Models, mechanisms and pathways of succession

Abstract

The study of succession has been hampered by the lack of a general theory. This is illustrated by confusion over basic concepts and inadequacy of certain models. This review clarifies the basic ideas of pathway, mechanism, and model in succession. Second, in order to prevent inappropriate narrowness in successional studies, we analyze the mechanistic adequacy of the most widely cited models of succession, those of Connell and Slatyer. This analysis shows that models involving a single pathway or a dominant mechanism cannot be treated as alternative, testable hypotheses. Our review shows much more mechanistic richness than allowed by these widely cited models of succession. Classification of the mechanisms of specific replacement, called for by existing models, is problematic and less valuable than the search for the actual mechanisms of particular seres. For example, the “tolerance” mechanism of succession has at least two contrasting meanings and is unlikely to be disentangled from the “inhibition” mechanism in field experiments. However, the understanding of particular species replacements through experiment and knowledge of the conditions of a particular sere and species life histories is a reasonable and desirable goal. Finally, we suggest the need for a broad mechanistic concept of succession. Thus, based on classical causes of succession that have survived recent scrutiny, we erect a framework of successional mechanisms. This framework aims at comprehensiveness, and specific mechanisms are nested within more general causes. As a result of its breadth and hierarchical structure, the framework performs two important functions: First, it provides a context for studies at specific sites and, second, is a scheme for formulating general and testable hypotheses. The review of specific successional mechanisms and the general mechanistic framework can together guide future work on succession, and may foment the development of a broad theory.

Full text

Models, Mechanisms and Pathways of Succession
Author(s): S. T. A. Pickett, S. L. Collins, J. J. Armesto
Source:
Botanical Review,
Vol. 53, No. 3 (Jul. - Sep., 1987), pp. 335-371
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THE
BOTANICAL
REVIEW
VOL. 53 JULY-SEPrEMBER, 1987 No. 3
Models, Mechanisms
and Pathways
of Succession
S. T. A. PICKETT'
Department of Biological Sciences
Bureau of Biological Research
Rutgers University
New Brunswick, New Jersey 08903
S. L. COLLINS2
Division of Pinelands Research
Center for Coastal and Environmental Studies
Rutgers University
New Brunswick, New Jersey 08903
J. J. ARMESTO3
Department of Biological Sciences
Rutgers University
New Brunswick, New Jersey 08903
I. Abstract . - --336
Resumen
-.- -336
II. Introduction-..- -- 337
III. Limitations of the Connell and Slatyer
Models
-338
A. Fundamental Concepts
-.. 338
B. Application
of the Connell and Slatyer Models to Complex Seres -341
C. Testability
of the Models
- 345
D. Section Summary
-346
IV. Mechanisms of Succession --347
A. The Mechanism of Facilitation -347
B. The Mechanism of Tolerance
- 349
Current address: Institute of Ecosystem
Studies, Mary Flagler Cary Arboretum,
The
New York Botanical
Garden,
Box AB, Millbrook,
New York 12545.
2 Current address:
Department
of Botany and Microbiology, University of Oklahoma,
Norman, Oklahoma 73019.
3 Current address:
Laboratorio de Sistematica
y Ecologia Vegetal, Facultad de Ciencias,
Universidad
de Chile, Casilla 653, Santiago,
Chile.
Copies of this issue [53(3)] may be purchased from the Sci-
entific
Publications
Department, The New York Botanical Gar-
den, Bronx,
NY 10458-5126 USA. Please inquire as to prices.
The Botanical Review
53: 335-371, July-Sept.,
1987 335
C 1987 The New York
Botanical Garden

336 THE BOTANICAL
REVIEW
C. The Mechanism of Inhibition . 353
D. Generalizations About Mechanisms of Replacement -355
V. A Comprehensive Causal Framework - -356
VI. Acknowledgments--364
VII. Literature Cited--364
I. Abstract
The study of succession has been hampered by the lack of a general
theory.
This is illustrated
by confusion
over basic
concepts
and
inadequacy
of certain models. This review clarifies
the basic ideas of pathway,
mech-
anism, and model in succession.
Second,
in order
to prevent inappropriate
narrowness
in successional studies, we analyze
the mechanistic
adequacy
of the most widely cited models of succession, those of Connell and
Slatyer.
This analysis shows that models involving a single pathway
or a
dominant mechanism cannot be treated as alternative,
testable hypoth-
eses. Our review shows much more mechanistic richness
than allowed
by
these widely cited models of succession. Classification of the mechanisms
of specific
replacement,
called for by existing models, is problematic
and
less valuable
than the search for the actual
mechanisms of particular
seres.
For example, the "tolerance" mechanism of succession has at least two
contrasting
meanings and is unlikely to be disentangled
from the "inhi-
bition" mechanism in field experiments.
However, the understanding
of
particular species replacements through experiment
and knowledge
of the
conditions of a particular sere and species life histories is a reasonable
and desirable
goal. Finally, we suggest
the need for a broad mechanistic
concept of succession. Thus, based on classical causes of succession that
have survived
recent scrutiny, we erect a framework of successional mech-
anisms. This framework
aims at comprehensiveness,
and specific mech-
anisms are nested within more general causes. As a result of its breadth
and hierarchical
structure,
the framework
performs
two important func-
tions: First, it provides a context for studies at specific sites and, second,
is a scheme for formulating general and testable hypotheses. The review
of specific successional mechanisms and the general mechanistic frame-
work can together
guide future
work on succession, and may foment the
development of a broad theory.
Resumen
La
ausencia de una teoria general sobre la sucesion
ecologica
obstaculiza
el logro de un mayor conocimiento en la materia, crea
confusion en torno
a los conceptos m'as fundamentales de la disciplina, y fomenta el diseiio
de modelos inadecuados. Esta critica tiene como meta el aclarar conceptos
fundamentales
acerca de la trayectoria, el mecanismo, y el modelo de la

SUCCESSION 337
sucesion ecologica. En segundo lugar, intenta analizar la vtilidad me-
canica de los modelos de la sucesion ecologica mas citados tales como el
de Connell y Slatyer. Se sefiala por que aquellos modelos con una tra-
yectoria unica o con un mecanismo dominante no deben considerarse
como hipotesis validas por probar.
Por otra parte, se sefiala tambien la
existencia de una riqueza mecfanica
que va mas alla de lo admitido por
los modelos mas citados. La
clasificacion
de los mecanismos
de reemplazo
esbozados
en los modelos actuales causa
problemas y tienen poca utilidad.
El mecanismo de tolerancia durante
la sucesion ecologica, por ejemplo,
tiene por lo menos dos significados
contrastantes, y muchas veces resulta
dificil distinguir
en pruebas
de campo entre un mecanismo de inhibicion
y un mecanismo de tolerancia.
Un mejor conocimiento del reemplazo
de
una especie-mediante la experimentacion,
conocimiento de las condi-
ciones conducentes a la sucesion ecologica y del largo de vida de la es-
pecie-no obstante, sigue siendo una meta rezonable y legitima. Se su-
braya
la necesidad de un concepto mecanico de la sucesion
ecologica mas
abarcador
y se propone un marco de referencia
para los mecanismos de
la sucesion ecologica que toma en cuenta las causas
clasicas
de la sucesion
ecologica mas escudriniadas.
Este marco de referencia desempefia dos
functiones importantes: provee una estructura
para el estudio de lugares
especificos, y provee un esquema para la formulacion de hipotesis ge-
nerales por probar.
Esta critica tiene tambien como meta el servir como
guia para
futuros
trabajos
en la disciplina que fomenten el disefio de teorias
generales
de la sucesion ecologica.
II. Introduction
The study of succession, though central to plant ecology, has proven
difficult
(McIntosh, 1974, 1980). A number of factors
may have contrib-
uted to this. First, although
there is much information
available on pat-
terns of succession, there is currently
no general theory to organize this
information and to relate pattern and mechanisms. Second, the basic
concepts required to focus successional
study are poorly articulated. Third,
the models that have been recently
proposed, in an attempt to stimulate
study of mechanisms and organize
that information, are of limited scope
or are poorly used in the literature.
No paper
of moderate
length could fully correct these lapses. Additional
observations and experiments on succession are also required. However,
raising the issues and reviewing the literature that addresses these prob-
lems can indicate the state of the discipline, and encourage further work
toward remedying
the lapses. While the time may not yet be ripe for the
elaboration
of a complete theory of succession and vegetation dynamics,

338 THE BOTANICAL
REVIEW
this review and analysis can advance that goal. In order to focus this
undertaking, we orient our review around
the influential paper by Connell
and Slatyer (1977). The problems suggested by that paper or by its use
by other investigators,
illustrate the three lacunae in the study of succes-
sion.
The purposes of this paper are 1) to clarify conceptual and termino-
logical problems concerning
models and mechanisms
of succession,
2) to
demonstrate
with examples from various successional studies the limits
of the Connell and Slatyer
(1977, hereafter
C + S) models as alternative,
testable hypotheses, and 3) to introduce
a general,
inclusive mechanistic
framework for future studies of succession,
a need emphasized by Finegan
(1984).
III. Limitations of the Connell and Slatyer Models
In attempting to fill the need for a theoretical context in succession
studies, Connell and Slatyer
(1977) proposed
that mechanisms of succes-
sion could be incorporated
into three alternative,
testable models: facil-
itation, inhibition, and tolerance
(Table I). Facilitation
is the Clementsian
model of relay floristics
(Egler, 1954) whereby early successional
species
modify their environment
and facilitate the establishment
of later succes-
sional species. According to the inhibition model, the initial invaders
(Egler, 1954) regulate
succession so that later successional
species cannot
invade and grow
in the presence of healthy, undamaged early
successional
species. In the tolerance model, floristic changes may be a function of
differential life history
traits and the differential
ability of late successional
species to tolerate initial environmental
conditions. To review the liter-
ature that addresses these models, evaluate the adequacy of the models
and ultimately generate
a broad framework of mechanisms of succession,
we will first define three
fundamental concepts: pathway, mechanism,
and
model. Then we will discuss the application of the Connell and Slatyer
models to complex seres. Finally, we will discuss the testability of the
models.
A. FUNDAMENTAL CONCEPTS
(1) A successional pathway is the temporal pattern of vegetation
change.
It can show the change in community types with time, the series of
system states,
or describe the increase
and decrease of particular
species
populations. A complex successional pathway from the Lake Mich-
igan dune succession (Olson, 1958) serves as an example (Fig. 1).
(2) A mechanism of succession is an interaction that contributes to
successional change. A mechanism is an "efficient cause" in the Ar-
istotelian sense.

Table I
Abstract of the Connell and Slatyer (1977) models of successional mechanismsa
Step Facilitation Tolerance Inhibition
A. Disturbance Open site Open site Open site
B. Establishment Only early species Any species Any species
C. Recruitment
of Early
species disfavored Early species disfavored All recruitment .
later species Later species favored No impact on later species disfavored C'
D. Growth
of later Later species favored Later species grow in All subsequent
species spite of earlier
species invaders inhibited zC
E. Continuation As above until no As above until no more No change in
environmental change tolerant species available intact community
F. Change
only with
disturbanceb To A To A To A
a The steps of each model are sequential. Disturbance
can interrupt
the process at any point, but is indicated
here only at step F.
b Specific
site and species pool determines disturbance
effects
in all models.

340 THE BOTANICAL REVIEW
INITIAL DAMP' UPPER BEACH ERODING DEPOSITING STEEP POCKETS
CONDITIONS DEPRESSION SURFACES CRESTS LEE SLOPES
PHYSIOGRAPHIC FORDUNE __ BLOWOUT
PROCESSES FORMATION INITIATION
MARRAM -
PIONEER RUSH COTTONWOOD SAND REE'j . SHRUBS -- BASSWOOD
VEGETATION MEADOW LITTLE BLUESTEM P
TEMPORARY JACK ARBOR VITAE BALSAM FIR
CONIFERS WHITE PINES
RED
CLIMASX TALL GRASS RED MAPLE BLACK OAK OAKS -MAPLES BEECH HEMLOCK -BIRCHES
PRAIRIE SWAMP `'J
Fig. 1. Alternative
successional
pathways
on the Lake
Michigan
Dunes. Except
for the
physiographic
processes,
no mechanisms
are included.
From Olson, 1958.
Which specific interaction
will be called a mechanism depends on
the level of organization
addressed. At the community level, a mech-
anism of turnover in succession can be a general
ecological process
or interaction
(e.g., competition, predation,
establishment).
As mech-
anisms of change in a community, facilitation, tolerance and inhi-
bition fit this description. However, these mechanisms can also be
addressed
at lower levels of organization. For example,
the interaction
of inhibition may be subdivided into more detailed mechanisms that
encompass the specific environmental resource and stress levels, the
physiology of nutrient uptake and resource allocation by the inter-
acting plants,
and their
resultant architectural
and
reproductive
status.
In studies where both levels of organization must be addressed, we
suggest
that the two corresponding
levels of mechanism be differen-
tiated. The most easily understood and least ambiguous way to do
this is to specify the level of organization under discussion. In this
paper
we will need to speak
of mechanisms
in both general and specific
senses.
(3) A model of succession
is a conceptual construct to explain successional
pathways by combining various mechanisms and specifying
the re-
lationship among the mechanisms and the various "stages" of the
pathway. To illustrate, we reproduce a schematic general model of
succession
(Fig. 2), devised by MacMahon (1980), which is applicable
to many natural
systems. These constructs can have verbal, diagram-
matic, or quantitative
forms.

SUCCESSION 341
LNVIKU~~~ URVIVAL OF DIVER
E RESIDUALS T
, | S ; ~~~E,R
@IG ATI N|
/~~
(R)
su o
( tE., R ar i
IN
P TERACTIONS|
Fig. 2. A generalized model of succession. Boxes represent system states or stages in the
succession (SO, Sl, etc.), diamonds are drivers of the succession, circles are intermediate
variables, and bowties are control gates, some of which are equivalent to Clementsian causes
of succession (Table I). Dashed lines represent information flows. Environmental drivers
(E) and reactions (R) affect control gates at the points indicated. From MacMahon, 1980.
Connell and Slatyer
use "model" in the sense of both mechanism and
model as we have defined them. In their diagram of the three models,
abstracted here in Table I, "model" is used in our strict sense. However,
in their
discussion of mechanisms and
discriminating
tests, they use mech-
anism and model interchangeably.
Much of their discussion of specific
cases of successional turnover is an examination of mechanisms
of species
replacement
in the strict sense.
B. APPLICATION OF THE CONNELL AND SLATYER MODELS TO COMPLEX SERES
In addition to potential confusion of the ideas of model, mechanism,
and pathway, there are several additional concerns in applying the C +

342 THE BOTANICAL
REVIEW
S models to specific field situations. The first question is whether the
individual C + S models account
for the variety
of successional
pathways
encountered
in the literature.
Although Connell and Slatyer
did not ad-
dress explicitly the multiplicity of successional pathways, their presen-
tation of each model as the repeated
operation of a mechanism implies
a particular
pathway. The facilitation model implies a linear, obligatory
succession of stages (Fig. 3a). The tolerance model also implies a linear
pathway, but the earlier stages may not be obligatory.
Finally, the inhi-
bition model implies a pathway
that depends on the frequency
of distur-
bance. If disturbance of high frequency (between
steps D and E in Table
I) occurs,
the resultant
pathway
will resemble
Horn's
(1981) synchronous,
large
scale,
chronic
disturbance
type (Fig. 3c). Alternatively,
if disturbance
occurs
at a lower
frequency (after
step F in Table
I), then an asynchronous,
small scale, chronic disturbance
pathway
(Fig. 3b) is suggested.
The implied linkage
of each C + S model with a specific
pathway
results
in two problems. One is that the variety of pathways
found in nature
is
larger
than the range suggested
by a literal reading
of the C + S models
(Fig. 3, e.g., Horn, 1981; McCormick, 1968; Shafi & Yarranton, 1973).
Second, actual successions may exhibit complex combinations of path-
ways, as shown by Horn's (1981) competitive hierarchy
(Fig. 3d). This
complexity makes it unlikely that the C + S models will represent
the
entirety
of many successions. To be sure, there is nothing in Connell and
Slatyer's
concepts that prevents combining various of their mechanisms
in the study of an actual sere. Indeed some statements
indicate that Con-
nell and Slatyer
intended combining mechanisms:
[T]he
mechanisms
of model 1 apply
in the early
stages of colonization
of very
rigorous
extreme
environments.
Whether
this model applies
to replacements
at later
stages of terrestrial
succession
remains
to be seen.... (1977, p. 1124)
[T]hefirst
alternative
(models
I and 2 rejected)
seems to apply to manyforests
in the intermediate
stages of succession.
(1977, p. 1127)
On the other hand, other of their statements suggest
that a single model
might, in some circumstances,
apply to an entire succession:
The
mechanisms
ofthefacilitation
modelprobably
apply
to most
heterotrophic
successions.... (1977, p. 1124)
It [facilitation]
should
apply
to many
primary
successions.... (1977, p. 1127)
The three models of succession described
earlier are based on three quite
different
views of the way ecological communities
are organized.
(1977, p.
1136)

SUCCESSION 343
a A -B --C E
A
b
B/IC
c ,,A~
B
Fig. 3. Generalized successional
pathways
abstracted from referenced sources.
a. Direc-
tional change
with termination
(McCormick, 1968). b. Chronic
disturbance, asynchronous
and small scale (Horn, 1981). c. Chronic
disturbance, synchronous
and large
scale (Horn,
1981). d. Competitive
hierarchy (Horn, 1981). e. Cyclic (Miles, 1979). A, B, C, D, and E
represent
different plant species. Real successions may be composed of combinations
of
these simplified
pathways.
In some original
sources for these pathways,
mechanisms
were
implied
or stated; thus some are the graphic basis of models in the originals. Here,
however,
we represent
them as pathways only.
Given the immense variety
of actual
successional
pathways,
it is advisable
to recognize that particular
mechanisms and pathways
are not bound to
one another. Rather,
C + S mechanisms and models account for specific
transitions
within a sere.

344 THE BOTANICAL
REVIEW
The second question is whether
the C + S models account for the full
range of successional causes. Recognition of complexity in causality is
required
to answer this question.
Causality
can be construed
in both broad
(explanatory) and narrow
(agent
and effect)
senses (Kuhn, 1977).
Clements
(1916) appears
to have used both broad and narrow senses of causality
in constructing his general
classification
of successional
causes. Clements'
(1916) mechanistic scheme is sufficiently broad to still be useful
(MacMahon,
1980, 1981;
Miles, 1979).
There
are no specific
mechanisms,
either demonstrated
or possible, that cannot be incorporated
within that
scheme. Furthermore,
the scheme is ordered,
exposing
the expected
tem-
poral sequence of interactions. We use that scheme to ask whether the
C + S models address
the entire
range
of causes that contemporary
work-
ers (Miles, 1979) have recognized.
The processes defined by Clements are
(1) nudation, which is the removal of vegetation
by disturbance
on a site
in which succession can occur,
(2) migration,
arrival of organisms
at the open site,
(3) ecesis, the establishment of organisms
in the site,
(4) competition,
the interaction of organisms
at the site, and
(5) reaction, the alteration
of the site by the organisms.
Here we omit "stabilization," Clements' "final cause," because it is a
result
of the other five causes, and because
it reflects
Clements'
belief that
succession was the development of a superorganismic climax vegetation.
In this omission, we accept the arguments
of Gleason (1917), Cooper
(1926), Tansley (1935) and Whittaker
(1951). Furthermore,
we recognize
that "competition"
is not the only sort of interaction of interest.
Not all of Clements' categories of cause are variables that allow dis-
crimination among the C + S models, though all receive some mention
(Table II). The nature of the disturbance
(size, severity, seasonality,
re-
lation to climatic cycles, isolation in space from other disturbances),
is
not discussed
as a factor
differentiating
the models. It is evaluated
relative
to community stability. A brief mention of migration
(propagule
source,
agents,
residual
propagules)
is made
in Connell
and Slatyer's
table 1.
These
omissions might cause the models to be inapplicable,
either
to a particular
succession,
or for
comparing
seres
(see
also Botkin, 1981).
Ofthe Clements-
ian causes, the emphasis in the C + S models is on ecesis, competition
and reaction.
For example,
whether
early
or late successional
species
have
different
competitive abilities, or whether site occupancy is a result of
preemption is a critical switch in the C + S models. Likewise, whether
or not establishment
of later species depends on environmental
modifi-
cation by earlier species is critical. Whether later successional species
establish immediately after disturbance
is also a differentiating
process

SUCCESSION 345
Table II
Correspondence of Clementsian "causes" of succession with aspects of Connell
and Slatyer's (1977) models. F = facilitation, T = tolerance, I = inhibition
Level in
Connell
and Allows differentiation of modelb Considered
as
Clementsian Slatyer a variable
in
causes modelsa F T I models?
Nudation A, F - - - No
Migration B, F - - - No
Ecesis B + - - Yes
Competition D - - + Yes
Reaction C, D + - + Yes
Stabilizationc Irrelevant
a Refer
to Table I.
b A "
+" indicates that a particular Clementsian
cause applies
to one of the Connell and
Slatyer models, a "-," that it does not apply.
c
Omitted from consideration for reasons
given in text.
between facilitation and the other two C + S models, while the nature of
reaction and competition appear
to discriminate between tolerance and
inhibition (Table II).
Each
C + S model allows only one mechanism
(sensu
stricto)
of succes-
sion (including
both competition and reaction
of Clements).
For example,
in stage D of the diagram
of the C + S model (Table I), the facilitation
model allows only environmental amelioration
for later species, the tol-
erance model allows environmental alteration
but with no effect
on later
species, and the inhibition model allows only competitive suppression,
by whatever
species are present,
of subsequent
colonists. It is quite likely,
however, that actual seres show some combination of these mechanisms
(Finegan, 1984). We review examples later in the paper.
C. TESTABILITY OF THE MODELS
Connell and Slatyer present the three models as testable alternatives.
The models have been used in that way in both experimental
and de-
scriptive studies (e.g., Armesto & Pickett, 1986; Debussche et al., 1982;
Glasser, 1982; Harris
et al., 1984; Hils & Vankat, 1982; Houssard et al.,
1980; del Moral, 1983; Sousa, 1984; Turner, 1983). Quinn and Dunham
(1983) present
a theoretical
analysis of the testability
of C + S models as
they are most often construed in the literature.
The existence of intran-
sitive competitive relationships, indirect
interactions
among
species
with-
in a sere, and species-specific
mechanisms of interaction,
may all mitigate
against
the models being clearly
differentiable
alternatives
(Botkin, 1981;
Quinn & Dunham, 1983). They can serve as testable hypotheses of the

346 THE BOTANICAL
REVIEW
mechanism of particular
species replacements, but cannot explain the
multispecies sequences that succession often entails. Because, as Quinn
and Dunham (1983) among others (e.g., Clements, 1916; Miles, 1979)
note, succession is a multifactored
process, the use of univariate tests
between alternative
causes and effects is likely to be ineffective (see also
Hilborn & Stearns, 1982). Quinn and Dunham (1983) propose a multi-
variate
approach
to understanding such
ecological
processes as succession.
Our hierarchical scheme of successional causes, presented
in Section V,
can serve as a framework
for such multivariate,
mechanistic studies.
An additional
problem
in applying
C + S models as testable
alternatives
is using the tolerance
model as a null hypothesis
(e.g., Quinn & Dunham,
1983). Because the tolerance model cannot be discriminated from the
other two by the unique action of any Clementsian
process (Table II)
it
may appear to be a neutral model. A problem with tolerance as a null
model appears in the work of Hils and Vankat (1982). They could not
differentiate
between
tolerance and inhibition
models based on their
com-
munity-wide experiments. Assuming adequate statistical design of the
experiment,
additional
work on demography
of the interacting
species or
on resource levels and use, would be required to discriminate between
mechanisms of tolerance and inhibition. For instance, adding a late
successional
species to an early
successional
community
(e.g., McDonnell
& Stiles, 1982) may affect
dispersers
or herbivores
and influence the ap-
pearance,
density or growth of other species. A removal or addition ex-
periment
focused on the phenomenon at the level of the community
could
not discern such complicating effects.
Thus, tolerance
should not be used
as a null model. In addition, C + S tolerance might be erroneously
ac-
cepted because some interaction
not exposed by the model is acting in a
sere. An extreme and inappropriate
statement of the view that tolerance
is a null model, is that tolerance
is a "neutral
mechanism"
of succession
(Harris
et al., 1984). It is more valuable
to refer
to a mechanism
as acting
or not in a particular
situation,
rather
than being inherently
neutral.
Later
we give other reasons
for eschewing
the view of tolerance
as a null model.
D. SECTION SUMMARY
Along with their clear value (e.g., stimulation of experimental and
mechanistic approaches
and inclusion of animal effects), the models of
Connell and Slatyer
(1977) have some inherent limitations, which have
not been recognized in various applications. The meaning of "model"
can be confounded with specific mechanisms or pathways. Each of the
C + S models implies a subset of all possible pathways of succession.
More importantly,
all of the major
sorts
of mechanisms
that act in succes-
sion, or processes
that modify the mechanisms in a particular
succession,

SUCCESSION 347
are not included as variables. The Connell and Slatyer models will not
often apply
to entire successional
pathways
but usually
will be appropriate
only when applied to specific mechanisms within a pathway. Finally,
taking these complex models as simple hypotheses, testable for whole
seres, is likely to be unproductive
or misleading.
To prevent inappropriate application of the ideas, we suggest that a
productive approach
to understanding
how succession
proceeds
is to focus
on the specific mechanisms operating
in succession, as did Connell and
Slatyer, but put those mechanisms in the broader environmental and
historical context that can affect their workings
and outcomes. The next
section reviews those mechanisms and gives examples of how they might
operate.
IV. Mechanisms of Succession
Succession is fundamentally
a process of (1) individual replacement
and (2) a change in performance
of individuals. Successional processes
are essentially demographic,
and have complex relations to biotic and
physical
environments. These processes
have profound
results at the level
of community and ecosystem structure
and function.
This view of succes-
sion is an old one (Gleason, 1917), but it has been verified and effectively
used to explain particular
seres only rather more recently (Horn, 1974;
van der Maarel, 1978; Peet & Christensen, 1980; Pickett, 1982). In order
to illustrate the value and limitations of considering
successional
replace-
ment in terms of facilitation, tolerance and inhibition, we present ex-
amples of these specific
mechanisms
in successions
from several different
systems. In presenting those examples we will subdivide the tolerance
mechanism into passive overlap of contracting life histories and active
tolerance
of low resources
resulting
from competition.
Oldfields and mesic temperate
deciduous forests
provide
a large number
of studies of successional mechanisms. Even in these sites, however, no
complete sere has been mechanistically examined. We exemplify the
mechanisms of replacement using whatever cases are available. In fair-
ness, we note that several examples postdate Connell and Slatyer's paper.
There is a need to compare mechanisms in different sites and to examine
the mechanisms throughout individual seres.
A. THE MECHANISM OF FACILITATION
Facilitation may operate through enhanced invasion, amelioration of
environmental
stress or increase
in resource availability. This expands on
Connell and Slatyer's (1977) conception since invasion is considered as
a given in their model of facilitation. A clear example of facilitation
appears
in early oldfield succession at the Hutcheson Memorial Forest on

348 THE BOTANICAL REVIEW
the New Jersey
Piedmont. Small et al. (1971) report
that survival of tree
seedlings in the first year is quite low. Only with the deposition of litter
on the bare soil or a persistent winter snow cover is survival of tree
seedlings
likely. With little or no snow cover, frost
heaving kills most tree
seedlings. This relationship is reflected in the high mortality of woody
plants in the first few years after establishment
(Pickett, 1982).
The establishment
of trees in a Michigan
oldfield has been found to be
enhanced by a precedent species. Rhus typhina, a sumac, increases the
survivorship of trees by thinning the dense herbaceous cover that had
formerly excluded tree seedlings (Werner
& Harbeck,
1982).
This example
illustrates a problem in applying
the terms facilitation,
inhibition or tol-
erance to whole successions. The successful
establishment of trees in the
herbaceous community was prevented or inhibited by the dense herb
cover until Rhus invaded. Thus, part of the entire interaction, which
involves three
different life forms,
is inhibitory
(grass-tree
seedlings),
while
part is facilitative (Rhus-tree
seedlings). Labelling
the entire interaction
as one or the other seems fruitless.
Indeed, Connell and Slatyer's
step C
in the facilitation model (C + S fig. 1) recognizes the compensatory
trade-off
between the mechanisms of facilitation and inhibition.
A similar
pattern
occurs
in grasslands
in the prairie-forest
border
region.
In the absence of fire, woody vegetation may invade and dominate late
in succession (Bragg & Hulbert, 1976; Collins & Adams, 1983). Petranka
and McPherson
(1979) demonstrated that the establishment and growth
of tree seedlings
during
succession
was enhanced
by the presence of Rhus
copallina. Few tree seedlings occurred
in the prairie
surrounding
clones
of Rhus. Within clones, tree seedlings were more abundant, light was
reduced below the tolerance levels of many grass species, and nutrient
levels were greater
than in adjacent
prairie.
Both examples of interaction
among grasses,
Rhus, and tree seedlings
can be interpreted
variously, depending not only on which member of
the interacting
pair of taxa is examined, but perhaps also on when ex-
periments are performed (P. S. White, pers. comm.). If experimental
removal
of Rhus were
to be performed
after
tree seedlings
had overtopped
the grass
layer
or established
in the thinned
sod, the Rhus
would
be labelled
as an inhibitor rather than a facilitator. Altered timing of experiments
might alter the interpretation
of other mechanisms of turnover as well.
A species-specific
example of facilitation is known to occur in North
American
deserts
(Yeaton, 1978) where
Larrea
tridentata
shrubs
provide
the sites for establishment
of the cactus
Opuntia
leptocaulis.
In arid
zones,
shrubs
directly
modify the environment
beneath
the canopy
(MacMahon,
1981) which may provide adequate
sites for establishment
and growth
of
other species. This phenomenon of nurse plants is widely recognized
in
deserts
(Niering
et al., 1963;
Turner et al., 1966)
and
has also been reported

SUCCESSION 349
to occur
in Mediterranean
shrublands
in Chile (Fuentes
et al., 1984). The
early facilitation of an invader by a nurse plant often gives way to inhi-
bition as the invader matures. This is the case in the example studied by
Yeaton (1978) in which Opuntia eventually contributes
to the demise of
Larrea. This leads to a cyclic succession and, importantly,
indicates that
whether an interaction
is inhibitory or facilitative depends on where in
the cycle it is examined. In a similar case the tree Cercidium
microphyllum
facilitates the establishment
of Carnegiea gigantea but the latter species
eventually outcompetes and replaces
its nurse plant (McAuliffe, 1984).
A final example of facilitation is the enhancement
of invasion of woody
species into fields
by the presence
of other
woody occupants.
The increas-
ing importance of animal-dispersed species during post-agricultural
successions is a widespread phenomenon (Bard, 1952). The role of facil-
itation in this trend has been documented in abandoned orchards in
southern France
by Debussche et al. (1982) and experimentally
demon-
strated by McDonnell and Stiles (1982) in Hutcheson Memorial Forest
oldfields.
Removal of woody stems or emplacement
of artificial,
branched
structures altered the input of bird-disseminated seeds into fields
(McDonnell & Stiles, 1982).
B. THE MECHANISM OF TOLERANCE
Discussion of tolerance
is complicated because the term can be inter-
preted
in two ways. On the one hand, it refers to the ability
of an organism
to endure low resource levels (Grime, 1979). On the other, it refers to
successional turnover
due to organisms having contrasting life histories,
as when a longer-lived, slow-growing species dominates after
a fast-grow-
ing, short-lived species senesces (Connell & Slatyer, 1977). We will call
endurance of low resource
levels the "active"
mechanism
of tolerance vs.
the "passive" mechanism of tolerance through possession of contrasting
life histories. The two interpretations are biologically related.
High rates
of resource use are often correlated with short life-cycle length, early
maturity,
and copious reproductive output (e.g., Pickett, 1976). High rates
of resource use are inimical to tolerance of low levels of resource avail-
ability (Grime, 1979). Likewise, rates of resource use may be related to
competitive ability, with more effective competitors outstripping
the re-
source use of poor competitors.
This complication of the two meanings of tolerance is problematic
because some users of the C + S models consider the tolerance
model as
a neutral
meshing
or complementarity through time (Fig.
4) of contrasting
life histories (e.g., Harris et al., 1984). This interpretation
derives from
the statement
(C + S, p. 1
122) that "the sequence of species
is determined
solely by their life history characteristics." Also step D in C + S fig. 1

350 THE BOTANICAL
REVIEW
states that later species grow "despite the continued presence
of healthy
individuals of early successional species." In contrast, Connell (pers.
comm.) states that Connell and Slatyer (1977) did not mean that inter-
actions were totally absent in the tolerance model, and in fact they do
generalize
that late successional species can shade out early successional
species.
Thus, the tolerance model can be interpreted
in two alternative
ways.
One requires
active replacement
of earlier
by later species through, for
example, exploitation competition. This case is supported
by the state-
ment (C + S, p. 1125) that "this model specifies that later species are
superior
to earlier ones in exploiting resources." The second way to in-
terpret the tolerance model resides in using the term tolerance
both for
the model of turnover and one of the specific mechanisms by which it
occurs. This interpretation
is supported
by the statement
(C + S, p. 1
126)
that "the later species simply survive in a state of 'suspended
animation'
until more resources
are made available by the damage or death of an
adjacent
dominating
individual." This permits interpretation
of the C +
S tolerance
model as one of passive turnover. The contrasting
active and
passive connotations of the term "tolerance" must be recognized
and kept
separate.
In noting the two major implications of the tolerance
model, a signif-
icant difference
between our approach
and that of C + S becomes ap-
parent. Connell and Slatyer (p. 1122) indicate that their interests are
principally
in "the mechanisms that determine how new species appear
later
in the sequence."
Earlier, we noted our
concern
with both how species
acquire
and yield space in succession. We prefer
the more comprehensive
approach
as it ultimately must be employed for a complete mechanistic
understanding of succession.
Several studies in Mediterranean
plant communities suggest both pas-
sive and active mechanisms of tolerance occur during
succession in such
communities.
In France,
Houssard et al. (1980) report
that
"woody
species
belonging to more mature stages of succession colonize very early...."
This may represent the passive case. Seventy-five percent of the species
of the "terminal"
(late successional)
community are present
one year
after
fire in garrigue
ecosystems (Trabaud & Lepart, 1980). In mallee shrub-
lands, seedlings of late successional shrubs are abundant
one year after
fire,
together
with herbs and grasses, but the percent
cover of each species
changes within six years from dominance by porcupine
grass to mallee
shrubs
(Noble et al., 1980). Porcupine
grass is still abundant
in old stands,
suggesting that its replacement as a dominant is the passive result of
increase
in cover of mallee shrubs
(Noble et al., 1980). At the same time,
other herbs are excluded from old stands, which may be due to either
interference
or passive life cycle complementarity.

SUCCESSION 351
w
w
z
cr
o
,
TIME
Fig. 4. Passive tolerance
due to life history meshing. To clarify
the definition
of life
history meshing, we present
diagrammatic
cases. a. and b. Performance
of two species on
the equivalent sites over time in the absence of one another. c. Performance
of the two
species on the same site when together.
Passive meshing of life histories that differ, for
whatever
reason, is shown by the similarity
of the performance
curves of each species in
panels a, b, and c. d. Successional
pattern
resulting
in part from interaction
of the two
species,
and in part
from their
inherently
different life histories.
The cases
where both species
are affected
negatively
or where the later species alone is negatively
affected
by the juxta-
position, are not shown. Conceptually, passive and active tolerance are two ends of a
continuum of interaction.
Tolerance of low resource levels is an important mechanism during
grassland succession. Levels of available nitrogen change during prairie
succession. The N03-N which predominates
in early succession is easily
leached from the soil (Rice & Pancholy, 1972) and requires
more energy
to exploit since it must be reduced to NH3. The late-successional
prairie
species produce significantly
more biomass per unit N on NH4-N than
on N03-N (Smith & Rice, 1983). Detailed studies on permanent
plots
indicate that the late successional
grasses
Schizachyrium
scoparium
and
Andropogon
gerardii
invade shortly
after
disturbance. Their poor perfor-
mance during
early
succession
is due, in part,
to intolerance of low NH4-N
availability in disturbed
areas.

352 THE BOTANICAL REVIEW
The replacement of pioneer
trees by later successional trees in oldfields
appears
to be a particularly
clear
case of differential
tolerance
of resources
driving successional turnover. In general, pioneer trees require higher
levels of light than later successional trees (Bazzaz, 1979; Bazzaz
& Carl-
son, 1982). Thus, seedlings of oaks (e.g., Quercus rubra) can survive
beneath stands
of pioneering
Juniperus
or Pinus (Bormann,
195
3; Kramer
& Decker, 1944; Oosting, 1942), but the seedlings of the pioneers are
intolerant
of any closed canopy. The same applies to beech (Fagus
gran-
difolia) or maple (Acer saccharum) versus the pioneering oaks (Horn,
1971), and is reflected
in the absence of oak regeneration
beneath late-
successional, mesic canopies where seedlings of the tolerant maples are
present
(e.g., Brewer, 1980; Miceli et al., 1977). Active tolerance
may be
a common mechanism
of replacement
because of the differential
demand
for nutrients
(Parrish
& Bazzaz, 1
982a) and water
(Bazzaz, 1979) of early
versus late successional
woody and herbaceous
species. Again, however,
we note that the correlation of life history length, rate of growth and
resource
demand complicate the interpretation
of these cases.
Because the demography
of pioneer stands has not often been moni-
tored, or the causes
of mortality
documented,
the mechanisms
of turnover
are not known. However, the presence
of dead, or moribund
pioneer
trees
in stands of tolerant
species is common (Peet & Christensen,
1980). Cou-
pling such observations
with data on life history and ecophysiology
dis-
cussed above suggests that the passive mode of tolerance does occur.
Replacement results from the rapid growth and death of pioneers while
the later successional species grow relatively unperturbed
by the pioneer
canopy [e.g., Prunus
pensylvanica
(Marks, 1974) in temperate
forests
and
Cecropia
(Bazzaz
& Pickett, 1980) in neotropical
forests].
Passive tolerance
may also contribute
to successional
turnover
because
inherently
contrasting
life histories
dovetail (Fig.
4) especially
during
early
oldfield succession. Summer annuals dominate the first growing season
after spring disturbance,
while winter annuals dominate in the second.
After fall abandonment,
winter
annuals
dominate
the first
growing
season
(Bard, 1952;
Keever, 1950;
Raynal
& Bazzaz, 1975). Similarly,
life history
characteristics
of biennials restrict
them to structural
dominance of old-
field assemblages later than either winter or summer annuals. Keever
(1950) reports that the replacement of early successional and shade in-
tolerant
Aster
pilosus occurs because seedlings of larger
shrubs
and trees
that "appear
in small numbers
along with the first
herbaceous
plants ...
continue to grow in number and size until they in turn dominate the
community" (Keever, 1979, p. 307). Likewise, the replacement
of the
annual Ambrosia artemisiifolia by the biennial Erigeron annuus in early
oldfield succession is the simple result of their different life histories
(Raynal
& Bazzaz, 1975), with neither
facilitation
nor tolerance
involved,
as shown experimentally
by Armesto and Pickett (1986).

SUCCESSION 353
What is observed
as life history
complementarity,
however,
can indirectly
be the product
of species interaction.
Early
successional
biennials
can live
for longer than two years when other species interfere
with their perfor-
mance
(Werner,
1977).
They may flower
only after
reaching
certain
thresh-
olds of size (Gross, 198
1). Peterson
and Bazzaz
(1978) reported
that
Aster
pilosus, which normally
behaves as a short-lived
perennial
requiring
sev-
eral
years
to flower,
behaves as a biennial
or even an annual
when supplied
with high resource levels. Research
into the life histories of a number of
species suggests
that obligate bienniality is rare
(Hart, 1977; Silvertown,
1984). Thus, what might be observed in the field to be non-interactive
meshing of life histories, supportive
of a tolerance
mechanism, might in
fact have an inhibition facet (Fig. 4). The fundamental
caution here is
that of complex, decomposable
causality (Hilborn
& Stearns,
1982).
Rath-
er than classifying mechanisms of turnover into supposedly exclusive
categories,
hypotheses about the use of resources,
role of life cycle com-
plementarity,
and effect of endurance of low resource
levels, for example,
are likely to be more useful in understanding
succession.
C. THE MECHANISM OF INHIBITION
Structural or competitive dominants in a community can prevent the
establishment or ascendancy of later successional species, or, for that
matter, species of any successional status (Connell & Slatyer, 1977). In-
corporating
this concept into the broad framework
of succession is cer-
tainly one of the valuable
contributions of Connell
and Slatyer.
The phys-
iological senescence of a dominant or its death due to an acute biotic or
physical disturbance may open space and free
resources.
The clearest
and
most widely
documented
evidence
for this mechanism
comes from
forests.
In dense mesic forests,
replacement
of canopy
individuals
most commonly
occurs when some disturbance
opens a gap or large patch (Brokaw,
1982;
Denslow, 1980;
Runkle, 1982;
Veblen, 1985).
Although
large
gaps
usually
favor pioneer species, most gaps in mesic forests are small, and late
successional species tend to accumulate
over a sequence of such distur-
bances (Connell & Slatyer, 1977).
In oldfields, disturbance
may relieve competitive inhibition and ad-
vance succession as it does in forests. Many oldfield communities have
several strata and a dense overstory that reduces light and moisture in
the understory.
Opening the overstory can permit the invasion of new
species or enhance the growth of subordinate
species in the community.
The invasion of woody species is encouraged
by certain thinning treat-
ments (Armesto & Pickett, 1985). Gross and Werner
(1982) have also
shown successional
turnover to be advanced by disturbance in oldfields.
In other
cases, however,
depending
on time and size of disturbance,
earlier
successional species persist in the patch (Armesto & Pickett, 1986). A

354 THE BOTANICAL
REVIEW
similar phenomenon occurs in grasslands
where biotic and abiotic dis-
turbances are common (Collins & Uno, 1983, 1985).
The mechanism of inhibition is a complex one. It may in fact grade
into the mechanism of tolerance
depending
on whether
the interaction
is
seen from the viewpoint of the incumbent
or the challenger.
For example,
one reason that
late successional
species
tend to accumulate over relatively
long times is that their
juveniles have the ability to tolerate low resource
levels beneath an inhibitory overstory (Connell & Slatyer, 1977). Such
tolerance should permit the accumulation of late successional canopy
species to be more rapid than allowed simply by their great longevity.
Even the long-lived and highly shade-tolerant
species, e.g., Fagus gran-
difolia, Tsuga
canadensis,
and
Acer
saccharum
require
gaps
to ascend
into
the canopy and do not simply grow slowly up through
the closed canopy
(Canham
& Marks, 1985; Hibbs, 1982; Poulson, pers. comm.).
Inhibitory
chemical substances have been found in many shrub
species
of chaparral
communities in California (Halligan, 1975; Muller et al.,
1964). These substances
may play a role in maintaining
the dominance
of shrubs and restricting
annual herbs to the early stages of succession
after fire. Their real importance in arresting
vegetational change is still
controversial (Bartholomew, 1970). Overstory-understory
relationships
in sclerophyllous vegetation appear to constitute the best examples of
inhibitory
effects.
Gradual
exclusion of understory
species seems to occur
as a result of the sequestering of nutrients
by shrubs
(Kruger,
1983). Cycles
of vegetational
change
are thus related to senescence
of overstory
species,
and confound inhibition with passive tolerance.
An additional
axis of gradation
between
inhibition and tolerance
mech-
anisms lies in the variety of modes of disturbance not considered as
variables
in the C + S models (Table
II).
Disturbance
is commonly
defined
as an event that destroys biomass (Grime, 1979), and alters community
structure
and resource
availability
(Bazzaz, 1983;
White & Pickett, 1985).
The result is the same whether the disturbance is caused by a physical
event originating
outside the assemblage, or is caused by a biotic inter-
action involving resident predators or herbivores, or is caused by the
senescence of dominant individuals. The division between "autogenic"
and "allogenic"
processes is artificial
(Miles, 1979). Successional
turnover
can be due to physiological
senescence
of the dominant or to some physical
or biotic disturbance
independent of the life history of the dominants.
According
to C + S models, the first
case would be labelled as tolerance,
while the second
would be a clear
case of inhibition.
Furthermore,
physical
disturbance
events may have different
effects
on the community depend-
ing on whether the dominant(s) is in a senescent or moribund state. In
such cases, it would be difficult
to assign the turnover to either active or
passive tolerance or to inhibition. The common recognition of alternating

SUCCESSION 355
phases
of stand
deterioration and stand or canopy
consolidation
(Bormann
& Likens, 1979; Odum, 1960; Oliver, 1981; Peet & Christensen, 1980)
suggests
that the interaction of individual life cycles and disturbance
may
be a common but periodic one in succession. This further
suggests
that
a single species may participate
in different
types of turnover
mechanisms
depending on its own life history, the condition of its neighbors, the
presence
and tolerance
of competitors,
and the disturbance
regime,
among
other factors.
For example,
the invasion of Aster
species may be the result
of their own life history patterns
meshing with those of prior dominants
(Keever, 1950), while their demise may be the result
of their being over-
topped by more tolerant, woody species, or taller herbs (Pickett, 1982).
D. GENERALIZATIONS ABOUT MECHANISMS OF REPLACEMENT
The examples of successional
mechanisms
drawn from
oldfields,
forests,
grasslands
and shrublands
suggest
some cautions in the use of the C + S
models and support several generalizations.
(1) One succession may ex-
hibit several mechanisms. Thus, a single sere cannot be characterized
by
one mechanism
and [to the extent that Connell
and Slatyer's
(1977) models
imply a link of specific
mechanisms with a specific
pathway]
neither can
single C + S models apply to a sere. (2) Different
mechanisms of replace-
ment may act in one sere at a given time. (3) One species can participate
in several
mechanisms,
depending on competitive rank
and which
portion
of the sere is under
examination.
(4) The mechanisms can
be discriminated
only by determining
demographic
and ecophysiological
causes of turn-
over. Both experimentation
and observation will be required
but simple
species removal or addition experiments
may not be readily
interpretable
in terms of the three conceptually
distinct mechanisms. (5) Coordinated
work is needed on environmental
change and the demography
and eco-
physiology of successional
turnover.
Because the terms facilitation, tolerance, and inhibition are useful in
describing
particular
interactions
in a sere, as intended by Connell and
Slatyer,
and in emphasizing that succession
proceeds
by a variety of modes
of turnover,
they should
be restricted
to describing
particular
replacements
of species
in succession.
The limitations
of the Connell and Slatyer
models,
and the difficulty
of discriminating the three
types of mechanism,
exposed
in this review, suggests a different
approach.
Understanding
how succes-
sion as a whole occurs would be best served by addressing
the specific
array
of mechanisms
and circumstances
acting
at a time and place rather
than by dividing that suite into classes (see also Finegan, 1984 and Breit-
burg, 1985). In the next section, we present a framework for examining
the mechanisms of succession. The models of Connell and Slatyer can
continue to play an important heuristic role of conceptually
identifying

356 THE BOTANICAL REVIEW
nodes in the vast web of successional interactions, but the distinction
between models and mechanisms must be maintained.
V. A Comprehensive
Causal Framework
Connell and Slatyer (1977) chose to focus on specific aspects of the
successional process. However, the applications
of the C + S models in
the literature have often extended beyond the limits noted earlier. This
indicates a need for broad analysis of successional causes. Because a
complete understanding
of succession must ultimately consider all im-
portant influences on succession, and not just mechanisms of turnover,
we believe it would be valuable to incorporate all causes of succession
in
a complete mechanistic scheme. We build on Clements' (1916) classifi-
cation of successional causes because of its generality
and comprehen-
siveness (Miles, 1979).
While the resulting framework
is not itself a completely elaborated
theory,
it is more than a simple list of successional causes. It is a conceptual
structure
to help organize
various aspects of successional
theory. A com-
plete successional
theory would be a broad
and inclusive conceptual
con-
struct used to understand the process. It would include explicitly stated
assumptions, definition of units and phenomena, generalizations about
trends and relationships, models of various component processes and
phenomena, and it would suggest
hypotheses and predictions.
Space and
the state of the discipline prevent us from elaborating
more than the
mechanistic superstructure
of that theory here. That superstructure is the
causal
framework we derive from the Clementsian
causes. The framework
will be useful in guiding
the development of successional
theory. Specific
models of various successional
processes
and phenomena can be related
to the framework
to determine
their inclusiveness
and generality,
and the
need to link them to other models, concepts, and phenomena. Without
mechanistic inclusiveness, and linkages between different aspects of
successional
process, a complete understanding
will not be possible. Be-
cause
the framework is hierarchically
organized,
theoretical
developments
and empirical work in one aspect (branch
of the hierarchical
tree) or on
one level of generality (order of branching)
can be related to work on
other branches or levels. Without such a framework,
we suspect that
theoretical work on different
aspects of succession will remain isolated.
Furthermore,
in the absence of a framework
the need and strategy
for
theoretical
and empirical syntheses would not be apparent.
There are additional values of adopting a comprehensive
mechanistic
scheme. It need not be biased toward
an endpoint in general,
and certainly
not one in particular. It is not inherently
biased toward
a single or dom-

SUCCESSION 357
inant mechanism or driving force. Finally, it is not married
to any par-
ticular pathway of succession. A mechanistic, "process-oriented"
ap-
proach (Vitousek & White, 1981)
is applicable
to a broad
variety
of biomes
and situations. The mechanistic
framework can incorporate
specific models
and subtheories
that
will generate predictions
for field or other
appropriate
tests. However, we cannot include all detailed subtheories
in this paper.
Indeed, many such subtheories have yet to be developed.
Although we have based our comprehensive mechanistic framework
on the causal scheme of Clements, we depart
from it for several reasons.
Clements' scheme confounds different
levels of generality
in causation.
It
also inappropriately
includes Aristotelian final cause. In addition, some
of Clements' "causes" (Table II) are actually effects (e.g., stabilization)
and others are permissive
conditions (e.g., nudation).
These problems
can
be remedied by creating a hierarchy of causes ranging from the most
general and universal to those that are site- and situation-specific.
The
higher level causes can be decomposed into the more specific,
lower level
causes. We also include formerly neglected
influences
on succession,
such
as herbivory, predation
(Connell
& Slatyer, 1977;
MacMahon, 1980, 1981),
and disturbance (Grubb, 1977; Pickett & Thompson, 1978; Pickett &
White, 1985b; White, 1979).
We begin the mechanistic hierarchy at the most general
level by asking,
"What causes succession?"
The universal answers
are that (1) open sites
become available, (2) species are differentially
available at a site and (3)
species have different, evolved or enforced capacities for dealing with a
site and one another (Table III). These answers
are explanatory and not
predictive, but they apply to all cases, and guide our search for more
specific causes about which testable predictions are possible in specific
sites. These answers also apply to all spatial and temporal scales (e.g.,
Delcourt et al., 1983) of vegetation dynamics and thus emphasize the
commonality of causation
in various processes involving species replace-
ment (e.g.,
seasonal
turnover, post-glacial
migrations),
regardless of whether
they are called succession or not (Pickett & White, 1985a).
The second level of the hierarchy (Table III) is constructed of the
answers
to the question, "What
interactions, processes or conditions con-
tribute to the general
causes of succession?" The answers
are broad cat-
egories of ecological phenomena, which suggest the range of processes
that must be considered to understand
each case of vegetation dynamics.
The third
and most detailed
mechanistic level encompasses site-specific
factors or behaviors that determine the nature
or outcome of interactions
of the plants and other organisms that affect them. These interactions are
the essence of succession. These organism- and site-specific features are
responsible
for
the great variety in the successions we observe. The specific

358 THE BOTANICAL
REVIEW
Table III
A hierarchy of successional causes and references demonstrating the action of
factors in particular successions
General causes Contributing processes
of successiona or conditionsb Modifying factorsc
Site availability Coarse-scale disturbance Size
de Foresta, 1983
Davis & Cantlon, 1969
Denslow, 1980
Curtis, 1959
Miles, 1974
Grubb, 1982
Severity
Malanson, 1984
Monte, 1973
Time
Small et al., 1971
Keever, 1979
Altieri, 1981
Perozzi & Bazzaz, 1978
Numata, 1982
Abugov, 1982
Dispersion
Differential Dispersal Landscape configuration
species availability Forman & Godron, 1981
Livingston, 1972
Olsson, 1984
Dispersal agents
Propagule pool Time since last disturbance
Wendel, 1972
Leak, 1963
Land use treatment
Oosting & Humphreys, 1940
Resource availability Soil conditions
Bard, 1952
Tilman, 1982, 1984
Grime, 1979
Bazzaz, 1979
Robertson & Vitousek, 1981
Robertson, 1982
Chapin, 1983

SUCCESSION 359
Table III
Continued
General
causes Contributing
processes
of successiona or conditionsb Modifying factorsc
Topography
Microclimate
Site history
Differential Ecophysiology Germination
requirements
species performanced Pickett
& Baskin, 1973
Willemsen, 1975
Peterson & Bazzaz, 1978
Grime et al., 1981
Assimilation rates
Wallace & Dunn, 1980
Bazzaz
& Carlson,
1982
Parrish & Bazzaz, 1982a, 1982b
Zangerl & Bazzaz, 1983
Bakuzis, 1969
Growth
rates
Marks, 1975
Bicknell, 1982
Sobey & Barkhouse, 1977
Grime, 1979
Population differentiation
Hancock
& Wilson, 1976
Hancock, 1977
Roos & Quinn, 1977
Life history strategy Allocation
pattern
Horn, 1981
Stewart
& Thompson, 1982
Soule & Werner,
1981
Beeftink et al., 1978
Campbell, 1983
van der Valk, 1981
Reproductive
timing
Baalen
& Prins, 1983
Reproductive mode
Noble & Slatyer,
1980
Smith & Palmer, 1976
Environmental
stress Climate
cycles
Buell et al., 1971

360 THE BOTANICAL
REVIEW
Table III
Continued
General
causes Contributing
processes
of successiona or conditionsb Modifying
factorsc
Site history
Woodwell
& Oosting, 1965
Prior
occupants
Whitford
& Whitford, 1978
Carmean
et al., 1976
Competition Hierarchy
Kramer
et al., 1952
Raynal
& Bazzaz, 1975
Parrish
& Bazzaz, 1982c
Kozlowski, 1949
Presence
of competitors
Werner, 1976
Identity
of competitors
Carvell
& Tryon, 1961
Petranka
& McPherson,
1979
Collins & Quinn, 1982
Werner
& Harbeck,
1982
Within-community disturbance
Gross, 1980
Werner,
1977
Armesto
& Pickett, 1985, 1986
Predators
and herbivores
Berendse & Aerts, 1984
Resource base
Huston, 1979
Maly & Barrett, 1984
Fowler, 1982
Tilman, 1985
Allelopathy Soil chemistry
Jackson & Willemsen, 1976
Rice, 1984
Soil structure
Microbes
Neighboring
species
Quinn, 1974

SUCCESSION 361
Table III
Continued
General
causes Contributing
processes
of successiona or conditionsb Modifying
factorsc
Herbivory,
predation Climate
cycles
and disease Predator
cycles
Schimpf
& MacMahon,
1985
Maarel, 1978
Kirkpatrick
& Bazzaz, 1979
Reader, 1985
McBrien
et al., 1983
Ashby, 1958
Plant vigor
Plant defenses
Community
composition
Smith, 1975
Brown, 1985
Southwood
et al., 1979
Patchiness
Smith, 1975
a The highest
level of the hierarchy
represents
the broadest,
minimal
defining phenomena.
b The intermediate
level represents
mechanisms
of change
or causation
of the higher
level.
c
The lowest level of the hierarchy
contains
the particular
factors
that act to cause
or limit
change
in the second level, and which are discernable
or quantifiable
at specific
sites. For
simplicity,
interactions
among factors
at each level are not shown.
d Consists
of both species properties
and environmental
determinants.
features can be quantified and incorporated into the flow model of
MacMahon (1980) (Fig. 2) and used to predict species replacement
pat-
terns and associated community and ecosystem level phenomena.
The nature and use of the third, most detailed level of the hierarchy
requires some explanation. We present a brief overview rather than a
complete review (Table ILL).
Because we are concerned
with succession,
the availability of open sites is the first component of the mechanistic
hierarchy.
The conditions within open sites depend on the characteristics
of the disturbance
(Connell & Slatyer, 1977; White, 1979). For example,
the size of a disturbance
affects
environmental
conditions and heteroge-
neity within open patches. The severity of a disturbance
(Sousa, 1984;
White & Pickett, 1985) affects
the survival of propagules
and advanced
regeneration,
as well as the openness
of the site. The time of a disturbance,
whether
on the seasonal
scale,
or relative
to the maturity
of the dominants,
can determine whether in fact a particular
site is available to particular
species.

362 THE BOTANICAL REVIEW
The processes
that affect
species
availability
are
dispersal
and the nature
of the propagule
pool. Whether diaspores reach an area will depend on
the features
of the landscape (sensu Forman & Godron, 1981) in which
the disturbed
site is embedded. How large
the opening is and whether
it
is isolated by barriers to biotic or abiotic dispersal vectors, will affect
availability of different potential occupants. Alternatively, species may
be made available through persistence
in the soil seed bank or pool (or
in many cases as advanced
regeneration).
The time since last disturbance
interacts with the depletion rate, through
death and germination,
of the
seed pool. Likewise, the nature and length of the prior disruption
of the
site (land use) will determine the size and composition of the seed pool.
The differential performance
of species that arrive at the open site is
the third general determinant of succession. Differential
species perfor-
mance can be determined
by evolved species characteristics
(Pickett, 1976)
and by interaction
with other species and the changing
environment of
the sere (Bazzaz, 1979). The physiological ecology of the species has
several relevant aspects: germination requirements
(dormancy, stratifi-
cation, light, water, etc.); assimilation rates (photosynthesis,
nutrient and
water requirements); and integration of the assimilation behavior into
whole-plant growth rates and architecture.
Finally, whether the individ-
uals of a species present early in the sere differ genetically or not from
those present later will affect turnover
and structure of the sere.
The life history
differences
among species in a sere
are
important
causes
for their differential
behaviors (Pickett, 1976). That species differentially
allocate biomass and nutrients
to different
components is an important
reason for their different
behaviors in succession. Whether they reproduce
early
in their
lives or not;
whether
they rely
entirely
on sexual
reproduction
or have the capacity
for vegetative spread (Pitelka & Ashmun, 1985); and
the horizontal and vertical architecture
resulting
from these components
of the species strategy, are critical determinants of their performance
relative to other species.
Environmental
stress can differentially
affect performance
of various
species in succession. This item refers to the unpredictable
imposition of
stress
during the succession.
Climate cycles can trigger
droughts and affect
fire
probabilities, for instance. The recent
history of a site may determine
whether the soil is capable of storing water or supplying nutrients to
different
degrees. The identity and performance of species occupying the
site before initiation of the present sere may affect the availability of soil-
mediated resources, or the existence of safe sites. To the extent that
different
species are differentially tolerant of the stresses,
resources, and
opportunities presented throughout a sere, these factors and processes
outlined above will determine, in part, the course and rate of succession.
The direct ecological interactions among organisms, which determine

SUCCESSION 363
the progress
of succession can include, at the least, competition, allelopa-
thy, predation and herbivory. Various mutualistic interactions can be
considered under the specific resource
or life history feature
they affect,
or be grouped
as a class along with the various interactive
processes
listed
here.
Competition will affect succession if species differ
in their competitive
rankings
(Connell & Keough, 1985). If competitive hierarchies are
absent,
transitive,
or cyclic, then the course of succession
may differ.
Specifically,
the presence
of competitors
and their identities at various stages
must be
known to understand
the role of competition in a succession. Whether
the small-scale component of the disturbance regime, that which acts
within a community without obliterating
it, has a different
impact on the
species in the sere must be known. Predators and herbivores can be
considered a within-community component of the disturbance regime
(Denslow, 1985; Karr
& Freemark,
1985) and may alter the outcome of
competition in a similar manner to physical disturbance.
An additional factor affects the outcome of competition. Generally,
competitive exclusion will proceed faster where the available resource
base is greater
(Huston, 1979). Thus, the resource
base at the outset of
succession, or its change over time, can influence the outcome of com-
petition and hence the rate of succession. The presence
or abundance of
mycorrhizae
can influence succession through
competitive effects or di-
rectly
through access
to resources
(Allen
&
Allen, 1985).
Little
information
is available on this aspect of succession, but certain
levels of disturbance
can alter
mycorrhizal
abundance
(Doerr
et al., 1984). Subsequent
changes
in mycorrhizae can contribute to successional
change
(Reeves et al., 1979).
Allelopathy is an important
process in some successions (Rice, 1984).
Whether and how strongly it acts will depend on soil characters,
like
texture, chemistry, moisture and microbial activity. It will also depend
on the allelopathic
potential,
vigor, and dispersion of neighboring
species.
Herbivory
and predation,
though
potentially
quite important
processes
that might
affect
succession,
are
under-investigated in that
context
(Brown,
1984). They are both influenced
by such factors
as climatic cycles, cycles
of their own and interacting
predator
populations, and the vigor of the
host species as determined both by biotic and abiotic limitations. Ad-
ditionally, the defensive capacity of the plants, both constitutive and
inducible, are influenced by resource
levels and environmental stresses.
The identity and palatability of plant
neighbors
and patchiness
of the host
species may also affect predation
and herbivory.
This enumeration of the various processes that cause succession and
the component modifying factors is meant to be illustrative
rather
than
exhaustive. We have not tried to note all the interactions
between
factors
and processes within a level of the hierarchy.
Undoubtedly mechanistic

364 THE BOTANICAL
REVIEW
and experimental
studies will identify additional factors
and specific
pa-
rameters
required
to make sound mechanistic
predictions
of successions
and to understand
completely the mechanisms of any particular succes-
sion. This is only a first attempt at a mechanistic framework called for
in recent
reviews (e.g., Finegan, 1984; Horn, 198
1).
A mechanistic frame-
work for successional causation shows the context of specific models of
various components of succession. Furthermore,
it is needed to comple-
ment general models (Breitburg,
1985)
such as those of Connell and
Slatyer
(1977), or MacMahon
(1980), when the goal is to understand a particular
sere. The framework
indicates the specific factors that must be accom-
modated in translating from the general
theoretical statements
to useful
testable predictions
relevant to specific seres. Most importantly,
the mech-
anistic framework
represents
the initial tentative outline of a complete
successional
theory. The development of a broad, inclusive, mechanistic
theory is one of the principal
goals of contemporary plant ecology. This
review has indicated the mechanistic richness that such a theory must
incorporate.
VI. Acknowledgments
We are deeply indebted to a number of people for significant
improve-
ments in conceptual
and organizational
matters.
J. H. Connell provided
a detailed, insightful and civil review of an earlier
draft.
His contributions
to our
understanding
of succession
both in that review
and in his published
works is substantial.
We hope our high respect
for those contributions is
apparent
here. Fakhri
Bazzaz,
Peter
White
and Lawrence
Walker
provided
us with creative and thoughtful
reviews as well, and we especially thank
them for spurring
us on to greater
rigor. John Pastor also raised useful
points. Beverly Collins, Kevin Dougherty,
Joel Muraoka, and Walt Car-
son, all of the Laboratory
of Plant Strategy and Vegetation Dynamics,
were constantly battered in our thrashing
these ideas about and helped
through discussions and editing various drafts.
Lisa Bandazian
prepared
the figures.
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