, J. K. Hibberd, fernalis. Herpetologica 32:323-325. J. M. Sykes, V. Bampoe, and M. E. Nesbitt. 1976. The decomposition of Sedell, J. R., F. J. Triska, and N. S. branch-wood in the canopy and floor of Triska. 1975. The processing of a mixed deciduous woodland. Oecologia conifer and hardwood leaves in two 16:139-149. coniferous forest streams. I. Weight loss in associated invertebrates. Verh. Internat. Ver. Limnol. 19:1617- 1627. 190 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

Taylor, W. P. 1935. Ecology and life history of the porcupine (Erethizon epixanthum) as related to the forests of Arizona and the southwestern U.S. Univ. of Arizona Biol. Sci. Bull. 3,6:5-177.

Triska, F. J. 1970. Seasonal distribution of aquatic hyphomycetes in relation to disappearance of leaf litter from a woodland stream. Ph.D. thesis, Univ. of Pittsburgh, Pa.

Waring, R. H. 1980. Vital signs of forest ecosystems. (In this volume).

Winn, D. S. 1976. Terrestrial fauna and selected coniferous forests habitat types on the north slope of the Unita Mts. USDA Forest Service Region 4, Wasatch Natl. Forest, Salt Lake City, Utah. The Multiple Linkages of Forests to Streams

Kenneth W. Cummins

INTRODUCTION 1963; Ross, 1963). A major development of the 1970's has been the measurement of Headwater stream ecosystems in forest- watershed material-balance budgets. Such ed watersheds are intimately related to studies have shown that streams are not their vegetative setting. The riparian merely conduits that export forest eco- zone, the source area of soil-forest pro- system products from within the boundaries ducts which enter the stream, contributes of surface watersheds and subsurface source to channel stability and generates bio- areas, but rather that they store and bio- logically active organic substrates. Large logically process organic inputs (Fisher woody debris often constitutes stable geo- and Likens, 1973; Sedell et al., 1974). morphic features which retain mineral sedi- Budgets for reaches, rather than for entire ment and finer organic material (Swanson watersheds, require that appropriate seg- and Lieukaemper, 1978; Swanson, Triska, ments be chosen for study with all inputs this volume). Inputs of organic solutions adequately taken into account (Fisher, and particulates (and inorganic nutrients) 1977). In all budget studies it is impor- provide energy for the stream community tant to measure storage carefully and to over an annual cycle (Fisher and Likens, relate release from (or accrual to) storage 1973). The stream also represents a to the annual inputs. Also, the losses to potential source area for the riparian zone and introduction from storage must be re- of the forest ecosystem at times of greater lated to the seasonal and long-term flow than bankfull discharge (Merritt and Law- regime (Swanson, this volume). son, 1979). Thus, because of the interactive nature of forest-stream ecosysteus, stream com- PERSPECTIVES munity structure and function should be studied within a watershed context (Cuinmins, The 1970's also have involved the 1974; Hynes, 1975). development of conceptual models of head- water stream ecosystem structure and func- tion (Cunmins, 1974; Minshall, 1978). Re- BACKGROUND finement of existing models and elaboration of new ones will undoubtedly continue to be Prior to the 1960's the primary a major feature of stream-watershed research emphasis in stream ecosystem investigations in the 1980's. Examples would be evaluating was on invertebrates as food organisms for and testing the "River Continuum" and game fish in specific stream reaches. In "Nutrient Spiraling" hypotheses. The former these studies a wide variety of methods was depicts stream-river drainage nets as con- employed to sample plants and animals tinua of biological organization that reflect associated with the channel sediments (see geomorphic control (Cummins, 1975; Vannote review by Cummins, 1962), but the key role et al., 1980) from low order headwater played by the watershed in supplying organic streams to higher order receiving rivers substrates utilized by stream organisms was (Strahler, 1957; Leopold et al., 1964). largely neglected. "Nutrient Spiraling" (Webster, 1975) refers The heterotrophic nature of forested, to the partially open nutrient cycles headwater stream ecosystems and their characteristic of running waters. Portions allochthonous-based energy source was f or- of the inputs to a given reach are stored mally recognized in the early 1960's (Hynes, and processed and some fraction released

191 192FORESTS: FRESH PERSPECTiVES FROM ECOSYSTEM ANALYSIS

by downstream. The incomplete efficiency of greater abundance of FPOM is reflected storage and processing provides energy and a change in community structure; for inorganic nutrients for downstream communi- example, larger populations of collectors ties. The more efficient reaches (i.e., (filter feeding invertebrates) (Wallace and higher retention and processing) are con- Merritt, 1980). sidered to have the "tightest" spirals.

Nutrient Recyling The River Continuum Present research on nutrient relation- A major distinction between lotic eco- ships--particulate and dissolved (DON, systems can be made on the basis of the < 0.5 pm) organic matter and inorganic relative importance of in-stream primary ions--viewed as partially closed cycles, production versus inputs of terrestrial points up the need for measurements of both origin as the major source of organic matter physical storage and biological processing. for community processes (Vannote et al., The use of radioactive tracers (Ball et al., 1980). In forested ecosystems, small, 1963; Ball and Hooper, 1963) or stable iso- shaded, cool headwater steams (approximately tope ratios--e.g., 13C/12C--(Rau, 1978) can orders 1-3) may derive more than 90 percent provide data for determining pathways and of their organic carbon from the terrestrial residence times of nutrients in stream eco- surroundings (Fisher and Likens, 1973; systems. Sedell et al., 1974). The riparian zone Storage pools or compartments can be vegetation functions both in light attenua- defined as locations where organic matter tion and as the source of allochthonous accumulates and is processed (utilized) at inputs, including long-term structural rates slower than the average or exposed (wood debris) and annual energy supplies. (oxygenated) sites in the channel. There The ratio of daily gross primary pro- are three general areas: the deep sedi- duction (P) to total daily community ments (low oxygen), the inner core of respiration (R)(Oduin, 1956) reflects the woody debris jams (low oxygen), and the relative dominance of autotrophy versus upper bank or floodplain (low moisture). heterotrophy. However, as Minshall (1978) When organic material buried in the sedi- has shown, even when primary production ments and within debris jams is excavated, exceeds upstream and riparian inputs of or that on the upper bank is captured, and organic matter, the in-stream derived re-enters the aerobic stream channel pro- organic substance is used primarily in a cessing regime, it is utilized at a faster moribund state in detrital food chains. rate (Cummins and Klug, 1979; Merritt and Where riparian vegetation has been removed, Lawson, 1979). Thus, the annual--and as in clearcut timber harvest, or is natu- longer--hydrographic pattern is critical in rally sparse (high altitudes and latitudes determining the proportion and timing of and xeric regions), autotrophy dominates processing and export of annual terrestrial (P/R > 1). In wide shallow, generally inputs warmer, well-lighted midsized rivers (orders Along with channel and upper bank 4-6), primary production is also the domin- storage or retention, biological processing ant source of organics. is the major control of quantities of In addition to increases in primary material introduced and their rates of re- production related to higher light regimes, cycling. The prediction from the "River another significant feature of the adjust- Continuum" hypothesis (Vannote et al., 1980) ment of biological communities to changes in is that spiraling would be tighter, espe- geomorphology, channel configuration, and cially for coarse particulate organic matter vegetational setting downriver (along the (CPOM, > 1 mm particulate size), in head- "continuum") concerns the size distribution water streams due to more efficient reten- of the particulate organic matter (POM, tion and processing. > 0.5 pm particle size) resources. Head- water streams characteristically have greater inputs of coarse material (CPOM, ORGANIC RESOURCES AND > 1 mm particle size) and, therefore, FUNCTIONAl GROUPS greater concentrations of the microbial and macrobial biota for which coarse mate- The quantities and qualities of organic rial is the primary nutritional resource resources exert a major influence on stream (Cummins, 1974). With increasing stream community structure (Cummins, 1974; Hynes, size and reduced importance of direct 1975; Minshall, 1978) which is expressed in riparian inputs, a larger proportion of the the functional roles of macroinvertebrate POM is fine particulate organic matter species. Different functional groups have (FPOM, < 1 mm particle size) transported adapted morphologically, behaviorally, and from the headwater drainage net. The Table 1. Categorization of organic resources in lotic ecosystems (modified from Cummins and Kiug, 1979) Resource particleApproximate Major carbonRatio ofto Macroinvertebratefunctional feeding Periphyton category size range In-streamSources nitrogen (C/N) group using resource Macrophytes (macrop(microproducers) roducers) >< 1500 cm >(some 10 pm macroalgae)< 1 cm > mm In-stream photosynthesis 13-70:15-10:1 Shredders,Scrapers scrapers Woody detritus > 10 cm (coarse) < 10 (fine)cm > 10 mm Riparian zone duringtributaries(upstream floods) 200-1,300:1 Shredders (gaugers) Nonwoody detritus matter(particulate or POM) organic > 0.5 pm Riparian zone, upstream 70-80:1; portion10-11:(microbial 1) FineCoarse (FPOM) (CPOM) <> 1 mm > 0.5 pm Upstream,Riparian zone riparian zone 20-80:17_40:11 CollectorsShredders Dissolved organic matter(DOM) < 0.5 pm Subsurface source riparianareas, upstream,zone < 17 lower)portion(labile None Animal tissue > 100 pm (microforms > 10 in) In-stream < 17 Predators significant portion of the nitrogen may be biologically very resistant. C-) (I-, 194 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

physiologically to utilize various compon- to those observed annually (Cummins et al., ents of the spectrum of available resources 1972; Manny and Wetzei, 1973). The rapid (Cummins, 1974. 1975; Merritt and Cummins, incorporation of the labile fraction of 1978; Cummins and Klug, 1979). DOM onto particles and into microbes con- stitutes the important retention character- istic of streams because of the reduced Organic Resources probability of export of particles as opposed to solutions. Of the remaining The basic categories of organic re- annual organic flux, about one-half is fine sources in running waters (Table 1) differ particulate organic matter (FPOM); the significantly in nutritional content as de- greatest percent of CPOM is found in head- fined by microbial and animal growth. In water streams, reflecting the close associ- addition to animal tissue used by predators, ation with the riparian zone. there are three general classes of organic Annual POM input, exclusive of large resources: (1) those with chlorophyll woody debris, to headwater forested streams (living micro- and macroproducers), (2) ranges from 300 to 800 g AFDW m2 (Anderson detritus, ranging in size from large wood to and Sedell, 1979). Although annual inputs particles less than 1 pm and all with may be low, headwater streams character- associated microorganisms, and (3) dissolved istically have large standing stocks of organics (which can be taken up by microbes). large wood (approximately > 2 cm): from If the ratio of carbon to nitrogen (C/N) is 1 to 2 k m2 in Michigan streams to 10 to used as an index of resource nutritive 15 kg m in western Oregon streams value, ratios of 17 or less are generally (Anderson et al., 1978; Swanson and Lien- considered in the high quality range kaemper, 1978). The coarse woody debris (Russell-Hunter, 1970). However, low undoubtedly plays a major role in retaining ratios may be misleading, as in the case of nonwoody POM inputs, resulting in mean some FPOM (Table 1), because the nitrogen annual standing stocks of approximately may be in a recalcitrant form (Ward and 200 to 500 e AFDW m2. Cummins, 1979). Fungi are relatively more important on CPOM where mycelia can develop, and bacteria Macroinvertebrate Functional are predominant on FPOM (Cunimins and Klug, Feeding Groups 1979). Because the microbial biomass associated with detritus is nutritionally Recognition of stream microinvertebrate superior (e.g., low C/N) to the organic functional groups (Fig. 1) has shown con- particle substrate which is high in cellu- siderable promise as a tool for assessing the ecological state of a running water lose and lignin, it exerts the major control on the rate of detritus processing. This is community (Cuimnins, 1974; Merritt and mediated both through direct microbial Cummins, 1978). The relative abundances of metabolism of the detrital substrate and the groups reflect environmental conditions, particularly the quantity and quality (i.e., regulation of invertebrate feeding (Peter- sen and Cummins, 1974). Substrates, such nutritional value) of particulate organic as different species of leaf litter, vary matter inputs and periphyton growth. in the rate at which microbial colonization Arduous and incomplete efforts at taxonomic and metabolism and, therefore, invertebrate description can be reduced or circumvented by concentrating on morphological-behavioral feeding proceed. Thus, differences in In addi- quality of inputs are realized as differ- adaptions for food acquisition. tion, because most species are , ences in stream community metabolism. The distribution of detrital size this method avoids the lack of resolution fractions in stream ecosystems is a func- associated with concentration on macroin- Thus, the ratios of tion of the vegetative and soil character- vertebrate diets. various functional groups reflect the nature istics of the riparian zone, hydrologic events, and biotic processing. Dissolved of the organic food resources available organic matter (DOM) generally accounts for (Cumniins and Klug, 1979; Wiggins and 50 percent or more of the total annual Mackay, 1979). There are five basic macroinvertebrate organic flux in forested headwater streams functional feeding groups. Figure 1 links (Fisher and Likens, 1973; Sedell et al., each group with a nutritional resource that 1974). A significant proportion of the DOM generated is quite labile, being physi- it is morphologically and behaviorally adapted to harvest and physiologically cally adsorbed and flocculated, and bio- The highest quality logically incorporated by microorganisms adapted to assimilate. nutritional resources are animal tissue, at rates approximately equal to its pro- nonfilamentous periphytic algae, and the duction. This is exemplified by similar measured daily changes in DOM as compared microbial biomass component of detritus (Table 1) (Anderson and Cummins, 1979). K. W. CUMMINS195

The CPOM: fungal-hacterial :shredder particles from the stream bottom sediments association (Fig. 1), is exemplified by (many species of midges). Although col- large invertebrates such as larvae of the lectors require the presence of microbial cranefly Tipula, which feed on conditioned biomass on ingested FPOM for adequate nutri- leaf litter. Conditioning involves rapid tion, they show less adaptation for selec- leaching of soluble organics followed by tive feeding (i.e., selection for highest colonization and growth of aquatic fungi food quality) than shredders (Cummins and and bacteria. After microbial populations KIug, 1979). The relationship of collectors have softened the substrate, shredders to the riparian zone is less direct because begin actively feeding on CPOM (Curnmins, a significant portion of the FPOM is gen- 1974; Cuminins and Klug, 1979). Shredders erated within the stream ecosystem (Fig. 1). selectively feed on the CPOM with the maxi- Therefore, the ratio of shredders to col- mum microbial biomass, and account for at lectors in a stream community reflects the least 30 percent of the total processing balance between CPOM and FPOM and the rela- (conversion of CPON to CO2. FPOM, and con- tive dominance of the riparian zone. sumer biomass)(Petersen and Cunimins, 1974). Macroinvertebrates of the periphyton: The shredder functional group represents scraper association have adaptations for the closest invertebrate linkage with the removing attached algae (primarily nonfila- riparian zone, with growth and survival mentous forms) from surfaces (Fig. 1). dependent upon the quantity and quality of Because they frequently feed in exposed the terrestrial inputs. sites, scrapers are also adapted morpho- The FPOM:bacterial:collector associa- behaviorally for maintaining position in tion (Fig. 1) includes macroinvertebrates the current; for example, the heavy mineral that feed by filtering particles from the cases of scraper caddisflies or the dorso- passing water, for example, with filtering ventral flattening of heptageniid mayf lies fans (blackflies) or silt nets (net-spin- that allows them to avoid the main force of ning caddisflies), and those that gather the flow. Abundance and growth of scrapers

CPOM LIGHT NUTRIENTS / /

STHESIS

MICROPRODUCERS -m:AN FPOM'KTECESS MACROPRODUCERS (FECES:'

> j >

SHREDDERS FILTERING & GATHERING COLLECTORS SCRAPERS-PIERCERS PREDATORS

Figure 1. Diagrammatic representation of majorresource inputs and partitioning among invertebrate functional groups in forested, headwaterstream ecosystems. The major inputs shown, CPOM, light, and nutrients (FPOM and DOM alsoenter from the riparian zone, not shown), are partitioned among five general processingsubsystems associated withmacro- invertebrate functional feedinggroups. These are the CPOM:fungal-bacterial:shredder; FPOM:bacterial :collector; algal :scraper; macrophyte:piercer;and predator:prey associations. Production of DOM from CPOM and pathways of FPOM generation are also shown. (Shredders-- amphipod, detrital stonefly, caddisfig, and cranefly; filtering collectors--biackfliesand net spinning caddis fly; gathering collectors--burrowingmayfly; scrapers--tortise-shell case caddisfly, limpet, heptageniid , waterpennybeetle larva; piercez-s--micro- caddisfi/es; predators--predaceous stonefly,sulpin.) 196 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEM ANALYSIS

is correlated with in-stream algalprimary ACKNOWLEDGMENTS production, for example, P/R ratio(Anderson Preparation of this paper was supported and Cummins, 1979). Ratios of shredders or collectors to scrapers are indicative of the by Contract DE-ATO6-79EV-10004 from the importance of CPOM or FPOM relative to pen- Division of Biomedical and Environmental phyton as nutritional resources. Research, U.S. Department of Energy. The piercer:macrophyte association Rosanna Mattingly and George Spengler are (Fig. 1) in streams is represented almost gratefully acknowledged for their aid in exclusively by microcaddisflies, which preparing the manuscript. Technical Paper utilize filamentous macroalgae by sucking No. 5341, Oregon Agricultural Experiment the fluids from individual cells. As pri- Station. mary producer communitiesin streams shift from diatoms to macrophytes, the ratio of piercers to scrapers increases. The LITERATURE CITED piercers are a unique group in that the major utilization of macrophytes in streams Anderson, N. H., J. R. Sedell, L. M. 1978. The is in detrital food chains (Minshall,1978). Roberts, and F. J. Triska. Predator:prey associations (Fig. 1) in role of aquatic invertebrates in pro- for- stream communities appear to be relatively cessing wood debris in coniferous Amer. Midl. Natur. constant and ubiquitous. Animal tissue est streams. represents the highest quality food re- 100:64-82. source (Anderson and Cummins, 1979),but 1979. the relatively low density of prey relative Anderson, N. H., and J. R. Sedell. to other nutritional resources means thac Detritus processing by macroinverte- Ann. Rev. predators are required to expend more brates in stream ecosystems. energy in acquiring food. Ent. 24:351-377.

Anderson, N. H., and K. W. Cummins. 1979. MANAGEMENT CONS IDE RATIONS Influences of diet on the life his- tories of aquatic insects. J. Fish The multiple and intimate relationships Res. Bd. Can. 36:335-342. between the riparian zone and the stream 1963. ecosystem in forested watersheds makethis Ball, R. C., and F. F. Hooper. Translocation of phosphorous in a trout a critical interface for management. The riparian zone should be maintained as a stream ecosystem. In oolog, suitable source area for long-term physical edited by V. Schultz and A. W. Kiement, channel structure (e.g., wood debris) and Jr., pp. 217-228. First Nati. Symp. annual organic resources. Tools are avail- Radioecol. able for evaluating the stream community Ball, R. C., T. A. Wojtalik, and F. F. response to changes in the riparian source Hooper. 1963. Upstream dispersion the C/N of nutritional re- area, such as: of radiophosphorous in a Michigan sources, community metabolism (P/R, and Pap. Mich. Acad. Sci. macroinvertebrate functional group ratios. trout stream. Arts Lett. 48:57-64. Because the quality and quantity of inputs to forested headwater stream eco- 1962. An evaluation of systems from the riparian zone exerts a Cummins, K. W. some techniques for the collection and major control on community structure and analysis of benthic samples with function, a number of management strategies special emphasis on lotic waters. are possible. For example, selective har- Amer. Midl. Natur. 67:477-504. vest or enhancement of tree, shrub, or herbaceous species in the riparian zone Cummins, K. W. 1974. Structure and func- would be possible. Species such as alder BioScience generate rapidly processed litter which tion of stream ecosystems. produces nitrogen-rich leachate that is 24:631-641. quickly converted to FPOM, while conifer The ecology of run- needles (e.g., Douglas-fir) are utilized at Cummins, K. W. 1975. In much slower rates over longer time periods. ning waters: Theory and practice. In general, management of riparian Great Lakes Pollution from Land Use zones is management of headwater streams, Activities, Proc. Sandusky River Basin and management of headwater streams is cri- Symp., Joint Comm. mt. Ref. Gp., tical for managing the larger receiving edited by D. B. Baker, W. B. Jackson, streams and rivers. and B. L. Prater, pp. 227-293. Washington, D. C.: U.S. Govt. Printing Office. K. W. CUMMINS 197

Cummins, K. W., and M. J. Kiug. 1979. Odum, H. T. 1956. Primary production in Feeding ecology of stream inverte- flowing waters. Limnol. Oceanogr. brates. Ann. Rev. Ecol. Syst. 10:147- 1:102-117. 172. Petersen, R. C., and K. W. Cummins. 1974. Cummins, K. W., M. J. Kiug, R. G. Wetzel, Leaf processing in a woodland stream. R. C. Petersen, K. F. Suberkropp, Freshwat. Biol. 4:343-368. B. A. Manny, J. C. Wuycheck, and F. 0. Howard. 1972. Organic enrichment Rau, G. 1978. Carbon-l3 depletion in a with leaf leachate in experimental subalpine lake: carbon flow implica- lotic ecosystems. BioScience 22:719- tions. Science 201:901-902. 721. Ross, H. H. 1963. Stream communities and Fisher, S. G. 1977. Organic matter pro- terrestrial biomes. Arch. Hydrobiol. cessing by a stream-segment ecosystem: 59:235-242. Fort River, Massachusetts, U.S.A. mt. Rev. Ges. Hydrobiol. 62:701-727. Russell-Hunter, W. D. 1970. Aquatic Pro- ductivity. New York: Macmillan Co. Fisher, S. G., and G. E. Likens. 1973. Energy flow in Bear Brook, New Hamp- Sedell, J. R., F. J. Triska, J. D. Hall, shire: an integrative approach to N. H. Anderson, and J. L. Lyford, Jr. stream ecosystem metabolism. Ecol. 1974. Sources and fates of organic Monogr. 43:421-439. inputs in coniferous forest streams. In Inteerated Research in the Conifer- Hynes, H. B. N. 1963. Imported organic ous Forest Biome, edited by R. H. matter and secondary productivity in Waring and R. L. Edmonds, pp. 57-69. streams. Proc. 16th Internat. Congress Univ. of Washington, Coll. Forest Zool. 3:324-329. Resources, Conif. For. Biome Bull. 5.

Hynes, H. B. N. 1975. The stream and its Strahier, A. N. 1957. Quantitative valley. Verb. Internat. Verein. analysis of watershed geomorphology. Lixnnol. 19:1-15. Trans. Amer. Geophys. Union 83:913- 920. Leopold, L. B., M. G. Wolman, and J. P. Miller. 1964. Fluvial Processes in Suberkropp, K., and M. J. Kiug. 1976. Geomorphology. San Francisco: Fungi and bacteria associated with Freeman. leaves during processing in a woodland stream. Ecology 57:707-719. Nanny, B. A., and R. C. Wetzel. 1973. Diurnal changes in dissolved organic Swanson, F. J., and G. W. Lienkaenper. and inorganic carbon and nitrogen in a 1978. Physical consequences of large hardwater stream. Freshwat. Biol. organic debris in Pacific Northwest 3:31-43. streams. USDA Forest Service, Gem. Tech. Rep. PNW-69. Pacific Northwest Merritt, R. W., and K. W. Cummins, eds. Forest and Range Expt. Sta., Portland, 1978. An Introduction to the Aquatic Oregon. Insects of North America. Dubuque, Iowa: Kendall-Hunt. Vannote, R. L., G. W. Minshall, K. W. Cummins, 3. R. Sedell, and C. E. Cush- Merritt, R. W., and D. L. Lawson. 1979. ing. 1980. The river continuum con- Leaf litter processing in floodplain cept. Can. J. Fish Aquat. Sci. 37: and stream communities. In Strategies 130-137 for Protection and Management of Floodplain Wetlands and Other Riparian Wallace, J. B., and R. W. Merritt. 1980. Ecosystems, Proc. Symp. Forest Service, Filter-feeding ecology of aquatic edited by R. R. Johnson and J. F. insects. Ann. Rev. Ent. 25:103-132. McCormick. USDA Tech. Rep. WO-l2.

Ward, C. N., and K. W. Cumniins. 1979. Minshall, G. W. 1978. Autotrophy in Effects of food quality on growth of stream ecosystems. a BioScience 28:767- stream , Paratendipes 771. albimanus (Meigen) (Diptera: Chironomidae). Ecology 60:57-64. 198 FORESTS: FRESH PERSPECTIVES FROM ECOSYSTEMANALYSIS

Webster, J. R. 1975. Analysis of potassium and calcium dynamics in stream eco- systems on three southern Appalachian watersheds of contrasting vegetation. Ph.D. thesis, University of Georgia, Athens.

Wiggins, C. B., and R. J. Mackay. 1979. Some relationships between systematics and trophic ecology in Nearctic aquatic insects, with special reference to Trichoptera. Ecology 59:1211-1220. Appendix

FORTIETH ANNUAL BIOLOGY COLLOQUIUM

Theme Forests: Fresh Perspectives from Ecosystem Analysis

Dates April 27-28, 1979

Place Oregon State University, Corvallis, Oregon

Colloquium Committee Jerry F. Franklin, James D. Hall, J. Ralph Shay, Richard H. Waring, Donald B. Zobel

Standing Committee for the Biology Colloquium John L. Fryer, John C. Gordon, Norman E. Hutton, Charles E. King, Betty E. Miner, Thomas C. Moore, Dale N. Moss, James F. Oldfield, Theran D. Parsons, Henry Van Dyke, B. J. Verts, David L. Willis, Margy J. Woodburn

Colloquium Speakers, 1979 Daniel B. Botkin, George C. Carroll, Kermit Cromack, Jr., Kenneth W. Cumrnins, Jerry F. Franklin, W. F. Harris, James A. MacMahon, D. McGinty, R.V. O'Neill, Dennis Parkinson, D. F. Reichle, Dan Sanantonio, Wayne T. Swank, Frederick J. Swanson, Frank J. Triska, Jack B. Waide, Richard H. Waring

Sponsors Agricultural Experiment Station Ccllege of Science Environmental Health Science Center Environmental Protection Agency Phi Kappa Phi Research Council School of Forestry Sigma Xi