understanding ecological community succession: causal models and theories, a review

Vegetatio 110: 115-147, 1994. © 1994 Kluwer Academic Publishers. Printed in Belgium. 115

Understanding ecological community succession: C a u s a l mode l s a n d theories, a review

L. J. McCook Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada Present address: Australian Institute of Marine Science, PMB =~ 3, Townsville, M. C., Queensland, 4810, Australia

Accepted 1.12.1992

Keywords: Succession, Inhibition, Facilitation, Life history, Constraints, Autogenic

Abstract

Critical review of explanations for patterns of natural succession suggests a strong, common basis for theoretical understanding, but also suggests that several well known models are incomplete as explanations of succession. A universal, general cause for succession is unlikely, since numerous aspects of historical and environmental circumstances will impinge on the process in a unique manner. However, after disturbance, occupation of a site by any species causes changes in the conditions at the site. Sorting of species may result, since different species are adapted to different regions of environmental gradients. Such sorting can generate several patterns of species abundance in time, but commonly results in sequential replacements of species adapted to the varying conditions. This may be due to constraints on species' strategies, or life history traits, placed by the limited resources available to the organism. These constraints often result in inverse correlation between traits which confer success during early and late stages of succession. Facilitatory or inhibitory effects of species on each other are best understood in terms of these life history interactions, perhaps as restrictions on, or as moderation of, these processes.

Strong support for the importance of correlations in life history traits stems from comparisons of simulated succession with and without these correlations. These simulations are reviewed in some detail, and followed by brief reviews of other prominent models for succession. Several aspects of the confusion and controversies in the successional literature are then discussed, with a view to a more optimistic synthesis and direction for successional ecology.

"7 confess I was surprised to find my theory so perfectly proved in this case. '" (Thoreau, H. D. 1860. The succession of forest trees, p. 235)

Introduction: Succession- ubiquitous pattern, unique processes

Ecological succession is an important concept to understanding ecological systems. Successions may be observed at a broad range of scales, from the microscopic to the continental, from minutes

to millennia. Patterns of succession or vegetational change can be asserted, to some degree and at some scale, for almost any natural system (e.g. Anderson 1986). Yet in many respects, individual successional processes appear to be unique, and dependent on timing, initial conditions and other factors (eg. Sousa 1984). The goals of succes-

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sional ecology are to describe the similarities and differences in both the pattern and the process: to extract generalizations, and to identify the bases for differences in process.

The field has generated both excitement and controversy for biologists for over a century (e.g. Thoreau 1860; Clements 1928; Gleason 1927; Loehle 1988, 1990; Shrader-Frechette & McCoy 1990; Farrell 1991). In fact, understanding succession is as important today as ever, both in terms of amount of research effort and in terms of understanding changes in natural and man- aged environments.

The patterns of succession: empirical observation

It has long been observed that natural vegetation at widely different sites often undergoes similar basic patterns of change in species abundances, in response to disturbances or changes in the environment. These changes often involve the appearance or dominance of species with progressively greater maximum size, age, and shade tolerance, and progressively lower maximum growth rates and dispersal abilities. Such generalizations are easily recognized, yet real situations vary enormously in both empirical and interpre- tative details (e.g. Clements 1928; Drury & Nis- bet 1973; Sousa 1984; Walker & Chapin 1987; McCook & Chapman 1991, 1992, in press; Mc- Cook 1992).

Unfortunately, our understanding of ecological succession has been impeded by several problems, resulting in considerable confusion about the processes that are important during successions. In particular, the successional literature lacks integration. Many field studies are either poorly designed, purely anecdotal, or test theoretical concepts that are inconsistent or confounded. Many papers summarize previous work, but fail to integrate it with new hypotheses or models. For instance, the very formative work of Connell and Slatyer (1977 & Connell et al. 1987) does not refer to the powerful simulation models of Botkin et aL (1972a, b) and Shugart and West (1977), despite the crucial rigour these simula-

tions offer in understanding species interactions during succession (see Discussion; see also e.g. Noble and Slatyer 1980 cf. Connell & Slatyer 1977).

I consider the last point to be one of the most critical: the relationships between different explanatory models for succession are generally vague, making it difficult to frame field studies that make sensible tests. As a result there have been only a few field studies that adequately address the reasons for patterns of species abundance during succession. Reviews of succession tend to be historical accounts of the debate between proponents of a reductionist, individualistic view, and the proponents of a holistic, ecosystem, integrative or facilitatory 'superorganism' view. Reviews often include anecdotal accounts of field work in support of arguments, but have little critical or integrative analysis of the actual models. This approach offers a good understanding of how ideas developed, but not of their utility, and even leads to quite dismal prospects for general understanding of successional processes (e.g. Horn 1976; McIntosh 1981; Finegan 1984; Miles 1987; Shrader-Frechette & McCoy 1990). I feel that a more synthetic approach warrants a much more optimistic view.

Outline and purpose of current review

In the light of these criticisms, the present review attempts a critical theoretical synthesis, with emphasis on integration of useful current understanding, playing down debates and controversies, and avoiding the customary historical order of presentation. I begin by summarizing what I consider the most useful aspects of current successional theory. After outlining what I hope is a useful theoretical basis for ideas on succession, I then discuss other models and theories, and some of the problems, controversies and issues arising from them. I believe that this approach reduces much of the controversy. Final discussion includes the types of theoretical and field research that might most usefully draw upon present understanding.

I am concerned here with understanding the causes of succession at the community level, and focus on models relevant to that understanding. I examine these models for insight into the primary question: "Why do different patterns of species abundance occur during autogenic succession, once a disturbance has freed sites for colonization?" Subsidiary questions include: "What can cause one species or group of species to be displaced or dominated by another or others?" and "What effects do earlier species have on the success of later species?" Different models have different purposes, and hence achieve different ends (and these differences are not always intentional or explicit). In asking these questions my perspective is that of a field ecologist who requires rigourous, testable hypotheses about ecological processes, and who seeks explanation in the interactions between organisms and their environment. Thus my criteria, discussed later, are different to those of either theoretical mod- ellers or applied ecologists, and further reflect subjective opinions about which aspects of succession need explanation.

I generally limit the review to mechanistically (or causally) based understanding of community level, autotrophic, autogenic succession on fairly spatially homogeneous sites, after extrinsic disturbance, and excluding major disturbances during the course of the succession. Although some of these are clearly unrealistic limitations, and the approach very reductionist, they allow the isolation of factors that can cause succession in such limited conditions. Such factors may then be in- corporated into more complex, integrative models. For similar reasons, the review examines succession as expressed by the major structural species in communities, and ignores other community elements.

Ideally, this review would be followed by a critical review of extant field evidence, to test the relevance in nature of the present argument. However, such a dual review is beyond the scope of the current paper, and I feel that it is not constructive to assess further the applicability of models without first establishing a clear, consistent, theoretically rigourous, and biologically in-

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terpretable model. Models which are internally inconsistent or vague are less able to produce tests with useful biological conclusions, and in fact can delay understanding (Loehle 1988, 1990; Shrader-Frechette & McCoy 1990). Thus, I am assessing the models on their perceived theoretical biological merit alone, and not on field evidence.

To present the ideas as clearly as possible, I defer discussion of successional concepts, defini- tions and categories until later in the review, but several points should be made beforehand. In this paper, succession is taken to refer to (directed) changes in vegetation composition in time, in response to external changes or disturbance, and autogenic succession is that succession which occurs independently of continuing change in external environmental conditions (although in response to some discrete, initial, external disturbance). Successional patterns that involve sequential replacement of species are called sequential succession. The term community is used simply to describe an assemblage of individuals, and dominant is used to imply high relative abundance, without necessarily a competitive connotation. Although the concepts of successional climax and stable endpoints are widely discredited, this does not devalue understanding the dynamics of successional change. Rather, frequent disturbances imply that successional processes are all the more important. Thus, the review ignores the issues of successional endpoint or climax stability and patch dynamics, and concentrates on the dynamics of within successional change.

The process of succession: theories and models of causal mechanisms of (autogenic) succession

Resource allocation strategies, tradeoffs and autogenic succession

Synthesis It is almost a biological truism that any organism cannot be simultaneously well-adapted to all environmental conditions, and this is especially true when biological interactions such as competition

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and predation are important. This 'Strategic Re- source Allocation' concept suggests that limitations on the supply and allocation of metabolic resources to different physiological functions generally involves tradeoffs between those functions. A plant that allocates resources to a particular function cannot allocate those same resources to other functions. Thus, for example, resources allocated to rapid accumulation of photosynthetic tissue cannot be allocated to structural growth or disease resistance. Obtaining light requires above- ground tissue, whereas obtaining soil resources requires below-ground tissue, and the most effective allocation of tissue will depend on whether light or soil resources are limiting. The particular balance of allocation to different functions will result in a particular adaptive 'strategy' of the plant, and a particular set of environmental conditions in which it is competitively most successful. Further, strategies or structures that benefit one function can often be directly costly to another (e.g. large size may increase light capture, but also will increase wind damage). Thus there are constraints on and tradeoffs between the adaptive strategies that result from a species' life history traits, and life history traits adaptive to different conditions are likely to be inversely correlated.

Detailed formulations of this concept include the single axis r and K strategies of MacArthur and Wilson (1967); Grime's (1974) two dimensions of stress and disturbance; Tilman's (1982, 1985, 1988, 1990a) above and below ground tissue allocation and resource ratio concepts; classification of species as early or late succession species with an attendant set of presumed traits (e.g. Connell & Slatyer 1977); and Huston and Smith's (1987, Smith & Huston 1989) more general growth rate/resource availability tradeoff. The discrepancies between these ideas, and the detailed nature of the tradeoffs and constraints and their evolutionary aspects need not be discussed in detail here.

A plant's particular strategy, or life history traits, thus determines its success at a particular region of any environmental gradients. If environmental resource or stress levels change in ei-

ther space or time, species composition will probably also change (e.g. Gleason 1939).

The central tenet of this review is that autogenic sequential succession can be explained by certain correlations between life history traits such as growth form, growth rate, and shade tolerance. If these correlations are absent, succession may not involve the sequential dominance by different species, but may form another pattern of species abundances. These correlations are the predict- able consequence of limitations on metabolic resource allocation. Thus, species that have wide dispersal, high recruitment and high growth rates tend to be intolerant of shade, and have low maximum age and height. Species which allocate fewer resources to dispersal and rapid growth, tend to be able to grow in shade and to achieve greater heights and ages.

This correlation suggests the following mechanistic interpretation of sequential succession: Im- mediately after a disturbance makes a site available, species with high colonization and growth rates are likely to rapidly recruit to, and dominate, the site. However, such species will, by their very occupancy, alter the resource levels at the site. For instance, if shade tolerance and colonization are inversely correlated, then these species may be less able to recruit or continue growing in the shade that they themselves produce at ground level. Other species, which have slower growth rates, but can grow in the shade of the early dominants, and can grow to greater maximum size, are likely to eventually emerge from the canopy of early species and shade them. This is likely to prevent further recruitment and growth of the shorter-lived early dominant species, which may then decline, leaving the community dominated by the slower-growing species. This process could then be repeated as species with increasing shade- tolerance and maximum age or height progressively dominate the community, giving a sequence of successional dominants.

It is a matter of common observation (Egler 1954; Drury & Nisbet 1973; Grime 1974; Noble & Slatyer 1980; Tilman 1982, 1990a, b; Huston & Smith 1987; Smith & Huston 1989; Pickett & McDonnell 1989) that in nature these traits are

indeed often inversely correlated. In fact, species are often classified by successional timing, according to a long list of traits, including dispersal mechanisms, responses to disturbance, ability to persist through disturbances by seed bank or vegetative regeneration, maximal height, longevity, resistance to stresses, resistance to small scale disturbances or herbivory, recruitment and growth rates at different resource levels (particularly shade tolerance) (e.g. Odum 1971, Table 9.1).

This interpretation of autogenic succession is simply a sufficient model (Botkin 1981), not an exclusive explanation, and it does not rule out the possibility of other interactions or factors. With or without such correlations in life history traits, other factors also may generate such patterns of species abundances. Species without these correlations may still appear in sequence if, for instance, their timing of recruitment differs. Fur- ther, the detailed expression of this process can and will be modified by numerous factors, including species availability, disturbance levels, history, and, in particular, the effects of different species on each other.

The assertion that correlations in life history traits can explain successional patterns has been, in various empirical or theoretical forms, a common vein in successional theory for a considerable time (see references above), but there has been virtually no tests of the sufficiency of the assertion itself. Tilman (e.g. 1985,1990a, b) has made several valuable theoretical and experimental contributions that support this explanation, but has not directly tested the importance of tradeoffs in general. However, recent simulation work by Huston and Smith (1987) actually provides a clear-cut demonstration of the sufficiency of the concept to explain sequential species replacements during (simulated) succession.

Simulation models by Huston and Smith, Botkin and others Perhaps the most convincing evidence for the importance of correlations in life-history traits stems from the simulations of terrestrial forest succession by Huston and Smith (1987). The most at-

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tractive feature of this work is that they actually test the importance, to the simulated successional patterns, of the correlation between life history traits, using an a priori biological framework. The simulations basically follow individual trees through their lives, modelling birth, growth and death as life history traits modulated by competition for light, which is in turn explicitly and in- dividually modulated by neighbours. This model is explicitly derived from earlier individual-based terrestrial forest simulation models originated by Botkin etal. (1972 a,b: JABOWA model), and more widely developed by Shugart and colleagues (e.g. Shugart & West 1977, 1980 FORET model, see review by Shugart 1984, Ch 1-3). I will concentrate most on the model of Huston and Smith (1987), which is more concerned with explanations of succession than with modelling forest dynamics for applied prediction and management purposes.

Crucial features of these models include: interactions among individuals rather than populations; competitive ability as an individual char- acteristic based on the interactions of life history characters and the individual's environment, rather than abstract parameters for an entire population; non-equilibrium dynamics; and autogenic changes, that is changes induced by the plants themselves, in the critical resources for competition.

As in the earlier work, Huston and Smith (1987) argue that species interactions, such as competition for light, occur at the level of the individual, rather than the population, and hence simulation models should follow individual trees throughout their life. These models thus avoid assumptions of integration to the population level of interactions such as competition, which may affect individuals differently. Botkin and Shugart's models consider the effects on individual growth of resource levels averaged over an entire patch or gap. Huston and Smith, however, model resource availability at the individual level, calculating the effects of neighbours on resources for each tree.

The simulations by Huston and Smith and, to a degree, their predecessors have important fea-

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tures that make them especially attractive models. The models incorporate a priori, rigourous and causal biological concepts. These are: competition, for light and nutrients, based on growth and mortality; recruitment and mortality with stochastic and physiological components; growth based on estimated photosynthetic rates for the particular species at particular light levels; and changes in resource levels in the immediate environment. In fact, competition is not considered in abstract terms, but as the effects of species on resource levels, and of resource levels on species. The models focus on processes, to provide a priori information about similarities and differences at the level of pattern.

Because they are mathematically based simulations, the models' output is quantitative and testable (with limitations) (cf. verbal models discussed later), can be integrated into higher level and larger scale models, and their assumptions are necessarily precise, criticisable and explicit. Assumptions are biologically realistic, and are limited to those needed to reproduce succession (Botkin et al. 1972b): there is no assumption of equilibrium in species interactions, no assumption of integrative competition for a whole population and, most importantly, in Huston and Smith's model there is no a priori assumption of relationships between life history traits such as those attributed to early and late successional species.

This is a crucial point and the unique feature of Huston and Smith's work: minimal initial as-

sumptions generate baseline models of species abundances; this allows the later addition of further assumptions, and hence allows the determi- nation of the consequences of various empirical observations, including the correlation between certain life history traits.

Model results

By 'decoupling' the correlations between traits associated with early and late successional species, Huston and Smith can assess objectively their importance to the (simulated) temporal patterns of species abundances. Using two species and varying combinations of life history traits, the simulations indicate that five patterns of species abundances are possible during regrowth: sequential successional replacement; divergence; convergence; total suppression; and pseudo-cyclic replacements (see Fig. 1).

Sequential succession, which Huston and Smith call successional replacement, involves sequential peaks and declines in abundance of different species. Divergence involves initially similar abundances, followed by fairly stable dominance of some species, and reduction or dis- appearance of others. Convergence means stabilization to co-existing similar final abundances from initially very different abundances. Total suppression implies the immediate and lasting dominance of some species, with other species never achieving significant abundance. Finally, pseudo-cyclic replacement involves the more or less cyclical reappearance of species abundant

Biomass

Sequential Succession

Time

Divergence

k Total

Suppression Convergence "Pseudo-cyclic"

Replacements

Time Time Time Time

Fig. 1. Five different patterns of abundances for two species during succession, as described by Huston and Smith (1987). In simulated successions, Huston and Smith (1987) found that different combinations of life history traits for the two species generated different patterns of species abundances. In particular, sequential species replacements occurred when life history traits such as wide dispersal, rapid growth, and high maximum growth rates are inversely correlated with traits such as high shade tolerance or high maximum size. (Based on Huston & Smith 1987).

earlier. Each pattern of regrowth arises from particular combinations of traits for each species.

The most interesting result is that sequential successional replacements occur when life history traits usually found in early and late successional species are inversely correlated. That is, successional replacements occur when species attributes such as wide dispersal, rapid growth, and high rates of sapling establishment are exclusive of traits such as high shade tolerance or high maximum size (which gives light competitive dominance). If these traits are not inversely related, other patterns of species abundances occur (Hus- ton & Smith 1987).

Such correlations appear common in nature, as already noted, and Huston and Smith do not claim to originate the idea. The significance of Huston and Smith's work lies in taking this idea beyond mere assertion, to a clear demonstration that this correlation in traits can generate successional sequences of species where species are otherwise not sequential (albeit in a simulation). They thus derive the conclusion from first principles, rather than empirically: the model determines the consequences of the empirical observations, rather than interpreting the observations a posteriori.

These results portray a kind of baseline model for sequential succession, based on competition for light, autogenically decreasing substrate light

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levels, and sequential dominance by species that can grow, albeit slowly, in progressively lower light levels. This model is not an exclusive explanation of succession, but rather a simplest case, which demonstrates that complex, facilitative interactions between species are not necessary to generate sequences of species dominance.

Huston and Smith (1987) use their model to examine some other possible factors and aspects of succession, but disappointingly, neither they nor Botkin or Shugart adequately address the controversial issue of net facilitatory or inhibitory effects of early dominant species on later species. There are some relevant results, discussed here, but I argue in the Discussion that detailed examination of species interactions and their mechanisms are called for.

Huston and Smith (1987) expanded their model to include more species, and find that similar successional sequences occur as with two species, even amongst species that all have 'late' successional attributes (see Fig. 2b). They also found that the slower growth rates of the species abundant in later succession cause prolonged coexistence of species, in comparison to earlier succession.

But more interesting is the incidental insight this expanded model gives into species interactions during succession. Understanding the effects of species on each other requires the re-

Biomass

t Time Time

Fig. 2. Simulated removal of early colonist from successional sequence, rearranged and reinterpreted from Huston and Smith (1987). (A) Simulated succession with four species with varying life history attributes. (B) The same succession without species 1. Comparison of (A) and (B) suggests that the early colonist (species 1) was inhibiting species 2, and indirectly facilitating species 4.

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moval of an early dominant species. Such a result can be found by reinterpretation of one of Huston and Smith's results as a simulated species dele- tion (Fig. 2). This interpretation shows that removal of an early dominating species causes a dramatic increase in the growth and dominance of the next dominant, and a delay in the biomass growth of the final dominant. This shows that the early dominant species inhibits the growth of the next dominant species, but (indirectly) facilitates the final dominant.

Huston and Smith's model also can incorporate competition for multiple resources, including water and nutrients such as nitrogen. In particular, they model succession with initially limiting nitrogen levels. Terrestrial primary succession commonly involves initially low nitrogen levels, which increase reciprocally as (sub-canopy) light levels decrease during succession (e.g. Tilman 1982; Walker & Chapin 1986). Huston and Smith (1987) compared simulated species abundances under conditions of high initial light and nitrogen, with conditions of low initial nitrogen (but high light). As expected, with initially low nitrogen, there was a dramatic initial dominance by a nitrogen-fixing species, a concomitant rapid rise in nitrogen levels, followed by a decline in the nitrogen-fixing species. At this point, the pattern converges to that found when initial nitrogen levels are high.

Unfortunately, Huston and Smith did not ex- tend their analysis of nitrogen limited succession to examine the species interactions and to test for possible facilitation of subsequent dominants by the nitrogen-fixing species. Primary succession initially limited by resources other than light, is often considered a likely candidate for 'facilitatory' successional interactions, whereby earlier species actually improve the establishment or growth of later species. It would therefore be very interesting to compare simulated succession with low initial nitrogen levels, with and without a nitrogen-fixing species. This could show clearly whether species that dominate under restored nitrogen levels are significantly affected by early abundance of the nitrogen-fixing species. Obvi- ously, such an interaction could involve facilita-

tion of later species, by excess nitrogen produc- tion, as well as inhibition, by shading by the rapidly-growing nitrogen-fixers. The net effect of these two interactions has been the substance of some of controversy (e.g. Walker & Chapin 1987). It is also disappointing that Huston and Smith have not investigated the consequences of facilitation of colonization, particularly obligate facilitation. Obligate facilitation refers to the inability of a species to establish without the facilitatory effects of earlier species, such as nitrogen-fixers. Huston and Smith (1987) suggest that early colonization would increase the inhibition of later arrivals. Clearly this would only be true if the later colonizers did not depend on the initial colonizers, as they do in obligate facilitation.

Botkin (1981) briefly examined his model's implications for causality and species interactions during succession, particularly the effect of early species on later ones. He ran simulations in which he omitted groups of early species or of late species, and examined the abundance through time of the remaining groups. Botkin argues that in that system, the abundances of later dominants are qualitatively similar with or without early dominants, but that later dominants are quanti- tatively inhibited by the earlier dominant groups: he claims that the earlier dominants affect the abundance of later dominants, but not the timing of the outcome. Botkin's (1981) graphs show that these results are not clear-cut, but it is true that both groups of species appear with similar timing in the presence or absence of the other group. Also, as the early dominants only decline strongly in the presence of the final dominants, it is clear that the later dominants suppress the early dominants. Botkin (1981) interprets this result as showing that the process of sequential succession depends on life-histories alone, a null model (not equivalent to the tolerance model of Connell and Slatyer 1977). Unfortunately, Botkin interprets this result as generally true for forest succession in the field, and as discounting any facilitatory effects of early colonizers on later dominants. Failure to find a phenomenon in one simulated situation is not proof of its general absence.

Tilman's resource-ratio hypothesis The role of competition along gradients of resources has been the subject of an elegant resource allocation model by Tilman (e.g. 1982, 1986a, b, 1988, 1990a, b). Using models of resource availability, Tilman argues that the species able to establish, grow and reproduce fastest at a particular level of the limiting resource will be competitively dominant. In particular, Tilman (e.g. 1990b) argues that species will consume and decrease resource levels to an equilibrium level (R*), at which both population (or biomass) and resource level are at equilibrium. The species that is at equilibrium at the lowest (limiting) resource level should outcompete any others. Tilman em- phasizes the strategic allocation of resources, and the constraints and tradeoffs involved, particularly the tradeoff between below ground tissue (required to obtain soil resources), and above ground tissue (required to obtain light). However, these tradeoffs are an assumption of Tilman's model, whose importance is not tested. The tradeoffs mean that plants will tend to be best adapted to different points along resource gradients, and will tend to sort competitively along such gradients, as discussed earlier.

Tilman (1985, also 1990a) considers that this sorting along resource axes can explain species patterns in successions. He considers that a change in resource supplies, the 'resource supply trajectory', will cause a simultaneous change in the dominance of species. He observed that successional 'resource supply trajectories' often involve the reciprocal decrease and increase of two limiting nutrients. Such trajectories, in which two limiting resources are inversely correlated, will result in a sequential succession (if the dynamics of competition are faster than the dynamics of the resource trajectory). For example, in primary succession, with initially limiting nitrogen levels but high light availability (no canopy species present), species adapted to low nitrogen levels will initially outcompete other species. However, as numerous processes inevitably contribute nitrogen to the soil, and their canopy prevents light from reach- ing new recruits, the resource levels change to the relative advantage of species able to grow faster

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in the lower light levels and higher nitrogen levels. These species then outcompete the earlier dominants, and the process continues in this manner. During secondary succession, similar changes in competitive dominance occur simply because the species that can grow faster in the initially high light levels cannot outgrow shade- tolerant species under their own canopy. Al- though this is conceptually similar to previous models, Tilman (1985) was the first to use a formal, quantitative, mathematical model to produce the patterns.

Interestingly, Tilman (1985p. 845) states "changes in resource-supply rates (light and nitrogen) are not assumed to be under the direct control of photosynthetic plants . . . . it is not a model of autogenic succession". Yet his explanation of the generation of the resource supply trajectory is weak without changes wrought by the organisms themselves. Soil light levels are expressly altered by the accumulation of biomass (p. 836), and the suggested mechanisms for changes in the nitrogen levels (p. 835) are largely dependent on biologically derived nitrogen. The model predicts succession in response to changing resource levels, independent of the cause of the changes, but it is primarily directed to autogenic changes. It does not depend on autogenic or facilitatory changes, but in its simplest form it does model them.

Tilman's (1985) model includes the most explicit argument about the reasons for the exclu- sivity of different life history traits as adaptations to different environmental conditions, and the details of the mathematical/graphical model for competitive dominance at different resource levels are elegant. Furthermore, Tilman's (see particularly 1990a, b) hypotheses about interactions between resources and competing species give the most detailed and explicitly mechanistic interpre- tations of real, field successions (as opposed to simulations).

However, despite the clear affinity with the ideas of Huston and Smith (1987), the model makes several interrelated, questionable assumptions. Tilman (1985, p. 846) states that the main difference between his model and the simulation

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models of Botkin et al. (1972a, b) and Shugart and West (1977) is in its simplicity. I would dis- agree. Tilman's is a population level model, which does not clearly explain the origins of changes in resource levels, assumes equilibrium dynamics, and requires that "the rate of change in resource availabilities is slow relative to the rate of competitive displacement" (Tilman 1985, p. 833). Each of these is a critical assumption not made by the dynamic, individual based simulations already discussed. Huston and Smith (1987) point out that population level models (with constant parameters) ignore the potentially important variability in individual responses to competition etc.

The use of population level, equilibrium dynamics has been criticized as unrealistic, in terms of rates of equilibration, and for small population sizes, such as often found in forest patches or gaps (e.g. Huston 1979; DeAngelis & Waterhouse 1987). Although Tilman (1985) gives examples of slowly changing resource levels, it seems likely that many systems, especially successional systems, simply operate too rapidly to achieve or be realistically represented in terms of equilibrium dynamics. There is evidence that the time scales involved in competitive equilibrium dynamics are often considerably greater than those of the successional changes or the changes in resource levels (e.g. Drury & Nisbet 1973). In simulations, initially limiting nitrogen levels and available light levels reach final levels almost immediately, relative to the time course of the species dynamics (Huston & Smith 1987). Although these problems can be partly dealt with (Tilman 1990b), it seems that non-equilibrium models that do not depend on slow rates of change in resources (e.g. Huston & Smith 1987; Botkin etal. 1972a, b; Shugart & West 1980) are at least more general than the equilibrium model proposed by Tilman (1985).

Recently, Tilman (1990a) and colleagues have made detailed field studies that compare the explanatory power of different resource tradeoffs in old-field succession. Although this work makes valuable distinctions between different versions of the resource competition model of succession,

the goal of all of these tests is to identify which of the possible tradeoffs is at work. When the pattern conforms to the predictions of a particular tradeoff hypothesis, this is taken to support the hypothesis. Yet the underlying assumption that there is a particular tradeoff critical to the natural pattern is not critically tested, and such a test may be very difficult. Shipley and Peters (1990) tested and falsified a particular version of the tradeoff hypothesis. However, neither approach tests the null hypothesis of no (critical) tradeoff.

Other models and theories of successional processes

Clements' facilitation based succession Perhaps the most influential work on succession is the copious description and interpretation by Clements (1916 in Clements 1928, 1928). First hand examination of Clements (1928) suggested that Clements' ideas were not nearly as restrictive as more recent interpretation of his work implies (e.g. Anderson 1986; Drury & Nisbet 1973; Noble & Slatyer 1980; Crawley 1986; Miles 1987; Pick- ett & McDonnell 1989). However, Clements' (1928) tone of absolute and didactic generalization does detract from the considerable insight in his work.

Clements (1928, pp. 3 & 6) regarded succession as "the growth or development and the reproduction of a complex organism". This 'superorganism' description assumes a level of discreteness, integration and cohesiveness amongst the constituent species and individuals that appears to have no concrete support (e.g. Gleason 1939; Underwood 1986a; Wiegleb 1989, but see Discussion).

Clements assumed succession to be solely sequential. He considered that sequential dominance arises from dominant species modifying their environment (particularly soil and light) making it less favourable to themselves, and perhaps more favourable to new invaders, so that the new invaders can dominate competitively the earlier occupants (pp. 74, 80). The outcome of progressive 'reaction' (modification of environment by the plants) was considered to be progressive

stabilization, as fewer species could invade the changed environment (p. 98). This argument is supported by the simulation results of Huston and Smith (1987) above, who found that rates of successional changes decreased as succession progresses. Clements' interpretation assumes 'relay floristics', in which successive dominants arrive later than the pioneers, but only vaguely implies obligate facilitation - "plant populations of each (wave) have made conditions fit for the next c o m m u n i t y . . . " (Clements & Weaver 1938, p.71).

Furthermore, although Clements (1928 p. 79) says "The reaction of the community is regularly more than the sum of the reactions of the component species and individuals", he also places considerable emphasis on the role of individual organisms, albeit as elements of a group or stage. Whilst emphasizing the sequential stages in succession, Clements does not expressly assume the composition of these stages to be fixed between different particular sequences. Finally, Clements (1928, p. 147) strongly stresses the unidirectional, exclusively progressive course of succession, to an inevitable and fixed climax, but only in the absence of disturbance. Such generalizations, although perhaps not strictly tenable in the light of patterns such as divergent or cyclical species abundances, do however share clear similarities with presently held views of succession.

Individualistic or stochastic succession: Gleason and Egler Clements' analogies and overgeneralizations drew a strong response from Gleason (1926,1927, 1939), who considered communities to be far more individualistic: the nature of the changes in a site depended entirely on the species composition of a site, assembled by complex and stochastic means, and this resulted in successional courses of largely individual nature. Gleason considered successional communities to be incohe- sive assemblages, and patterns of similarity to result largely from coincident properties of species and similar environmental conditions. Glea- son (1939) argued against both classification of communities into taxa according to common lea-

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tures, and the idea that any particular community functions cohesively as an organism.

This argument was extended in a seminal paper by Egler (1954) who proposed that secondary succession in old-fields may be dictated more by the 'Initial Floristic Composition' of an area than the relay floristics of successively arriving species espoused by Clements. Thus Egler proposed an alternative hypothesis, in which succession is viewed as simply the consequence of different rates of growth of the different species that are initially present at a site. "After abandonment, development unfolds from this initial flora, without additional increments by further invasion (for the purpose of this discussion)" (Egler 1954, p. 415). This view implies that the appearance of a sequence of species is due to the rapid growth of some species eclipsing the growth of other species that later dominate, due to size, longevity and other life history traits. Egler does not clarify why the early species disappear. Note that Egler stated categorically that any real successional trajectory involves both relay floristic and initial floristic composition processes.

It is not commonly recognized that there are two critical differences, usually confounded, between Egler's Initial Floristic Composition model and the Relay Floristics of Clements. The two views differ both in the timing of arrival of later dominating species, essentially an empirical fact, and in the nature of the interactions between species. Unlike Clements, Egler (1954) made no assumptions about the effects of earlier dominants on the success of later dominants, although he did suggest invasion resistance as a possible alternative to the facilitatory interactions assumed by Clements.

Egler's alternative hypothesis raises the possibility of a null model of succession, in which succession is recognized as being potentially the result of life-histories, even in the absence of competition. Thus, although timing may generate succession, such patterns may occur independent of timing and species interactions. But Egler, by failing to separate the issues of timing of arrival and species interactions, did not fully formulate such a null model.

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Egler raised several other issues. He questioned the generality of any successional processes; he suggested the possibility of inhibitory effects; and he assessed the importance of colonization and extrinsic stresses and disturbances. He argued that the assumption of a single, stable endpoint or climax for any site is unproven. Finally, he criticized the term succession as implying saltatory change instead of the often observed gradual change, and suggested the term vegetation development as an alternative.

Drury and Nisbet's Life history based succession In a timely and highly critical review of field evidence against the accepted, 'Clementsian' view of succession, Drury and Nisbet (1973) proposed an alternative view very similar to that of Egler (1954). Drury and Nisbet showed that vegetation patterns of abundance following disturbances include not only successional replacements, but also cycles and divergences. They asserted clearly that "succession on a single site usually involves a sequence of species (rather than simply the growth of the ultimately dominant species) because no one species can dominate the vegetation throughout the period of growth. In other words the basic cause of the phenomenon of (sequential) succession is the known correlation between stress tolerance, rapid growth, small size, short life, and wide dispersal of seed." (Drury & Nisbet 1973, p. 360).

This is essentially the first unambiguous statement of the concept later demonstrated by the simulations of Huston and Smith (1987 - described earlier). However, whilst Huston and Smith provide a simulated demonstration that this is sufficient to explain the process, Drury and Nisbet (1973) state it as a definitive and exclusive explanation of succession, when it was really no more than an (well-conceived) assertion.

Drury and Nisbet drew the inspiration for their hypothesis from the similarities in vegetation sequences in temporal succession and sequences along spatial gradients of environmental stress. They considered that, if different life history strategies are generally mutually exclusive, then "most of the phenomena of succession can be under-

stood as consequences of differential growth, differential survival (and perhaps differential colonizing ability) of species adapted to growth at different points on environmental gradients." (Drury & Nisbet 1973, Summary p. 362).

A large part of Drury and Nisbet's (1973) paper consists of a very critical survey of field evidence relevant to aspects of successional theory. They concluded that the evidence did not support Clements' views, and emphasized that many natural successions are not entirely autogenic. This argument does not negate the need for a mechanism of change in autogenic succession, upon which allogenic changes can perhaps be superimposed.

Grime's description of plant strategies during succession Grime (1974, 1979) proposed a classification scheme of plant life history strategies, based on adaptation to particular levels of disturbance and stress, using stress to mean low levels of resources. This view is similar to that of Tilman, except that it aims to give an absolute and fixed classification to each species, rather than a relative rank depending on resource levels, and that it includes environmental disturbance as well as resource levels. Using the two dimensions of stress and disturbance, Grime classifies environments as low disturbance-low stress; high disturbance-low stress; and low disturbance-high stress. He proposes three extreme strategies for these conditions: that of competitor; ruderal; and stress tolerator, respectively.

According to Grime, observed changes during succession alter the environment from high disturbance-low stress (high resources) to low disturbance-high stress, with a concomitant change in dominant plant strategies from ruderal to stress tolerators. In more productive systems, there is a middle phase of high competition, with low stress and low disturbance. This is essentially an empirical description, with post hoc interpretation. There is little attempt to explain the changes in species composition, except as the implicitly equilibrium response to unexplained changes in the environment, autogenic or other-

wise. The model is thus vulnerable to the same criticisms as Tilman's model, but lacks the explicit and very mechanistic consideration of resource-species interactions that Tilman gives (see earlier). Further, because it assumes plants to have fixed strategies on this two dimensional gradient, it predicts constant successional relationships between any two species. However, the relative adaptive suitability of two species may vary, depending on the particular circumstances (e.g. Smith & Huston 1989).

Connell and Slatyer's 3 mechanisms of successional species interactions Some of the most formative, but perhaps over- extended, ideas on the process of sequential succession were synthesized by Connell and Slatyer (1977). In this paper, they expanded the ideas of Drury and Nisbet (1973) and Egler (1954) to suggest three 'alternative' models of succession: facilitation, tolerance and inhibition. Put simply, "earlier colonists could either inhibit later ones, have no effect, or facilitate them." (p. 1 of a later discussion paper: Connell, Noble & Slatyer 1987). By including 'alternatives' to the previously accepted facilitation pathway, Connell and Slatyer (1977) hoped to improve the possibility of testing the alternatives. They maximised the utility of these ideas by phrasing them as hypotheses, and proposing experiments to test them. The tests of these hypotheses essentially involve the removal of species to compare the colonization and growth of later species with untreated controls.

By directing successional field studies towards experimental comparisons of their specific hypotheses, Connell and Slatyer's (1977)ideas have been seminal for the development of the field for over a decade. However, I believe that these ideas are due for critical re-examination, particularly since they have been and are still the focus of so much field effort. I feel that there are several problems with the 'three-way model' of succession as generally interpreted in field studies, and that the hypotheses put forward by Connell and Slatyer (1977) have now been adequately addressed.

The 'three-way model' is not as simple as Con- nell and Slatyer claim in the original paper (1977)

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and subsequent discussion (Connell et al. 1987). Connell and Slatyer (1977 Fig. 1) propose these three different types of interactions as part of a quite specific and detailed model, in which sequential succession proceeds by one of three exclusive pathways (see Fig. 3). Aspects of both levels, pathway and interaction, are open to criticism.

Some problems with the idea of facilitation, tolerance or inhibition as simple species interactions were raised by Walker and Chapin (1987) and responded to by Connell, Noble and Slatyer (1987). The latter paper suggests that the three mechanisms model only the net effect of an earlier species on a later one; that the mechanisms represent the extremes of a (quantitative) continuum; and that the strengths and directions of these interactions could vary within a successional sequence. Thus an earlier species may have both facilitative and inhibitory effects on later species, and the primary concern is in the overall net effect.

However, these improvements overlook several other points. Connell and Slatyer (1977) do not consider the potential importance of qualitative distinctions of degree in facilitation or inhibition. Facilitation of later species may be sufficiently extreme to appear as obligate facilitation, a condition with quite different implications for succession than the simple increase in rate generated by a mild or non-obligate facilitation. Simi- larly, inhibition may simply slow a sequence of species by competitive inhibition of the colonization or growth by another species, or it may actually prevent the species' occupancy. This difference would affect the mechanism of succession: mild inhibition would allow succession by slow competition, whereas exclusive inhibition would require disturbance for succession to proceed. Thus, the 'continuum' of interactions can include obligate facilitation, facultative facilitation, tolerance, inhibition and exclusive inhibition. Connell and Slatyer (1977, p. 1123) in summary clearly exclude all but obligate facilitation and exclusive inhibition.

Variation in direction or strength of interaction can occur not only within successional sequences

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(Connell et al. 1987), but it could alter within an interaction: it may vary with the densities of the

two species (Walker & Chapin 1987); their life- stages; their relative dominance of the commu-

Facilitation: Tolerance: Inhibition: Pathway I Pathway 2 Pathway 3

Establishment:

Effects of early occupants on Recruitment:

Replacement:

I Disturbance I opens a relatively large space, releasing resources.

I Of those species that arrive in the open space, any that are I able to survive there as adults can establish themselves. I

I

Of those species that arrive in the open space, only certain "early succession" species can establish themselves.

Environment becomes: less suitable for recruitment of "early succession" species; more suitable for recruitment of "late succession" species.

Modification of the environment by early succession species facilitates the growth to maturity of later succession species. In time, earlier species are eliminated

Environment becomes: less suitable for recruitment of "early succession" species; this has little or no effect on "late succession" species recruitment.

I Environment becomes: less suitable for recruitment of both "early succession" and "late succession" species.

Juveniles of later succession species, already present or invading, grow to maturity, despite the presence of healthy individuals of early succession species. In time, earlier species are eliminated.

f

Earlier colonists exclude, suppress or Inhibit subsequent colonists of all species, as long as the earlier colonists persist undamaged and/or continue to regenerate vegetatively.

Continuation: This sequence continues until I This sequence continues until no the resident species no longer I species exists that can invade facilitate the invasion and growth and grow in the presence of the / of other species, resident. /

Long-term or ] At this stage, further invasion and/or growth to maturity can occur only when a resident individual is I Steady State: I damaged or killed, releasing space. Whether the species composition of this community continues to I

change depends on the conditions existing at that site, and on the characteristics of the species I available as replacements. I

Fig. 3. Three pathways of succession according to Connell and Slatyer (1977). In Pathway 1 early colonizers facilitate later species; Pathway 2 involves tolerance; and in Pathway 3 early colonizers inhibit later species. At each stage, further disturbance can return the system to the starting point. (Redrawn from Connell & Slatyer 1977).

nity; season and other timing factors; the size of the disturbance and the length of the interaction in time (Sousa 1984 discusses the importance of context on successional processes). An interaction also may occur indirectly (e.g. Fig. 2; mid- successional rockweeds inhibit late successional mussels by sheltering their predators - McCook & Chapman 1991).

It is perhaps most important to reconsider the nature of successional interactions as species interactions. Facilitation, tolerance and inhibition are essentially empirical descriptions or classifications, without explicit mechanistic bases. Im- plicit bases for each include life history factors, competition, and physiology, but the descriptions are essentially designed to answer the question "What net difference does the presence or absence of the early species have on the success of the later species?" Species removals do not explain how the presence of the early species causes any differences in late species success. This empirical perspective stems from the need for a more complete view of possible interactions than the limited view of Clements (1928) etc, and Connell and Slatyer's (1977) description led to the accumulation of empirical evidence for a range of interactions. However this description should not be mistaken for a mechanistic explanation of the changes in species abundance (but often is e.g. Begon et al. 1986). The basis of each classification is no more than the outcome of the successional step, and as such depends on the process by which succession occurs.

The pathways of community succession according to Connell and Slatyer Connell, Noble and Slatyer (1987) state that their models were not intended as sufficient explanations of succession. Other important factors, such as seed availability and stochastic physical factors were not included (nor intended to be included) in the models, because they only intended to address the empirical question posed above. Yet, their diagram (see Fig. 3 redrawn from Con- nell & Slatyer 1977 Fig. 1) maps out a detailed and exclusive course of succession for facilitation, tolerance or inhibition. The model does ap-

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pear as a complete description and does not indicate the other factors that may be important. The model is commonly described in reviews and introductory textbooks as a complete description. Further, I argue below that each pathway includes incompletely justified assumptions. I will describe these pathways briefly, in the light of their later recognition of the variable nature of these interactions (Connell, Noble & Slatyer 1987). The terms 'early' and 'late' species refer to the type of species, rather than to the timing of settlement.

In each pathway initial colonization necessarily renders the environment less suited for 'early species' recruitment. It is also assumed that "certain species will usually appear first because they have evolved certain 'colonizing' characteristics ..." (Connell & Slatyer 1977, p. 1122). Pathway 1 is distinguished by obligate facilitation by early species: later species are initially unable to colonize the space. Succession results from the absolute changes in recruitment suitability for early and late species: early species cannot persist, and late species are initially excluded. In pathways 2 and 3, early colonizers do not have exclusive ability to colonize the bare space, but any species that would be viable as an adult can colonize. In pathway 2, later species are unaffected by the presence of the early species, and succession results from the loss of recruitment ability of the early species, and the tolerance to changed conditions of the later species. In pathway 3, however, the modifications to the environment make it also unsuitable for late species recruitment, and so as long as the individuals of the initial colonists persist or regenerate vegetatively, they preclude succession.

In pathways 1 and 2, succession will continue until no' species can invade and grow in the presence of the residents, as in pathway 3. At this stage, no further change will occur except when resident individuals die or are damaged. In pathway 3, damage such as herbivory may be selective of the initial dominants, releasing later species from the inhibition, and allowing a successional sequence to occur. Succession also may result from differences in life-span of initial and late species: long-lived species will tend to

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accumulate if they can recruit at all, and may eventually dominate. At any point in each pathway, subsequent disturbances can cause the system to return to the starting point.

These pathways unfortunately depend on several questionable assumptions and distinctions. First, the assumption that initial colonizers ren- der the environment less suited for recruitment of early species is not sufficiently justified: a species that increases levels of a resource (e.g. nitrogen fixers) may improve the net absolute conditions for its own success. Nonetheless it may lose dominance to a species for which conditions are facilitated more - a relative decrease in suitability for the early species. Thus the facilitatory interaction pattern may result from different processes. Such effects on a species' success also could act through growth, not only through recruitment as assumed.

The process suggested for tolerance actually involves two processes: succession through the relative inability of early species to recruit, or the tolerance of growing late species to low resource levels caused by the initial dominants. Such relative increase in the viability of the late species, relative to the early species, is very similar to the process acting in the facilitation described above, except that the late species is not facilitated ab- solutely. On this basis, perhaps facilitation should be exclusively considered to involve an increase in resources, including suitable sites, by an early dominant. This would make facilitation distinct from simple changes in competitive balance that result from differential tolerances to the changed conditions.

Further, the process of succession by longevity in inhibited late species is not qualitatively different to that in the tolerance model. In both cases life history based tolerance to conditions allows competitive success of the late species. The only difference lies in the absolute effect of the occupants on the later species (but see below). For completely inhibited species, succession dependent on differential resistance to disturbance is also essentially dependent on life history based tolerances: herbivore resistance or unpalatability amounts to an investment of metabolic resources.

The only distinction lies in the immediate cause of death of early species: in all processes except complete or exclusive inhibition, the early species is killed by resource competition.

In describing their tolerance model, Connell and Slatyer (1977) use the term 'tolerance' in two different meanings: the tolerance to reduced resource levels (e .g .p. 1122); and, implicitly by comparison to the facilitation and inhibition, the tolerance of or null effect on later species by early species. This is unfortunate, as species that are successful by tolerance to conditions deleterious to others (e.g. shade) are nonetheless likely to do better in absolute terms at higher resource levels. This situation is hence qualitatively similar to the process proposed for (mild) inhibition, but may be confounded with a null model, in which no significant species interaction effects o c c u r .

In summary, these considerations, along with Connell, Noble and Slatyer's (1987) acknowledg- ment of the continuum of interactions, suggest that succession occurs by essentially similar processes in all three situations, and that the facilitatory or inhibitory effects of the interactions are not primary causes but empirical summaries, which describe limits or boundary conditions on the process.

Connell and Slatyer's (1977) paper has been seminal for the majority of (non-forestry) empirical research on community succession, and the explicit recognition of the facilitation-tolerance- inhibition classification was a major contribution. It is a direct result of this work that clear experimental evidence now exists for each type of effect, and that their complexity is now undeniable (e.g. Sousa 1979; Lubchenco 1982, 1983; Turner 1983; Walker & Chapin 1986, 1987; Farrell 1991; McCook & Chapman 1991, in press), if incompletely recognized. Further, the facilitation-tolerance-inhibition classification can provide a mechanistic basis for considering more complex effects. Farrell (1991) has provided a useful model for explaining and predicting the effects of grazers on successional rates, based on the Connell and Slatyer classification. Caswell and Cohen (1991) used a formalized version of Connell and Slatyer's

(1977) classification to examine species diversity and coexistence.

Despite these benefits, I consider that Connell and Slatyer's successional pathways should no longer be considered as a complete model of succession or as an explanation of species abundances. These problems are partly an inevitable result of ambiguity inherent in any verbal or conceptual model that is not formalized or quantitative (but see Caswell & Cohen 1991). Ecological theory may progress by increasing formalization and modification in response to critical theoretical or empirical testing (Loehle 1988, 1990; Shrader-Frechette & McCoy 1990). I believe that there is now sufficient evidence that Connell and Slatyer's (1977) 3 pathways are not conflicting hypotheses but classifications of different possible outcomes, each of which may occur in different circumstance. The concepts in this model have all been confirmed (but rephrased) and further 'tests' of this model appear unnecessary. By focussing on the consequences of these different effects or on more formalized aspects of the causes of species abundance during succession, future work may contribute more than the accumulation of examples of the three interactions. The context of facilitation and inhibition in succession and possible directions for experimental work are considered further in the Discussion.

Horn's Markov&n replacement probability prediction model One model which has been inappropriately used to explain successional changes (e.g. Horn 1981; Begon et al. 1986) is the Markovian probability projection models advocated in particular by Horn (1975a, b, 1976, 1981, see also Usher 1987). These models use estimates of the probabilities of each tree species being replaced by the same or other species. By arranging all such tree by tree replacement probabilities into a 'projection' ma- trix, and multiplying by a vector of the initial species composition, one can project the future composition. Dynamic systems in which transitions between states are described in probabilistic terms are referred to as Markovian processes. Horn estimated the replacement probabilities by count-

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ing the relative densities of saplings of each species under mature trees of each species and as- suming these proportions represent the likely replacements for each species. He used these techniques quite successfully to describe changes in species composition over time in a wood near Princeton, USA.

However, although these models have the potential to provide very useful predictions for applied research, they have two significant and related disadvantages. The first involves the estimates of replacement probabilities; the second involves the lack of theoretical or causal understanding contained in such a model. The model's strength, the undeniable, almost tauto- logical validity, is also its weakness: it is neither testable nor falsifiable.

With the pos sible exception of chaotic systems, the idea that the future state of a system can be predicted based on probabilities is a simple statistical truism. This adds considerably to the model's appeal as a predictive tool. In fact the simplicity of the model may make it most suited for management purposes. However, this structure also means that any predictions are only as good as the estimates of the replacement probabilities used to generate them. As Facelli and Pickett (1990) point out, such estimates either involve enormous data sets, requiring very long time periods, or enormous simplifications. Horn's (1975a, b, 1976, 1981) use of the sapling densities as estimates of replacement probabilities involves considerable assumptions about the importance of life history stages, and the constancy of these probabilities. In applying such a model, there is no measure of its validity. If the model successfully predicts the outcome, this provides no as- surance of the model's validity; if it doesn't, the failure simply reflects on the quality of the estimates of replacement probabilities (or their founding assumptions). The nature of Horn's technique for estimating replacement probabilities based on sapling densities prevents independent tests of the assumptions about the reliabil- ity of the estimates. If the estimates and applications are based on different sites, then the tests confound site with techniques. Further,

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Horn provides no test of the assumptions or of the sensitivity of the model.

The other concern with Horn's model is that it is essentially predictive, not explanatory, and is based entirely on empirical estimates of the replacement probabilities. The interpretation, in causal terms, of the successful application of this model to succession is that succession results from differential probabilities of replacement. This is simply an empirical observation, with little explanatory utility at all. Beyond species composition, the model does not allow manipulations to investigate the importance of different factors to community composition, and assumes equilibrium dynamics. Species interactions and other potential mechanistic factors are an implicit contribution to the replacement probabilities, but are entirely subsumed by the estimates, and hence their contribution cannot be examined. Thus, the structure of the model allows little insight into the processes of succession. Essentially the model treats the mechanisms and processes of succession as a black box, examining output only.

Nonetheless, several properties of the model, as a statistical system, are of interest. In particular, it is a property of all Markovian systems of this structure that the state of the system converges to a constant outcome, independent of the initial state (species composition). Thus, the model predicts that a single 'climax' state should exist for all successional courses based on the same replacement probabilities, and that the initial species composition will make no difference to the stable outcome. Horn (e.g. 1981, p. 30) argues that this convergence is entirely statistical and thus requires no biological cause. However, this ignores the biological basis of the replacement probabilities, and hence the need for a biological interpretation of the statistical consequence. The convergence results from the constant replacement probabilities, a biological assumption.

The assumption of constant values for the replacement probabilities (the Markovity assumption), is probably a significant oversimplification of a complex biological process. In reality, replacement probabilities are affected by recruit-

ment variations, which may change with local density dependence, time, conditions, neighbours, or herbivory and other disturbances. Since in nature, successions do not consistently result in the same climax community composition (Drury & Nisbet 1973), one can assume that these viola- tions of constant probabilities are significant. If replacement probabilities vary significantly, then Markovian models are probably inappropriate for natural successions in general. Horn (e.g. 1976) deals extensively with the considerable evidence for non-convergence of succession, and the im- plication that mathematical non-linearities would create such non-convergence. These non-linearities result from biological properties such as density dependence and disturbances. However, this is just the kind of biological interpretation that Horn denies the need for in convergence. These observations also demonstrate the inadequacy of his assumption of constant replacement probabilities (see also van Hulst 1980). Facelli and Pick- ett (1990) point out that as most forest succession studies are based on interpreting sites of different ages as different points on the same time trajectory, constant replacement probabilities also assume constancy in space as well as time.

Horn also discusses rates of convergence under different conditions of disturbance regimes, regeneration or recruitment, and competitive hierarchies or facilitatory interactions, but the arguments are predominantly intuitive, and inter- pretations of the effects depend on assumptions about the appropriate reference or comparison rate. It is worth noting that although Horn's applications of the model always assume standing trees in the initial species composition, it can be extended by inclusion of replacement probabilities for open space as a non-biotic species (e.g. McAuliffe 1988).

Population dynamics and the vital attributes of Noble and Slatyer Noble and Slatyer (1980) proposed an excellent, qualitative model of vegetation population dynamics, based on strategies. The model argues convincingly that the qualitative dynamics of species (as persistence or extinction) can be predicted

on the basis of certain 'vital attributes', or life history attributes of the population as a whole. van der Valk (1981) used a similar qualitative model to explain vegetation dynamics over several disturbances in freshwater wetlands, although van der Valk's model used life history traits of individual plants rather than of populations. These qualitative models amount in part to the classification of plants into those with similar strategies. However, the purpose of both these models is to describe vegetation dynamics under varying disturbance regimes over longer time scales than individual successions. As such, although their dynamics include successions, they do not address the question of species abundances during succession. Therefore I will not discuss these models in detail, except to comment on the novel approach, and some confusion sur- rounding Noble and Slatyer's model.

In the current context, the interesting feature of van der Valk's and Noble and Slatyer's work is the use of life history attributes of individual plants, or of population vital attributes that are based on the properties of individual plants, to explain patterns at the level of population and long-term dynamics. Empirical observations at the level of individual plants and disturbances lead to mechanistic understanding at the population level across many disturbances. Population attributes, such as dispersal, establishment rate, and longevity amount to strategies, which suit the population to different conditions and disturbance regimes. The models are thus analogous in approach to the explanations of species abundance within succession, based on individual life- histories (see also Shugart 1984). This analogous approach may provide a basis for integration of ideas on 'within-succession' processes with the broader scale of vegetation dynamics over many disturbances.

Unfortunately, the ideas in Noble and Slatyer (1980) are often treated as an explanation of succession rather than vegetation dynamics (e.g. Begon et al. 1986; Anderson 1986), and are often superficially described or poorly related to other ideas. Interestingly, the authors themselves barely relate the work of Noble and Slatyer (1980) on

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vegetation dynamics to that of Connell, Noble and Slatyer (1987; Connell & Slatyer 1977) on successional interactions.

Johnstone's concept of succession as a stochastic interaction between invasion, maintenance and de-

J

cline Johnstone (1986) proposed a conceptual framework in which succession was considered as a stochastic interaction between invasion, maintenance and decline of species at a location, and is observed as the stability or instability in species composition. Johnstone argued that invasion, maintenance and decline are consequences of the biotic and abiotic environment, and provided a qualitative classification of invasion probabilities. Based on Harper's (1977) concept of safe-sites for new species, Johnstone classified barriers to invasion as botanical or non-botanical and selective or non-selective of species, and argues that these two environmentally-derived criteria give rise to four, time-dependent categories of invasion probabilities. Johnstone considers his classification of invasion probabilities as analogous to Noble and Slatyer's (1980) classification of species vital attributes, which he considers a classification of maintenance probabilities. In each case, the interaction between environmental conditions and plant strategies explains invasion or maintenance potentials. Like Noble and Slatyer (1980), Johnstone's ideas refer more to general- ized vegetation dynamics under various environmental conditions, rather than the vegetation response to a specific disturbance.

Johnstone's framework suggests that different patterns of species abundance during succession result from different invasion, maintenance and decline of those species, in turn caused by environmental factors. Whilst Johnstone describes differences in these three processes, the differences are not explained in detail but presumably depend on differences in the environmental factors. I would argue that invasion, maintenance and decline depend on the interaction of those environmental factors with the life-history traits of the species invading etc. Johnstone considers it critical to realise that environmental factors

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cause invasion, maintenance and decline, but are not the direct cause of succession. This distinction may be less important to an explanation of changes in species composition that em- phasizes the properties of the species and their environment, rather than sub-processes of succession.

Johnstone (1986) argues that his framework is a significant improvement because it does not use time as a cause of succession. Since time is a dimension, not a process, it cannot be a cause. However, most of the models discussed in this review use time as a variable to describe succession (in time-course plots etc.) as Johnstone does, not to explain succession. Differences in timing are suggested to cause succession, but these are conceptually similar to Johnstone's time-based classification of invasion probabilities.

Factors which influence succession

I have argued that species life-histories, and competition between species with traits adaptive to different points on environmental gradients are sufficient to account for successional sequences. This does not mean that other processes do not add to, or also contribute to the observed patterns. The argument simply outlines minimal conditions for such patterns (see also Tilman 1985). Besides longevity, size, shade tolerance, and growth rates important species traits may include details of dispersal mechanisms and history, including stochasticity and propagule availability; vegetative regenerative abilities and seed storage properties; herbivore defences and structural defences against physical disturbances.

Moreover it is clear, on intuitive grounds alone, that there are many other factors that are likely to be important in generating particular patterns of vegetation development and to be unique for any particular succession. Clearly, the possibility still exists of facilitatory interactions, whereby some species simply cannot settle an area without the prior influence of other species. Allogenic changes in the environment, such as sediment or soil deposition, will certainly alter the dynamics of

growth and resource competition. Disturbances, either physical or biotic, are likely to alter the course of dynamic interactions, often selectively influencing some members of the community more than others: disturbances commonly considered in the literature are physical events such as fire, weather and waves, predation and graz- ing. Successional courses are clearly influenced by patch dynamic factors such as isolation, spatial heterogeneity, patch size, history, initial conditions and seasonality of patch creation (e.g. Glenn-Lewin 1980; various chapters of Pickett & White 1985).

Discussion

The history of successional theory has been dominated by observations on patterns, and by debates and controversies about the value of various approaches (see e.g. Gleason 1926; Drury & Nisbet 1973 acknowledgements; McIntosh 1981; Finegan 1984; Anderson 1986; Johnstone 1986; Huston & Smith 1987; Miles 1987; Walker & Chapin 1987; Pickett & McDonnell 1989). I consider that much of this controversy and confusion is misplaced, and results from a lack of critical integration of ideas and terminology, from failure to distinguish between related ideas and from differences in purpose or focus of different models. Many models and observations have common bases or assumptions, the recognition of which provides a powerful basis for unification and generalization. Clarification of terminology and classification criteria have been advocated as powerful tools in improving ecological theory (e.g. Loehle 1988).

Concepts, terminology and classification: succession, vegetation dynamics and climax The terminology of succession and vegetation dynamics is imprecise, reflecting the enormous and continuous variability of these processes in nature. The use of discrete classifications or defini- tions for continuous phenomena may be a necessary tool, but has resulted in considerable confusion in succession, as in other fields (Loehle

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1988). The term succession itself, classifications of autogenic/allogenic and primary/secondary succession, the context of succession within general vegetation or community dynamics and 'climax' communities are all attempts to describe processes or states that are intrinsically continuous in nature. These continua need to be accepted for effective research. Ecologists increase their effectiveness by focussing on particular processes or circumstances, but must accept that sharp distinctions are often artificial.

Natural communities exist in a dynamic state of continuous change in response to varying environmental and biological conditions. Within those dynamics, the perception of which depends on the spatial and temporal scale of observation, there is a generally recognizable pattern of response to or recovery from a particular disturbance, although this pattern grades into the general community dynamics at larger scales of observation.

Succession generally refers to changes in species composition and abundance during or following disturbance of a site. However, other authors use a broader definition that includes more general vegetation dynamic processes: "the change in natural systems and the understanding of the causes and direction of such change" (Shugart 1984, p. 5). Pickett and McDonnell (1989, p. 243) focus on terrestrial forests: "Con- temporary usage (of succession) is a near syn- onym of vegetation dynamics when focus is on the decade scale. While some degree of direction- ality is implied, neither monotonic change, progress nor stable termination is nece s s ary." The assignment of a particular time scale by Pickett and McDonnell (1989) is inappropriate, as it excludes many clearly successional processes (including e.g. many intertidal or decomposition successions, or post-glacial biogeographic. changes) and denies much of the ubiquity of succession. Johnstone's (1986) definition of succession as the outcome of loss and retention of species also involves this more general idea of vegetation dynamics.

As the changes involved in response to individual disturbances form distinct patterns, these

changes may be constructively considered as a distinct component of the more general changes and cycles of vegetation and community dynamics. On this basis, I have used succession to refer to the changes in species composition and abundance in response to a particular disturbance, as a distinct subset of community dynamics. As the response to a particular disturbance, succession will often involve directional changes such as an overall increase in biomass or change in life-form. Directional changes refer to a particular succession, and do not assume a unique climax for a site. Clearly the causes of succession are community dynamic processes, and other changes will be superimposed on the successional pattern in response to environmental changes and disturbances at other scales.

Even within the response to individual disturbances, the term succession is commonly used in two different senses: generally as any vegetational change in response to disturbance; or as a saltatory sequence of replacements in species abundances (e.g. Drury & Nisbet 1973 who disap- prove of this definition; Huston & Smith 1987). The latter definition is etymologically more cor- rect, involving successive replacements, but in ecology, the word succession has clearly come to refer to more general response to disturbance, even if such changes are gradual, or do not involve actual replacements of species. Field observations (see Drury & Nisbet 1973) and the simulations of Huston and Smith (1987) suggest that species abundances can form patterns other than sequential replacements, including convergence, divergence, total suppression and cyclic patterns.

The different meanings of succession have both arisen from, and contributed to confusion about the possible processes involved. These difficulties prompted Egler (1954) to suggest the term vegetation development in lieu of succession, but the literature has clearly failed to embrace this idea. Egler's term also has a connotation of organismic development, an association presently best avoided. Even the term 'revegetation' is unsatis- factory, as it excludes many important successional processes based on sessile animals. Whilst

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I am unable to propose a solution to this di- lemma, the importance of explicit discrimination between the two concepts is clear. For this reason, and because I have primarily discussed autogenic processes after disturbances, I have used 'succession' and 'sequential succession' to imply the general processes and sequential changes in abundances respectively.

Because succession is often taken to imply only sequential replacements, arguments tend to be limited to explaining the occurrence of such sequences, instead of considering the wider issue of which patterns follow disturbances, and under what conditions. Too narrow a definition can short circuit the investigation by hiding assumptions about the patterns. It is more constructive to begin with known properties of species and derive the possible patterns of abundances. These more rigourously derived patterns will lend themselves to fewer semantic confusions.

Successions are commonly classified as primary or secondary and as autogenic or allogenic. However, these are artificially discrete classifications of continuous phenomena, based on the kind of disturbances initiating them. The distinction between primary and secondary succession is essentially a distinction in severity of disturbance to the vegetation. A disturbance severe enough to remove all of the biotic material initiates primary succession, all others initiate secondary succession. As the degree of severity of disturbance is clearly a continuum, primary and secondary succession refer to regions of a continuum, with primary succession as an ideal, analogous to an absolute zero.

Similarly, allogenic and autogenic succession may be best understood in terms of the disturbance initiating them. In both cases, biotic interactions cause changes in response to external disturbance. Autogenic succession occurs after a rapid disturbance, allogenic succession occurs during a slow disturbance or change in the environment. The time length of the disturbance relative to the response periods of the vegetation forms a continuum. Effectively instantaneous disturbances initiate autogenic succession. When the disturbance lasts slightly longer, some species can

react and others cannot (e.g. mobile and sessile benthic species responding to seasonal disturbances). A disturbance on a time scale similar to the response times of the whole community initiates allogenic succession. Disturbances on the landscape/historic scale initiate evolutionary successions. Clearly autogenic succession is also an ideal: no site will be strictly free of any external disturbances.

Shugart (1984, p. 115, see also Drury & Nisbet 1973; Johnstone 1986) discusses allogenic and autogenic successions as alternate or conflicting hypotheses, and points out that they are both possible. Such conflict is misplaced: autogenic succession is better considered as an idealized point on a continuous description of disturbance, useful as a baseline model for processes of wider generality.

Confusion also arises when the terms autogenic and allogenic are applied to disturbances themselves (e.g. Shugart 1984, p. 65), as well as to succession, or when autogenic and facilitation- based successions are confounded (Tilman 1985). Johnstone (1986) as sociates autogenic succession with primary succession and 'Clementsian' changes, yet autogenic secondary succession can clearly follow discrete, mild disturbances (e.g. McCook & Chapman 1992).

The concept of a climax, the stable community composition that was considered to exist for any site, has been the source of considerable confusion and confounded arguments. Clements (1928) considered that the inevitable endpoint of any undisturbed succession was a particular, stable and mature climax composition. This idea has been sharply criticized (e.g. Pickett & McDonnell 1989). Drury and Nisbet (1973) raise these criticisms, and also make the useful observation that the original perception of a unique and static climax was developed against a background of static geomorphological theories, and before widespread acceptance of ideas such as plate tecton- ics and continental drift. I consider the issue to be of minimal importance to succession: the processes of succession by no means require the existence of a climax, and given the wide acceptance of the continuously dynamic nature of natural

communities, succession as a process becomes far more important than a putative and rare endpoint to the process. Further, comparisons of original and post successional vegetation compo- sitions are inevitably confounded by historical differences, preventing any valid conclusions about the climax, and making its nature fairly academic.

Types and purposes of models Other theoretical issues relevant to succession include the different purposes of models or explanations, reductionist, holist and hierarchical theory, and recent developments in plant competition (e.g. Keddy 1989; Grace & Tilman 1990; Tilman 1990a) and vegetation theory (Pickett & Kolasa 1989; Wiegleb 1989). As this paper can only touch on each of these issues, I have tried to be explicit about my purpose and criteria.

Many of the conflicts that have arisen in the succession literature may be the result of ambiguity about the purpose or scope of different studies, or the relevant scale or level of analysis. Dif- ferent models are designed, intentionally or otherwise, to achieve different purposes, and may be unsuitable for other purposes. Discussion of types of models generally distinguishes between descriptive, predictive and explanatory models and suggests that there is a hierarchy, such that, for example, explanatory models may predict, but predictive models cannot explain (Pielou 1981; Loehle 1983; Schoener 1986; McGuinness 1988. Note that Tilman 1990a appears to misinterpret Schoener 1986 and equate predictive and mechanistic models). For example, the simple predictive model of Horn (1975a, b) may make it highly suited to applied and management work in the field, but I have argued that its explanatory power is minimal. Similarly, explanatory models are unlikely to provide very precise predictions of specific natural systems.

Different models examine succession in terms of theory and explanation, or of management and applications; at the scales of landscape or individual organisms, and at the levels of population, community or ecosystem. In fact, as suggested for several models already discussed, whether a

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model is explanatory may depend on the level or type of phenomena of interest. Variables studied may be primary quantities such as species densities or may be derived quantities, such as diversity, patchiness, stability etc. Many of the patterns observed are dependent on the spatial and time scale of observation, yet field studies may examine widely divergent scales of process. Simi- larly, some models may be appropriate for examining only a subset of autogenic/allogenic and primary/secondary successions, or particular interactions within a succession (e.g. see Walker & Chapin 1987; Connell et al. 1987). Application of a model out of context will inevitably lead to conflicts. As Shugart (1984) points out, the best model is that best suited to the needs of the study, and no model can hope to explain all aspects of all successions (Tilman 1985). Assessment of a model should include explicit consideration of the purpose of the model, even if the authors themselves are unclear or misguided about their model's purpose.

Further, the explanatory value of a model depends on both the aspect of succession to be explained, and on the perspective of the observer. Connell and Slatyer (1977) explained the different impacts of occupants on subsequent colonization, as they intended, but did not explain different patterns of abundance, as is often stated. The nature of explanation (cf. description or interpretation) has been debated (Shrader-Fre- chette & McCoy 1990; Loehle 1990), but may be at least partly personal. Johnstone (1986) considers reduction of succession to invasion, maintenance and decline to explain satisfactorily succession, whereas Huston and Smith (1987) consider that succession (or invasion etc.) needs further reduction to the specific properties of organisms for satisfactory.explanation.

As stated, the purpose of this review is to assess models as explanations of patterns of species abundance, at the community level, in order to frame testable hypotheses for field study. I am specifically interested in explaining those patterns in terms of the interaction between organisms and their environment.

For this purpose, a minimal explanation of

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natural succession requires four steps: statement of species properties; statement of (minimal) initial conditions and physical parameters; examination of model community behaviour; and testing or comparison with the natural process. In stating the initial conditions and species attributes the author should distinguish between universal and regional, factual and assumed, and correlated and causally related phenomena. These distinctions are important to the applicability of the model.

Further, the most useful model should be based on clear, rigourous, explicit concepts (minimal structures - Pickett & McDonnell 1989) and require few such assumptions; it should be rigourously testable; and it should lend itself to incor- poration in models of more complex structures and processes. Such models would then be a minimal basis for modelling more complex processes, and could predict the importance of a process in natural succession. It is worth noting that the apparent mathematical complexity of the simulation models of Huston and Smith (1987) etc. belie a conceptual simplicity and concreteness not found in any of the other models.

Caution is needed in understanding succession by means of models, especially more concrete models such as mathematical projections and simulations. There is a tendency to confound the model or its outcome with reality. Such confusion may be subtle and largely due to careless word- ing, but it is important to distinguish between results of simulations and results in nature.

Understanding any phenomena in science can be obstructed by over-emphasis on complete generality, and consequent unnecessary conflicts between observations. It is more constructive to examine critically the applicability of components of a theory than to insist on either complete acceptance or rejection ('theory maturation' Loehle 1988, 1990). In particular, attempts to explain completely all successional patterns with a single mechanism, an apparently impossible task, have obscured much potential insight into both general and specific processes. For example the widespread dismissal of facilitation as the prime cause of all successional replacements has tended to

minimize useful consideration of the potential validity or the mechanism of the process (e.g. Peet & Christensen 1980; Botkin 1981; Tilman 1985; Huston & Smith 1987).

Testing of models Unfortunately the extremely long-term dynamics of terrestrial forest systems have effectively ruled out rigourous experimental tests of many models and hypotheses (e.g. Botkin 1981; Horn 1976). Most tests of proposed successional processes in terrestrial forests involve either the reconstruction of historical species abundances, or spatial chro- nosequences. The latter method involves the interpretation of sites of different ages as different time points for a single site. Neither of these methods allow strictly rigourous interpretation of differences in causal terms, as they do not allow manipulations of species etc, and the use of chro- nosequences to estimate successional courses necessarily confounds site with age of site.

Shugart et al. (1981) distinguish between verification and validation of models. Verification refers to the modification of the model parameters to make it consistent with a set of observations, whereas validation procedures involve the testing of the model against a set of observations independent of those used to structure the model.

However, these tests simply test the predictions of the models, not their explanatory power. Goodness-of-fit tests are appropriate to predictive models, but theoretical models require hypothetico-deductive methods (Loehle 1983), such as used by Huston and Smith (1987). I have briefly suggested both benefits and limitations of field tests of the Connell and Slatyer's (1977) classification of succession. Approaches which com- bine tractable field systems with explanatory modelling, such as Tilman's (e.g. 1990a) admi- rable work in oldfields, should prove more theoretically productive.

The forest or the trees: the great successional controversy: Clements, holism, and reductionism Probably the most impassioned and perhaps the least constructive controversy in successional literature has revolved around three aspects of

Clements' (1928) work: the concept of obligate facilitation in succession; the emphasis on development to a stable 'climax' community structure; and community level interactions and holistic community behaviour, exemplified by the analogy of the community as a 'superorganism', whose development parallels that of a developing organism. Particularly troubling is the failure to recognize the independence of these concepts: the evidence against the widespread existence of climax states or integrated community 'superorganism' behaviour do not deny the utility of emergent or collective properties, or preclude facilitation in nature• There is also a tendency to confound Clements' use of large spatial scales or ecosystem level processes with his often holistic perspective•

In reviewing Clements' work, I argued that much of the controversy over Clements work fails to recognize the strong kinship his ideas had with the more reductionist ideas currently in vogue• I gave several examples of such kinship, and ex- pand on one below. The emphasis on Clements analogy of the community development in succession with that of an organism has drawn attention away even from the more important issue of emergent, holist properties and from the emphasis on individual species traits that also per- vades his work.

This dual emphasis may be seen in his discussion of 'reactions': "The reaction of the community is regularly more than the sum of the reactions of the component species and individuals. It is the individual plant which produces the reaction, though the latter usually becomes recognizable through the combined action of the group • . .A community of trees casts less shade than the same number of isolated individuals, but the shade is constant and continuous, and hence controlling." (Clements 1928, p. 79). This paragraph seems clearly to imply a community property as a collective property of the component individuals. Salt (1979) makes a useful distinction between 'emergent' and 'collective' properties of a group of individuals: the latter can be inferred directly from the components of the system, although not necessarily as a linear summation• In this sense, Clements' overtly holistic paragraph

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may be seen as emphasizing individual contributions. Shading is undeniably a collective property of a stand, and clearly is more (or less) complex than a simple, linear sum of the contributions from individual trees.

The strong polarization between holist and reductionist approaches may be inappropriate. Rather than conflicting, these perspectives may be complementary aspects of an integrative and hierarchical approach to ecological theory, in which higher level phenomena are explicitly derived from, but interact with, lower level structures (Mclntosh 1981; Levins & Lewontin 1982; Allen & Starr 1982; Shugart 1984; Underwood 1986a; Loehle 1988; Wiegleb 1989; Keddy 1989). Loehle (1988) showed that holism is commonly used to describe a widely divergent range of approaches, and can allow for the useful integration from lower levels of theory. Wimsatt (1980) suggested that "reduction in science is better seen as the attempt to understand explanatory relations between different levels of phenomena, each of which is taken seriously in its own right." Indeed, the most explanatory models of succession are those that are most explicitly reductionist, based on physiological properties of the plants, yet these models are probably also the most integrative and useful at higher levels.

These ideas are somewhat abstractly formalized by Pickett et al. (1989) and Pickett and Mc- Donnell (1989)who suggest the existence of particular 'minimal structures' or appropriate minimal levels of reduction for understanding a higher level structure. In much the way that the above simulation models have done, Pickett and colleagues suggest the derivation of higher level properties from sets of basic and explicit concepts, and that if the minimal structure chosen is suitable then the higher level structures will be explained adequately and without conflict. Inap- propriate choice of basic structures or inappropriate integration will generate conflicts and in- adequate explanations.

Thus, Botkin (1981), and Huston and Smith (1987) suggest that individual trees are the most appropriate unit for modelling forest succession, and that community and even ecosystem and

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landscape level properties are best derived from the results of such models. These models derive the community properties from explicit consideration of growth rates and similar physiological level properties, but do not deny the importance to individuals of integrative or collective properties of the community. Allen and Starr (1982, p.177) say of the individual-based simulation models: "The individual trees and individual species assert themselves as quasi-autonomous wholes, while at the same time contributing to the vegetation-mediated environment within the stand. It is this dual existence of simultaneous wholeness and partness which is the cornerstone of hierarchy theory..." Similarly, the explanatory power of tree-based simulation models for ecosystem level phenomena may be greater than non- hierarchical, empirical models based on derived properties such as diversity (e.g. Shugart 1984). These considerations support my argument that successions other than autogenic succession can best be understood by starting with a minimal model of autogenic succession processes, and building the individual circumstances of allogen- esis, starting conditions, patch dynamics, and historical influences onto this foundation.

Competition, species strategies, constraints and tradeoffs Some confusion has arisen from the various schemes about species differential adaptation, by life history traits, for different conditions. Such schemes tend to assume particular sets of values for different attributes, or to assume anthropo- centric assessments of severity, which may not be broadly applicable. K selection, competitor, light competitor or 'late' species strategies are commonly considered 'mature' strategies, by association with competitive hierarchy and equilibrium views of community structure. However, such hierarchies may depend on a particular set of conditions (e.g. Grubb 1987), and the equilibrium view of climax community structure has been discredited.

It is more useful to consider the traits of a species case by case as strategies for the particular conditions. Plant strategies probably form a

multidimensional continuum and result in different hierarchies of relative adaptation to each different set of conditions (Huston & Smith 1987; Smith & Huston 1989). Horn (1981 p.35) states "...no absolute statements may be made about any particular species and its presumed adaptation to a given successional status, just as no absolute statements should be made about adaptation in general...The only statements that should be made are comparative ones involving differences between species and differences in successional status at a given time and place."

Several models of succession include species referred to a priori as 'Early' and 'Late' species, and endowed with the set of traits often observed (or assumed) in species of that class. Arguments are then given that suggest that the succession depends on those traits, because the species have them. However, this approach is nearly circular, as the purpose of the model may be to determine whether some species come before others (cf. Johnstone 1986). The choice of species labels car- ries implicit traits, which at least makes critical examination of the model difficult. A better approach is to derive the species 'timing' from its properties, and to use labels such as strategies (e.g. ephemeral; ruderal; or better simple num- bers, i.e. species 1, 2 etc. - e.g. Huston and Smith 1987).

Constraints on or tradeoffs in species life history strategies have considerable potential to improve our understanding of community dynamics (e.g. Keddy 1989; Petraitis etal. 1989; Grace 1990; Austin 1990; Tilman 1990a, b). Tilman (1990a) considers these ideas will provide a uni- fying and simplifying theme for vegetation competition theory, and Loehle (1988, 1990) considers them fundamental ecological principles. That such constraints are important is in a sense a truism, yet they are only recently receiving direct attention, and there have been few tests of their importance (but see Shipley & Peters 1990; Til- man 1990a, b). Indeed there are apparent excep- tions to the generalizations about constraints on possible strategies. A number of unusual species, known as 'superspecies', have rapid growth as well as large size and long life in particular habi-

tats (e.g. Grubb 1987). These species may be dominant throughout the course of a succession, an observation that adds weight to the idea that constraints on strategies are important to sequential succession. Detailed explanations of how such species avoid the restrictions other species face will presumably involve unusual combinations of environmental conditions and plant physiologies. A complete review of ideas on resource allocation strategies and tradeoffs is beyond the scope of this paper, but I advocate their explicit consideration in future experimental or theoretical work on succession.

The importance and nature of facilitation, tolerance and inhibition Much interest has focused on the effect that sequential successional species have on subsequent species, and the importance of such interactions to the successional processes. In reviewing the development of these ideas in the work of Clem- ents, Egler, Drury and Nisbet, and most importantly, Connell and Slatyer, I have questioned the value of facilitation, tolerance and inhibition as bases, causes or mechanisms for succession. I have suggested that these concepts are actually empirical observations, and that rather than being a model for succession, they are, like the entire successional process, a particular aspect of the outcome of interacting individual life-histories.

As such, mild successional interactions may be understood as acting like quantitative moderators of rate of the qualitative successional process that arises from the interacting differential adaptive- ness of different life-histories. Strong interactions, such as obligate facilitation, or complete, exclusive inhibition may be understood as limits, restrictions or boundary conditions on the process. In such a simple case, the rate of growth of a later dominant would increase with the amount of the earlier facilitatory species and decrease for an inhibitory species: the rate would be zero when the density of an obligate facilitatory species approaches zero, and when that of a strong inhibi- tor approaches some critical level.

Horn (1981) suggested that facilitation, tolerance and inhibition are simply statements about

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the comparative life-histories of different species found in association with each other. More specifically, I suggest that these 'simple statements' are 'simple quantitative statements' about comparative life-histories. As reviewed earlier, Botkin's (1981) results for the simulated removal of early or late successional species indicate a variable quantitative inhibition by both early and late species on the other category. It appears that the presence of inhibitory species modifies the dynamics of the other species.

Interpretation of possible facilitatory or inhibitory effects depends on the type of effect investigated. As implied earlier, the test of such effects requires the removal of the putative interactive species (species A), and comparison of the growth or recruitment of the following species (B) with and without the species A. B otkin (1981) outlines a more rigourous design, involving a control un- manipulated plot; a treatment in which species A is removed; and a second treatment in which an equivalent amount of species B is removed. Com- paring the recruitment or growth of B in the two treatments indicates the effect of A on B relative to the effect of B on itself. Inhibition is deduced if growth of B is greater when A is removed than when similar amounts of B are removed. Facili- tation is shown by a decreased growth of B when A is removed, relative to the removal of B. Analo- gous designs are used in studies of competition (Underwood 1986b).

However, I am unconvinced that this is the sole useful interpretation of these interactions. First, many potential effects, particularly fast-acting types of obligate facilitation, may be obscured by any occurrence of species A, before removal. As discussed earlier, it appears that many changes in resource levels occur very rapidly relative to the dynamics of the species involved in that change. This suggests that 'prevention', not removal may be required. Further, if species B were dependent on the initial presence of species A, prevention/ removal of B would be impossible or irrelevant. I consider that the absolute effects of the initial species on later species are also of value to understanding succession, especially early succession, when occupation is low. The question being

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asked is "Would there be more or less of species B if species A had never occurred there?" This question addresses the absolute effects of the species interactions, not the effects relative to those of the affected species itself. Thus both absolute and relative effects of species are of interest. Clear interpretation of results at least requires a distinction between the two effects. The identification of an effect also should state clearly the measures used for species abundance, as these effects may vary between measures such as biomass, growth, recruitment, rates of growth, or cover.

The significance of these effects to the process of succession, particularly simulated succession, also can be detected by manipulating more than simply the species concerned. Modifying the resource levels, or the species dependence on or effects on resources will give insight not available from simple species removals. Such manipulations could include increases and decreases in species densities; the levels of the resource involved in the interaction could be limited or sup- plied in abundance; and details of species traits, such as excess resource generation or resource dependence, could be altered. Such modifications are simple in simulations, and in the field may involve fertilizations or resource removals or buffering; shading and supplementary lighting; and species removals, additions and substitutions of species with slightly different properties. Thus the impact of facilitation on a successional sequence may be examined by removing some or all of the facilitatory species; by removing the facilitated species; by decoupling the increase in resources from the facilitator's success; and by initial artificial supply of the resource.

Finally, the processes generating inhibition and facilitation are of interest. Inhibition is easily understood as the effects of resource depletion, either directly or indirectly. However, facilitation is more difficult to explain without invoking altruistic traits, such as implied by the superorganis- mic facilitation of Clements. The selection of species that facilitate their own demise as a population is quite counter-intuitive, and may account for much of the controversy over the role of facilitation. However, these confusions stem in part

from inappropriate consideration of species as primarily adapted to a successional role, simply because the species is often found in that role (e.g. 'early species'). Such consideration would imply altruism in the facilitatory species.

A more sensible basis for facilitation is provided by patch dynamic concepts and ideas about species strategies as relative and dependent on the particular circumstances. A species may have traits, such as nutrient capture or synthesis, which make it suited to conditions at particular regions of spatial and temporal resource gradients. These traits may coincidentally make it likely to be found during early stages of successions, and perhaps also to facilitate the success of another species. Such a species may be every bit as 'mature' or competitively successful under the conditions to which it is primarily adapted. Under some (or all) circumstances, this species may produce an excess of a limiting nutrient, and will be dominated by other species, but as long as sufficient sites exist in time and/or space, the 'facilitator' will continue to persist on a large scale. This argument amounts to the dynamic niche separation concept central to vegetation patch dynamics, and portrays facilitation as a kind of parasitism ( - + interaction).

However, although these arguments explain the persistence of facilitators, they fail to explain why these species would not be selected to avoid pro- viding resources that otherwise limit their current competitors. For example, nitrogen fixers may be dominated by later species with greater shade tolerance, but only if the nitrogen-fixers leak enough nitrogen to allow such dominance. The only explanation for the existence of such altruistic facilitators is that excess resource provision is an inevitable consequence of the biological processes involved in the species' traits. For example, species suited to spatial conditions where resources are continually removed may need to generate quantities of that resource which result in facilitation of dominants under other circumstances. Alternatively, a species that only exists as an early successional 'fugitive' may provide the facilitatory resource as an inevitable consequence of its strategy. Examples of such circumstances include

structural resources, such as settlement sites for species unable to recruit to bare substrate. For example, on seashores some late successional dominants appear unable to recruit to bare substrate, and depend on the structure of prior occupants for colonization (Turner 1983; Farrell 1991; McCook & Chapman in press). Facilita- tion therefore must be viewed as a redundant but inevitable cost of either spatial or temporal niches (or both).

Conclusions and directions

Reviews of successional processes and their causes tend to be pessimistic about the progress to or even the possibility of generalization of mechanisms, as suggested earlier (e.g. Finegan 1984; Anderson 1986; Miles 1987; Usher 1987; Shrader-Frechette & McCoy 1990). Horn (1976, p. 202) states "The only sweeping generalization that can safely be made about succession is that it shows a bewildering variety of patterns". Whilst less pessimistic about the likelihood of synthesis, McIntosh (1981, p.23) states "An approach to a synthes is . . .would be more likely to occur if the groups . . .were less cliqueish and less prone to as sert their positions within the cloud of their own program."

Loehle (1988, 1990) and Shrader-Frechette and McCoy (1990) recently debated the potential for explanation of succession in terms of the properties of constituent organisms. They disagreed about whether succession is understood with sufficient precision at the community level to be explained by reduction, and about whether community or population phenomena can be explained by organism phenomena, if community/population and organism belong to different types of classification scheme. The first issue may be largely resolved by restricting the discussion to explanations of autogenic succession, by recognition that facilitation, tolerance and inhibition are not conflicting mechanisms of succession (cf. Shrader-Frechette & McCoy 1990p.110), and perhaps by a more critical integration of different ideas about succession. Terminological clarifica-

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tion may also help resolve the second issue: if communities are considered simply as assemblages of organisms at a site, rather than typo- logical (phytosociological) classifications, then community (or assemblage etc) phenomena may be expected to derive from the properties of the component organisms.

I have tried to present a much more optimistic perspective in this review. I have suggested that the support for a potential general basis for autogenic succession is now quite strong, although it is far from proven in nature. This support comes in particular from experimental manipulations in simulation models. I here reiterate and synthesize this perspective.

It appears that various patterns of species occupancy can result from the different life history traits of species adapted to different regions of continua of various resources. In general, limits on the allocation of metabolic resources result in tradeoffs between growth, and specialization for low levels of resources, particularly light. Such tradeoffs result in an inverse correlation between traits that favour species early in revegetation of a site, such as dispersal and rapid growth, and those which favour long term dominance, such as shade tolerance, longevity, height, and resistance to damage. When these traits are inversely correlated, successional replacements will result. Species able to colonize and grow rapidly will invade and dominate a site. However, such species will generally be gradually replaced by species able to recruit and grow better in the low substrate light levels, and able to resist causes of mortality.

However, if for some reason, such a correlation does not exist between species traits, other patterns of species occupancy can occur, including divergent or convergent species densities, cyclic replacements, and complete suppression by single species.

Finally, the detailed expression of this process can be modified by numerous factors, including species availability, disturbance levels, history, and, in particular, the effects of different species on each other. Species traits may result in their preclusion by or dependence on the presence of

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other species, to varying degrees, and with varying degrees of specificity.

This optimistic stance can provide improved direction and productivity for future work. Theo- retical work could concentrate on extending the experimental manipulative simulation work of Botkin (1981) and Huston and Smith (1987), in the same rigourous and mechanistic manner. The importance of particular species traits in particular situations could be investigated by altered longevity, dispersal rates and other aspects of metabolic resource allocation. Particularly needed are tests of the potential effects and importance of inhibition and facilitation, by decoupling different effects of species and their interactions, as discussed earlier. This approach should provide an understanding of the relationships between different successional processes based on functional homology, not simply on similarities in patterns.

There is also a need for expansion of simulation models to examine ideas such as allogenic changes, patchiness, different starting conditions and disturbances. These results would allow integration of patch dynamics, large scale dynamics and disturbance ecology concepts with successional understanding (see e.g. Smith and Huston 1989).

Especially useful would be construction of similarly powerful and experimental models for systems other than terrestrial forests, and particularly for systems more amenable to experimenta- tion and rigourous field testing. Such extensions should allow more understanding of the generality of successional processes, should improve integration of field work with theory, and, as suggested, should improve the testing of models.

Concentration of field studies on relatively simple species assemblages, with rapid dynamics, small scale spatial interactions, and species amenable to manipulation will improve the opportu- nities for rigourous tests of hypotheses. Obvious candidates for such work are rocky seashores (e.g. Farrell 1991; McCook & Chapman 1991, in press), saltmarshes (e.g. Bertness 1991) and other wetlands (e.g. Shipley & Peters 1990), and old- field grassland communities (e.g. Tilman 1990a).

However, field studies also would benefit from

a more rigourous basis in current theories on succession, resource allocation strategies, plant competition and vegetation theory. Further theoretical or experimental criticism of Clements' 'traditional views of succession' seems unnecessary. As a new tradition of criticizing Clements appears well established, future work may now focus on more constructive directions. Evidence for both valid successional facilitation and inhibition, and for the complexity of these interactions, is now sufficient (e.g. Sousa 1979; Turner 1983; Walker & Chapin 1986; Farrell 1991; Mc- Cook & Chapman in press). Although an essen- tial distinction, further tests of Connell and Slatyer's (1977) three pathways as alternative hypotheses seem unnecessary. Investigating the conditions likely to result in facilitation or inhibition is also unlikely to be useful, except in the context of interacting life-histories. However, understanding the consequences of facilitation and inhibition for other effects, such as herbivory, should be valuable (Farrell 1991).

These considerations emphasize the need for integrated theoretical and field work in more amenable systems, and especially for a rigourous review of extant field research findings, in the light of the emerging understanding of successional processes. It is critical, but challenging, that such reviews be more than anecdotal accounts of examples of different influences. A systematic and critical review is needed to examine the degree of solid evidence for different processes, with explicit consideration of the quality of the results. Although illustrative reviews (e.g. Drury & Nisbet 1973) serve very important functions, a thorough survey will provide a far more complete picture.

In conclusion, I have considerable optimism about understanding of the causal bases for succession. Considerable consensus exists in theoretical considerations of successional processes, despite the confusion and controversy in both the theoretical and field literature. These ideas, if borne out by future work, should form a strong basis for improving understanding of, and applications to, broader vegetation dynamic issues, at population, community, ecosystem and landscape

levels. Given an integrative yet rigourous approach to both theoretical and field studies, the prospects are good for understanding succession and revegetation processes.

Acknowledgements

Critical and thorough comments and discussion by A. R. O. Chapman, S. Walde and especially two anonymous reviewers markedly improved the content and tone of this manuscript, for which I am very grateful. I also thank J. H. Connell and S. Swarbrick for helping to clarify some of my ideas. However, I am solely responsible for any remaining shortcomings in the review.

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