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Ecology, 82(12), 2001, pp. 3275±3284 ᭧ 2001 by the Ecological of America

IS IT TIME TO BURY THE ? (WITH FULL MILITARY HONORS, OF COURSE!)1

ROBERT V. O'NEILL Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831-6036 USA

ROBERT V. O'NEILL, MacArthur Award Recipient, 1999

Abstract. The ecosystem concept has become a standard paradigm for studying eco- logical systems. Underlying the ecosystem concept is a ``machine analogy'' derived from . This analogy is dif®cult to reconcile with our current understanding of ecological systems as metastable adaptive systems that may operate far from equilibrium. This paper discusses some logical and scienti®c problems associated with the ecosystem concept, and suggests a number of modi®cations in the paradigm to address these problems. Key words: ecosystem; ecosystem stability; ecosystem theory; ecotone; Homo sapiens; natural selection; ; Systems Analysis.

INTRODUCTION cosm, a relatively closed, self-regulating system, an The term ecosystem was coined by Tansley in 1935. archetypic ecosystem. But as Botkin (1990) points out, the underlying concept Science emerged from the Second World War with goes back at least to Marsh (1864). Nature was viewed a new paradigm, Systems Analysis (e.g., Bode 1945), as relatively constant in the face of change and repaired which seemed uniquely suited for this ``balance of na- itself when disrupted, returning to its previous balanced ture'' concept, and ®t well with earlier work on the state. Clements (1905, 1916) and Elton (1930) offered stability of interacting populations (Nicholson and Bai- plant and animal succession as basic processes that ley 1935). Systems Analysis dealt with complex sys- permitted relative constancy by repairing damage. tems as interconnected components with Forbes (1925) described the northern lake as a micro- loops (Hutchinson 1948) that stabilized the system at a relatively constant equilibrium point. Systems Anal- Manuscript received 22 June 2000; revised 5 March 2001; ysis can be seen underlying E. P. Odum's (1953) def- accepted 6 March 2001. inition of the ecosystem as a ``. . . natural unit that 1 Presented 9 August 1999 in Spokane, Washington, USA. includes living and nonliving parts interacting to pro- 3275 3276 ROBERT V. O'NEILL , Vol. 82, No. 12

duce a stable system in which the exchange of materials cies diversity by adding edge species. Eutrophication between the living and nonliving parts follows circular leads to lakes with greater . There isn't any paths ....'' environmental crisis at all! The machine analogy, inherent in Systems Analysis, It is important to recognize that not all of the back- became a central paradigm for many ecologists (Odum lash has an ideological bias. The ecosystem concept is 1971, Holling 1973, Waide and Webster 1976). The also broadly criticized within ecology. One of the clear- paradigm offered a practical approach to the enormous est statements is given by Pickett et al. (1992): ``The of natural systems (Teal 1962, Van Dyne classical paradigm in ecology, with its emphasis on the 1969). The paradigm helped harness the power of the stable state, its suggestion of natural systems as closed computer in ecosystem models (Olson 1963). The par- and self-regulating, and its resonance with the nonsci- adigm permitted a holistic view of system enti®c idea of , can no longer serve such as nutrient cycling (Webster et al. 1974). The as an adequate foundation for conservation.'' familiarity of the machine analogy facilitated the com- There is the temptation, of course, to respond de- munication of ecological to the public. fensively to the backlash. After all, the ecosystem the- If the ecosystem concept has held such a central ory being attacked is a sort of historical artifact, a place in ecology and been so productive of new ideas, ``straw man.'' are now seen as disequili- why call it into question? The simple fact is that the brial, open, hierarchical, spatially patterned, and scaled ecosystem is not an a posteriori, empirical observation (O'Neill et al. 1982, Pickett et al. 1992, Levin 1999). about nature. The ecosystem concept is a paradigm Many of the criticisms have been addressed as the the- (sensu Kuhn 1962), an a priori intellectual structure, a ory matured. But rather than provoking a defensive speci®c way of looking at nature. The paradigm em- reaction, perhaps the backlash should motivate a care- phasizes and focuses on some properties of nature, ful re-examination of the ecosystem concept. while ignoring and de-emphasizing others. After a half century of application, the paradigm is showing some SCIENTIFIC PROBLEMS rust. Limitations in the concept are becoming more The ecosystem concept is a paradigm, i.e., a con- apparent and leading to a vigorous backlash toward venient approach to organizing thought. Like any par- ecosystem concepts in particular, and ecology in gen- adigm, it is a product of the human mind's limited eral. ability to understand the complexity of world. In the case of ecological systems, we are faced with BACKLASH AGAINST THE ECOSYSTEM CONCEPT hundreds to thousands of interacting populations. The Part of the backlash results from the apocalyptic fer- systems vary through time in complex ways, and they vor of the environmental movement over past decades. are spatially heterogeneous at every scale. Perspectives Ecology oversold its ability to predict doom, and is The ecosystem concept takes these impossibly com- now seen as unnecessarily constraining human freedom plex phenomena and focuses on a small subset: the and economic growth. In¯uential opponents simply average or integrated properties of all the populations dismiss the prophecy (Simon 1980), and offer opti- within a speci®ed spatial area. This approach has the mistic counterclaims (Naveson 1993). Human inge- advantage of identifying ``emergent'' properties such nuity is seen as suf®cient to feed, clothe, and supply as ¯ow and nutrient cycling, and permits study energy to an ever-growing population for the next seven of the relative stability of this abstract structure and its billion years (Myers and Simon 1994)! function. Clearly, there are ideological underpinnings to this But in order to gain these advantages, the concept backlash. Anything that limits human development is accepts a set of assumptions that limits our thinking immediately suspect. Nevertheless, the critique high- and determines the questions we ask. Therefore, we lights important limitations in ecological theory must continuously examine the assumptions, and con- (Shrader-Frechette and McCoy 1993, Shrader-Frech- sider the questions they might keep us from asking. ette 1995, Callicott 1996). The critics claim that the Most importantly, we must examine whether the as- ecosystem concept isn't a scienti®c theory at all, simply sumptions limit our ability to answer the very ques- a statement about physical constraints on living things tions, such as relative stability, that the concept was (Sagoff 1997). Concepts like stability and ecosystem designed to address. are ambiguous and de®ned in contradictory ways. In The proposed exploration is rendered dif®cult by the fact there is no such thing as an integrated, equilibrial, ambiguity of terms like complexity, ecosystem, and homeostatic ecosystem: It is a myth (Soule and Lease stability. Pimm (1984) pointed out that a change in 1995)! these de®nitions can lead to signi®cantly different con- If there is no stable equilibrium, why bother to con- clusions about stability. At present, the terms ``eco- serve? Protecting and restoring endangered species is system'' and ``ecosystem theory'' are used in many unnecessary, species go extinct all the time. How do different ways. At one extreme, ecosystem is a con- you restore ecosystems when you don't know what to venient term, relatively free of any assumptions, that restore them to? Fragmentation actually increases spe- indicates the interacting and abiotic factors December 2001 MACARTHUR AWARD LECTURE 3277 in an area. At the other extreme, ecosystem is a pre- heterogeneity. The stability of an ecological system cisely de®ned object of a predictive model or theory. cannot be predicted by a theory that ignores hetero- As a result, any limiting assumption that is offered here geneity. may be disavowed by some subset of ecologists. Nev- ertheless, the critical examination is important, even if Latin binomials are substitutable no single ecologist would admit allegiance to the total Most ecologists consider the species list critical to set of assumptions. With this dif®culty in mind, let us the de®nition of an ecosystem, often designating eco- consider some implicit assumptions and their impact system types by their dominant species. Nevertheless, on addressing stability. some degree of substitutability is implicit in the eco- system concept. For example, an impacted ecosystem Spatial closure would be considered ``recovered'' if succession re- The ecosystem concept considers a speci®c spatial placed the dominant species, and brought the system unit: classically, a small watershed for terrestrial sys- back to the same physiognomy and functional attri- tems and a lake for aquatic systems. The concept looks butes. But the species list of soil organisms, for ex- within these boundaries to locate the signi®cant dy- ample, need not be identical. The functional properties namics that require explanation and the signi®cant pro- of the system are restored, but with an altered species cesses that will explain the dynamics. The boundaries list. In fact, in much of ecosystem theory, the stated may be open to the exchange of organisms, energy, and variables are functional groups, such as trophic levels, matter. Nevertheless, the ecosystem concept assumes and which of several species perform the function is that the interactions and feedback loops necessary and not considered. suf®cient to explain dynamics occur within the bound- The ambiguity introduced by species substitutability aries. is often unrecognized. But the inconsistencies are The problem with this assumption is that the spatial brought out by the seemingly inane question: ``Do eco- distributions of the component populations may be systems die?'' Consider, for example, a northern lake much larger than the ecosystem boundaries. Indeed, that has undergone eutrophication. If the ecosystem is Perspectives even the home ranges of individuals may be larger than de®ned as a functional system at a spatial location, then the ecosystem, particularly for predators. This leads to the lake is the same ecosystem, albeit altered by anomalies, such as calculations determining changed conditions. On the other hand, if the ecosystem that an ecosystem can support one half of a top car- is de®ned by the species list, then the oligotrophic eco- nivore, without specifying which end. But importantly, system has been killed and replaced by a eutrophic dispersal from outside system boundaries is a critical ecosystem. The ecosystem de®ned by a species list is mechanism for system stability. Thus, an internal pro- almost always unstable because it rarely, if ever, re- cess, recovery, is not explicable by occurring covers to the identical list of species. within the system speci®cations. The critical obser- If the ecosystem is de®ned by the species list, the vation is that a plot surrounded by continuous only stable systems are found in extreme conditions forest behaves differently from that same forest plot in with impoverished species lists, such as the Arctic tun- isolation. At the minimum, the spatial context of the dra. In such conditions, recovery occurs to the same system and all its component populations must be in- species list because only a few species can survive. But cluded in the speci®cations of the ecosystem. The sta- this leads to the anomalous conclusion that stability is bility properties of an ecological system cannot be ex- inversely related to . Although the biodi- plained by a paradigm that only considers dynamics versity±stability relationship is questionable (see e.g., occurring within the ecosystem boundaries. Huston 1994), the relationship suddenly reverses and becomes crystal clear. The probability of a system re- Spatial homogeneity covering to an identical species list is dependent on A second assumption of the concept is spatial ho- how long the list is, making ecosystems more mogeneity. Spatial heterogeneity within the spatial unit stable than tropical ! is averaged in order to focus on integrated or emergent The dilemma would seem to be solved by de®ning properties. And yet it is the internal heterogeneity, or the ecosystem by the rate processes plus dominant spe- the heterogeneity of the larger spatial context, that cies. But problems still arise in dealing with stability. maintains the full range of populations needed to main- Consider a marine fouling (Sutherland tain stability. Without the heterogeneity, for example, 1974) that may recover to the same rate processes, but pioneer species are not maintained, and recovery be- any of several different species lists. In Serengeti±Mara comes impossible or follows an unpredictable course. woodlands, and ®re interact to produce a va- A homogeneous ecosystem, like an overspecialized riety of stable states (Dublin et al. 1990, Dublin 1995). species, cannot respond to change and is inherently Are these stable ecosystems with several ®nal states? unstable. The critical observation is that two forest Or are these unstable ecosystems? plots may have identical average properties, but dif- The problem is compounded by evidence from the ferent relative stability if they differ radically in spatial pollen record. Over glacial cycles, the record shows 3278 ROBERT V. O'NEILL Ecology, Vol. 82, No. 12

that species respond individually to changing condi- way, natural selection is assumed to operate slowly. tions (Davis 1976). Different species, even dominants, Therefore, its dynamics can be assumed to be constant move in or out of an area based on their individual over the time scales relevant to ecosystem behavior. responses to temperature and other changes (Delcourt But the advantage gained may not outweigh the losses. and Delcourt 1987). As a result, intact communities of Natural selection is the most powerful predictive theory organisms do not move as a unit, and the collection of available to ecology. interacting species at a location is continuously chang- In the extreme, ecosystem speci®cation may simply ing. The conservative conclusion is that the entity ignore the identity of component populations. But this ``ecosystem'' is unstable. The more radical conclusion extreme admits of a reductio ad absurdum. The forest is that ecosystems, de®ned by their species list, don't ecosystems of eastern North America have lost the cou- exist and never have. gar, woodland bison, wolf, and bear. The presettlement The solution to the problem would seem to involve Passenger Pigeon population is estimated at 3 to 5 bil- ignoring the species list altogether and assuming per- lion (Schorger 1955). In the 1870s, Audubon estimated fect substitutability. The stable entity is the collection a single ¯ock at 136 million. It moved ``. . . like a tor- of functional groups that recover to the same rate pro- nado through the forest ...''breaking off trees up to cesses, feedbacks, and complex organization. Indeed, two feet in diameter when it roosted (Schorger 1955). this solution is the one implicitly adopted in many ap- It is absurd to maintain that rate processes and stability plications of the ecosystem concept. But this solution were not altered by replacing these woodland species also leads to anomalous conclusions when applied to with Homo sapiens. In fact, many have ecological phenomena other than stability. this same disruptive . Examples include cattle, Consider, for example, the phenomenon known as kudzu, coconut, and zebra mussel. the ecotone. The ecotone is a tension zone where one The simple empirical fact is that ecosystems are col- vegetation type changes suddenly into another, e.g., lections of interacting populations. The component grassland into scrub (Hobbs 1986) or forest (Hansen populations have been shaped by natural selection. The et al. 1994). These transitions have long attracted the resulting biotic potential determines ecosystem dynam- attention of ecologists (e.g., Clements 1897, 1905, Liv- ics just as much as chemical and physical constraints. ingstone 1903, Griggs 1914). But the ecotone is de®ned Critically, natural selection is one of the processes that by a change in the species list, particularly in the dom- determines system stability. inants. Since environmental constraints are very similar on either side of the ecotone, rate processes would also Stability is a scaled concept be expected to be very similar. If the ecosystem is A different ambiguity arises because the concept of de®ned strictly in terms of function, there is not a dif- stability cannot be de®ned independently of the scale Perspectives ferent ecosystem on either side of the ecotone. In fact, of observation. The dependence on scale is revealed the ecotone doesn't exist! when one considers the full spatiotemporal spectrum Nevertheless, if we limit consideration to stability of disturbances. Disturbances that are frequent and phenomena, a functional de®nition with an assumption smaller in spatial scale than the de®ned ecosystem of species substitutability seems the logical choice. The boundaries can be counteracted by internal mecha- abstraction and the associated assumptions limit the nisms. The ecosystem would be considered stable to utility of the theory for explaining other phenomena, these disturbances. Up to some point, the ecosystem such as ecotones. Of course, this means that the eco- also recovers from larger scale , i.e., dis- system concept is not adequate as a general theory of turbances that have greater spatial extent and occur less ecological phenomena, but at least it permits expla- frequently. Recovery now involves mechanisms, such nation of stability. The functional theory de®nes an as dispersal, which are not ordinarily considered as entity that maintains a trophic structure, recycles nu- internal ecosystem processes. Nevertheless, we could trients, and recovers from disturbance. Minimizing the still consider the ecosystem as responding stably. role of latin binomials seems to permit a consistent Ultimately, of course, the ecosystem is unstable. It framework for dealing with stability. is only a matter of time until a disturbance of suf®cient intensity and spatial extent overwhelms the ecosys- Natural selection minimized or ignored tem's ability to respond. Examples include broad-scale The assumption of species substitutability minimizes deserti®cation and rare asteroid collisions. Over a suf- the role of natural selection. This may be the concept's ®ciently long period of time, the cumulative probability most serious limitation in dealing with stability. Nat- of a catastrophic event approaches 1.0. ural selection is relegated to a background role causing The problem would seem to be solved by specifying component populations to optimize or maximize their the time period of concern, e.g., the ecosystem is stable share of resources. As a result, functional groups can over millennia. But ambiguities remain. If stability de- be assumed to be operating at the rates set by physical pends on the spatial extent of disturbances, then the and chemical constraints. Ecosystem dynamics can size of the ecosystem matters. The relative stability of then be predicted from these constraints. Stated another two systems that differ radically in size cannot be ex- December 2001 MACARTHUR AWARD LECTURE 3279 plained by internal mechanisms. If the disturbance re- perature is increasing faster than it has in the last 10 000 gime is the same, the smaller ecosystem is logically yr (Arrhenius and Waltz 1990). The human economy less stable because it can sustain itself over a shorter uses 40% of net (Vitousek et al. period of time. If the disturbance regime is radically 1986). Soil erosion is nearly universal, with soil losses different, the relative stability of similar-sized ecosys- exceeding soil formation rates by at least 10-fold (Pi- tems cannot be explained by internal mechanisms. The mentel 1993). ecosystem in the harsh is logically less It is clear that Homo sapiens has altered the physical stable because it can sustain itself over a shorter period environment of the ecological system. We have of time. To deal with stability resulting from internal changed process rates ranging from productivity to dis- mechanisms requires that the de®nition of the ecosys- persal. We have changed ecological structure by elim- tem itself specify (1) the disturbance regime, and (2) inating our competitors, e.g., timber wolves, and even the size of the speci®c system under consideration. food species, e.g., Passenger Pigeon. It becomes fa- Another way to view the scale problem is to consider cetious to talk about and continued ex- how we use the term ``disturbance.'' Once the bound- traction of and services when we cannot specify aries of the ecosystem are delimited, the continuous with any scienti®c rigor how Homo sapiens has already distribution of environmental variability is divided into altered the stability properties of the system. internal conditions and external disturbances. Small- scale variability, such as the daily light cycle, seasonal Summary temperature changes, or the occasional death of a dom- The importance of the de®nitional ambiguities be- inant individual are considered to be part of ecosystem comes apparent if we consider the for coming dynamics. Larger scale variability, such as wild®re, is up with the ecosystem concept in the ®rst place. The not considered to be part of ecosystem dynamics. theory provides an explanatory framework for ecolog- By focusing on the ecosystem as a self-regulating, ical phenomena. Without reverting to a naive concept integrated system, we are led to focus on that system's of the balance of nature, the relative stability of eco- resistance to disturbances, minimizing the impacts, and logical systems represents a fundamental phenomenon Perspectives resilience or recovery from disturbance back to some to be explained. Therefore, an adequate theory must optimal state or states. Disturbances are viewed as a be able to deal with stability. At present, the ambiguity damaging external interference. Yet it is well docu- involved in the de®nition of an ecosystem leads to basic mented that preventing damage can be catastrophic. problems in explaining stability. Therefore, the ambi- The obvious examples are practices that guities undercut the very purpose for which the concept prevent small wild®res. The spatiotemporal spectrum was devised. of environmental variability determines ecosystem sta- The focus on internal dynamics and stability creates bility just as surely as internal feedback mechanisms. a mindset that excludes relevant phenomena. In fact, Therefore, ecosystem stability cannot be explained un- the most fundamental observation is sustainability un- less the disturbance regime is part of the speci®cations der conditions of constant change. The stasis implied of the ecosystem. by the ecosystem concept is self-limiting. The critical property is the ability to change state in response to a Homo sapiens is not a component of the ecosystem continuous spectrum of change and variability. Sus- The ecosystem concept typically considers human tainability of ecological systems involves two anti- activities as external disturbances to the ecosystem. thetical elements: (1) local and short-term stability in Other invasive pests, such as kudzu and brown rats, the sense of recovery from disturbance, and (2) ¯exi- are considered as ecosystem components, and their im- bility in the sense of maintaining variability of structure pact on structure and function considered explicitly. in space and time because conditions will change. Homo sapiens is the only important species that is con- sidered external from its ecosystem, deriving goods and ELEMENTS OF A NEW PARADIGM services rather than participating in ecosystem dynam- None of the criticisms offered in the previous section ics. are new. Many would seem to be addressed by so- If there was ever a species that quali®ed as an in- phisticated developments in ecosystem theory involv- vasive pest, it is Homo sapiens The litany is familiar ing, for example, nonlinear dynamics and fuzzy set but merits repetition. Since 1850, the human population theory. Unfortunately, the developments make the eco- has quintupled, and per capita energy use has quadru- system theory more intriguing for mathematicians, but pled (Holden 1991). Human inputs of nitrogen now less useful and intuitive for biologists. I would offer exceed natural rates of nitrogen ®xation (Vitousek for consideration that none of the developments address 1994), and nitrogen saturation leads to the loss of other all of the ambiguities, and that we are putting splints important nutrients, such as calcium (Vitousek et al. and patches on an old horse. 1997). Inputs of nitrogen to the North Atlantic have What is proposed here is not a complete theory. What increased by a factor of two to twenty compared to pre- is offered is a set of principles that might lay the foun- industrial inputs (Howarth et al. 1996). Average tem- dation for such a theory. In essence, these principles 3280 ROBERT V. O'NEILL Ecology, Vol. 82, No. 12

constrain the theory to (1) be explicitly scaled, (2) in- logic events may create or remove dispersal barriers. clude variability, (3) consider long-term sustainability These changes may happen slowly and monotonically, in addition to local stability, and (4) include population permitting adaptive responses by component popula- processes as explicit system dynamics. The ®rst step tions, or they may occur rapidly and produce cata- is to include the spatial context in the system de®nition. clysmic changes. In addition, conditions within the po- 1) An ecological system is composed of a range of tential dispersal range are not uniform. They vary on spatial scales, from the local system to the potential a large scale along environmental gradients, and they dispersal range of all of the species within the local vary locally due to soils, topography, aspect, etc. Thus, system. the spatiotemporal variability that can be ignored with- The recovery of the local ecological system depends in the boundaries of the local system may be critical, critically on the ability of individuals and populations and must be explicitly considered before the stability to disperse into an impacted area. Dispersal is a critical of the local system can be predicted. ingredient in explaining the stability of ecological sys- 4) Within the potential dispersal range is an effective tems (Huffaker 1958). Therefore, the minimal area re- dispersal range that is time-scaled to the problem at quired to explain recovery is not the boundary of the hand. local ecosystem, but the dispersal range of its com- Typically, an individual study focuses on a limited ponent biota. range of scales. For simplicity, consider a regularly 2) The potential dispersal range is set by (a) the repeating impact on a local ecological system. The in- environmental constraints (biotic and abiotic) for each terval between impacts determines an effective dis- species, by (b) dispersal barriers, and by (c) species persal range, i.e., the distance over which the popu- dispersal mechanisms. lations needed for recovery can move and become es- The critical area is not the total distribution of the tablished before the next impact. Over geologic time, species, but that portion of the range that is accessible the effective dispersal range might equal the complete to the local ecological system of interest. A dispersal potential dispersal range. For smaller scales or more barrier, e.g., human land use, may mean that the po- frequent impacts, the effective dispersal range would tential dispersal range is much smaller than the total be much smaller. distribution of the species. On the other hand, human 5) Within the local system, populations interact to activities may expand the potential range by providing maximize biotic potential. new dispersal routes that permit the invasion of non- A local ecological system, such as a watershed, forest indigenous species. stand, or lake, has three factors that determine dynam- Thus, human use of space may have critical impacts ics. First, the physical conditions at the site form a on stability by creating dispersal barriers. In constrict- constraint set that determines the dynamic potential. Perspectives ing the potential dispersal range, society limits the total Second, the potential biota are constrained to the pop- range of environmental variability to which the local ulations whose distributions overlap at this site. Within ecosystem can respond stably. For example, a small these physical and biotic constraints, the populations dam makes the upstream ecosystem unstable to any then interact to form complex networks and feedback ¯uctuation that kills ®sh and other organisms that must loops. migrate back into the area to permit recovery. Here the and determine what subset scaled impact is insidious because immediately follow- of the potential biota actually function on the site and ing construction of the dam, the upstream ecosystem may permit a of different states for the site. As and its internal feedback mechanisms appear intact. a result, the list of species currently resident on a site Thus, Homo sapiens is a , like the is not necessarily suf®cient to explain the range of beaver (Naiman et al. 1986) or star®sh (Paine and Levin potential system responses to impact. Indeed, ¯exibility 1981), that alters the structure of its ecological system. in the species list is critical to the sustainability of By introducing dispersal barriers, Homo sapiens ex- ecological systems across the geologic scale of vari- cludes populations even though the site is within their ability. potential dispersal range. And by constructing invasion Competition operates within the constraints of phys- pathways, Homo sapiens introduces populations that ical , such as , and the interacting would not otherwise occur. As a result, land use change populations move toward maximizing the biotic po- becomes a component of stability dynamics. Homo sa- tential of the site. The biotic potential forms an at- piens, as a dynamic component of the ecological sys- tractor, and interactions, such as nutrient cycling, move tem, may have more far-reaching impacts on stability the set of populations toward this potential. But nutrient than society viewed as extracting goods and services cycling is an emergent property that cannot be ex- from the local system. plained by competition alone. Energy ¯ow and nutrient 3) The potential dispersal range is not constant or cycling operate on the same spatiotemporal scale as uniform. competition, and it is the combination of the two dy- Over time, this potential dispersal range can change, namics that results in ecosystem function. for example, with changes in climate. In addition, geo- 6) As the local ecological system approaches the December 2001 MACARTHUR AWARD LECTURE 3281 biotic potential of a site, it increases local stability, If rates of change in the conditions are slow, or the but decreases global sustainability. recurrence interval of disturbances is long relative to As the system develops feedback loops and complex the rates of response by the local system, then the sys- networks of interactions, it becomes better adapted to tem is stable. If rates of change are rapid or the re- local conditions and more stable to local impacts. But, currence interval is short, relative to rates of response, over longer time scales, conditions change continu- the ecological system is unstable. If rates of change are ously. So as the system approaches the present attractor nearly equal to rates of response, the system will appear by maximizing biotic potential, it becomes suboptimal to be highly variable or even chaotic (Phillips 1996). to the changed conditions. A process analogous to spe- For this , human manipulations of the distur- cies specialization occurs. bance regime are just as important as disrupting the The existence of local attractors becomes conspic- structural and functional integrity of the local system uous at the ecotone. A small change in the environment itself. changes the competitive relationship between domi- 8) Stability of the local ecological system depends nants, and as disturbances destroy the existing vege- on the spatial scale of observation and the critical tation and open the opportunity for new vegetation to balance between (a) the size distribution of distur- take over the site, a different system of interacting pop- bances, and (b) the effective dispersal ranges of the ulations gains a competitive advantage. The critical biota. observation is that a small change in conditions has If the spatial extent of the ecological system under shifted the local attractor. The system that converged consideration is large, for example, approaching the to one attractor becomes suboptimal when the attractor size of an , then only extremely large and changes. It follows that the tendency to converge to a rare disturbances can overcome its ability to respond local attractor may also make the system vulnerable to stably. If a local system of small extent is being con- changes in the attractor. sidered, for example, an isolated forest plot, then the What maintains the sustainability of ecological sys- probability of a destabilizing event increases propor- tems over long periods of time is heterogeneity in time tionately. Perspectives and space. Heterogeneity is not an annoyance that com- If the spatial extent of disturbances is small relative plicates experimental designs, it is a critical ingredient to the size of the ecological system, then spatial het- in explaining the stability of ecological systems (Roff erogeneity will be maintained within the effective dis- 1974a, b). Consider, as an extreme case, that a uniform persal ranges of biota, and the system will be stable. plain with no variation in time could result in the loss If the disturbances are large and approach the effective of pioneer and successional species required for re- dispersal range of pioneer and successional species, the covery when the inevitable impact does occur. system will be unstable. If the disturbance size and The consideration of heterogeneity recommends an effective dispersal ranges are nearly equal, the local important change in ecosystem theory. The stability of system will appear highly variable or chaotic. the system depends on two complementary and scaled Clearly, time and space scales are related (O'Neill processes. Stability to smaller scale impacts depends 1988). Stability depends on disturbance intervals rel- on the system's ability to resist change and recover ative to recovery rates, and the spatial extent of dis- with resilience. But long-term stability or sustainability turbances relative to the spatial extent of the effective depends on a ¯exibility of response that can only be dispersal range (Turner et al. 1993). The critical ob- maintained in an environment that varies in time and servation is that the internal interactions and feedback space. mechanisms within the local system are only one of a 7) Stability of the local ecological system depends number of processes determining stability. The his- on the time scale of observation and the critical balance tory and dispersal ability of component populations, between (a) rates of change in environmental condi- and the heterogeneity of the landscape must also be tion, and (b) rates of change in the biota. considered. Over short intervals of observation, environmental 9) Homo sapiens is a keystone species that changes variability is likely to be small and the local system system stability by altering environmental constraints, will appear stable. Over geologic time, the probability rate processes, and biotic structures. of a catastrophic event approaches 1.0 (Crowley and The impact of Homo sapiens is not limited to the North 1988), and the local system is unstable. Even in quantity of goods and services extracted from the eco- the absence of catastrophic events, gradual change in system. The long-term impact of this keystone species the environment may eventually move the local system will likely be determined by the way it alters the sta- across a critical threshold, change the local attractor, bility properties of ecological systems. and make the local system unstable. Thus, the relative Homo sapiens changes the frequency distribution of stability of two systems is not simply measured by the disturbances. For example, the suppression of small rate of recovery from a disturbance, but also by the wild®res changes the competitive advantage of ®re- expected length of time until the next catastrophic resistant dominants and alters biotic structure (Botkin event. 1990, Buell et al. 1954). Fire suppression also decreas- 3282 ROBERT V. O'NEILL Ecology, Vol. 82, No. 12

es the small-scale heterogeneity of the landscape and CONCLUSIONS increases the probability of larger ®res. All of these Is it time to bury the ecosystem concept? Probably impacts change the stability properties of the system. not. But there is certainly need for improvement before By fragmenting the spatial structure of the landscape, ecology loses any more credibility. This paper suggests Homo sapiens alters connectivity and dispersal some of the key problems. Spatial pattern, extent, and rates (Gardner et al. 1993). By creating dispersal bar- heterogeneity are critical to stability. You cannot get a riers, this species decreases the potential dispersal predictive theory if you assume them away. Temporal range of endemic species. By creating dispersal path- variability and scale are critical to stability. You cannot ways, this species greatly increases the effective dis- get a predictive theory if you assume them away either. persal range of exotics (D'Antonio and Vitousek 1992). It is the interplay of natural selection and internal feed- Changes in landscape structure, such as habitat loss, back mechanisms that determines dynamics. Again, can be particularly insidious if an is you cannot get a predictive theory if you assume either incurred, and observable species loss does not occur away. Basically, all the processes and constraints need- until much later (Tilman et al. 1994, Loehle and Li ed to explain stability are not encompassed within the 1996). Once again, these changes impact the stability boundaries of the local ecological system. properties of the system even though they are not direct An improved paradigm would have many implica- effects on the interactions and feedback mechanisms tions for ecological applications, such as conservation. within the local ecological system. Increasing the size of an isolated preserve only in- Homo sapiens is changing the physical and chemical creases the length of time until the cumulative prob- constraint space within which ecological systems op- ability of a disruption approaches 1.0. Maintaining dis- erate. The average changes, e.g., in mean temperature, persal pathways might better conserve sustainability may be small and result in minor changes in average by keeping the potential dispersal range near its orig- rate processes. But even small changes can switch the inal, undisturbed scale. local attractor and move the system to a new state. There are also important implications for monitoring. Goldemberg et al. (1996) point out that even modest Current theory leads us to focus on average rates and increases in temperature can exclude crops that are in- standing crops at a location. Yet scale and variability tolerant to the additional few extreme days. Similarly, in space and time may be more important in determin- the temporal extremes of temperature at the spatial ex- ing sustainability. Mean values at two locations may tremes of system distribution are likely to move eco- indicate that no signi®cant change has occurred, but if tones by switching the local attractor. dispersal pathways between the sites have been dis- The assertion that Homo sapiens is impacting the rupted, one has reduced by orders of magnitude the

Perspectives stability properties of ecological systems is not extreme scale of a catastrophic disturbance. or apocalyptic. Sackcloth and ashes are not required, Perhaps the most important implication involves our just a review of documented examples that have already view of human society. Homo sapiens is not an external occurred (e.g., Loehle 1989): Extensive coral reefs disturbance, it is a keystone species within the system. have been destabilized (Hughes 1994), and grazing has In the long term, it may not be the magnitude of ex- destabilized semi-arid (Walker et al. 1969, tracted goods and services that will determine sustain- Loehle 1985). In the extreme, overgrazing turns the ability. It may well be our disruption of ecological to barren desert (Hills 1966). Nutrient addi- recovery and stability mechanisms that determines sys- tions have destabilized oligotrophic lake ecosystems tem collapse. (Recknagel 1985, Carpenter et al. 1998). Harvesting Certainly, we don't want to dismiss the current the- has destabilized competitive interactions leading to the ory prematurely. But we must understand that the ma- extinction of many ®sh populations (Watt 1968, Jones chine analogy is critically limited. In so far as the local and Walters 1976). Extensive agriculture destabilized system maximizes environmental potential, it neces- large areas of the United States to drought, resulting sarily sacri®ces stability when that potential changed. in massive erosion and the Dust Bowl (Kahn 1995). The challenge to the ecological system is optimization Theoretical studies provide the explanation for such to a moving target. Optimize too rapidly and the system destabilization in complex ecological systems in gen- is trapped in a local attractor and, like an overspecial- eral (May 1977), and ecosystems in particular (O'Neill ized species, cannot adapt when conditions change. So, et al. 1982, 1989). Tainter (1988) points to the possi- it would not be wise to send the old dobbin to the glue bility of similar mechanisms in the collapse of human factory before we determine how well the new one . takes the bit. But it certainly seems to be time to start The fundamental problem is that Homo sapiens is shopping for a new colt. moving ecological systems outside the envelope of conditions that have existed over evolutionary history. ACKNOWLEDGMENTS This is terra incognita and the assumption that ecolog- Oak Ridge National Laboratory is operated for the U.S. ical systems will respond stably is unjusti®ed. Department of Energy by UT-Battelle under contract number December 2001 MACARTHUR AWARD LECTURE 3283

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