Disturbance and Population Structure on the Shifting Mosaic Landscape

Author(s): James S. Clark

Source: Ecology, Vol. 72, No. 3 (Jun., 1991), pp. 1119-1137
Published by: Wiley
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Ecology, 72(3), 199 1, pp. 1119-1137
? 1991 by the Ecological Society of America

DISTURBANCE AND POPULATION STRUCTURE ON THE

SHIFTING MOSAIC LANDSCAPE'

JAMES S. CLARK
Department of Botany, University of Georgia, Athens, Georgia 30602 USA,2
The Biological Survey, New York State Museum, Albany, New York 12230 USA, and
Department of Ecology and Behavioral Biology, University of Minnesota, Minneapolis, Minnesota 55455 USA

Abstract. A stochastic model of plant population dynamics is developed and analyzed

to determine how density and age structure depend on thinning rates and disturbance
regimes. Probability distributions of age and density are derived from the distribution of
regeneration niches on a landscape and the thinning rates of cohorts on patches created by
adult mortality or larger disturbances. The theory is then extended to different types of
disturbances that operate at different scales and are interdependent, such as treefalls that
only become important as the early-successional trees that initially colonize an area affected
by a larger scale disturbance become mature.
In general, landscapes that provide frequent regeneration niches support high-density
young stands. Density distributions are negatively skewed. Decreasing frequency of regen-
eration niches results in lower mean density, higher variance, and increased (less negative)
skewness. When regeneration niches are rare, density is low, variance is low, skewness is
positive, and the age classes are highly variable. In more complex cases, regeneration niches
may depend on the time since the last large disturbance; for example, canopy gaps can
become more frequent as postfire cohorts become senescent. Then age class distributions
on a given disturbed area become increasingly platykurtic with time; skewness is negative
for early-successional species and positive for late-successional species. The exponential
distribution of age classes commonly observed in late-successional species is the asymptotic
result of a more general distribution that depends on time since the last disturbance. Across
a landscape that supports these interdependent disturbance processes, infrequent distur-
bances result in density distributions for late-successional species with large mean, negative
skewness, and low variance. An early-successional species is present at low density with
positive skewness and low variance. Density distributions for both species types are more
platykurtic and have higher variance when disturbance frequency - thinning rate. Frequent
disturbances produce higher densities of early-successional species with positive skewness
and lower densities of late-successional species. The landscape distributions of age classes
are J-shaped for both species. With frequent disturbance, age distributions are leptokurtic
for both species, but more so for late-successional species. Age class distributions are
increasingly platykurtic with less frequent disturbance. The "intermediate" disturbance
frequency that maximizes the probability of being reproductively mature at the time of
the next disturbance event (Clark 1991a) is also that which maximizes the density of
reproductive individuals on this shifting mosaic landscape.
Key words: age structure; demography; density; disturbance; patch; perennials; plant populations;
regeneration niche; shifting mosaic; stochastic process.

INTRODUCTION lem of applying to plants the population models de-

veloped for mobile organisms, such as animals or
The development of an analytical theory of plant
plankton in chemostats, has long been recognized
demography has been frustrated by problems of com-
(Schaffer and Leigh 1976, Pacala 1989). Plant recruit-
plexity related to spatial heterogeneity in population
ment, growth, and mortality respond to extremely lo-
structure and limiting resources (Schaffer and Leigh
calized resource levels rather than to landscape aver-
1976, Pacala and Silander 1985, Pacala 1988), asym-
ages. There is also an uncertainty associated with the
metric competition (large individuals control a dispro-
timing of recruitment events, which occur episodically,
portionate share of the resource base) (Harper 1977,
even in "undisturbed" assemblages (Harper 1977, Spurr
Weiner 1985, 1986), and time-dependent parameters
and Barnes 1980). Different species require different
such as birth and death rates (Clark 1991 a). The prob-
types of disturbances or "regeneration niches" (sensu
Grubb 1977), and it is likely that the pattern of these
' Manuscript received 22 December 1988; revised 15 Feb-
events has important implications for population dy-
ruary 1990; accepted 10 August 1990; final version received
14 September 1990. namics at the metapopulation scale (Comins and Noble
2 Present address. 1985, Warner and Chesson 1985, Hastings and Wolin

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 1120 JAMES S. CLARK
1989, Pacala 1989). Local dynamics are further com-
plicated by larger scale "disturbances" that cause adult
mortality, permit regeneration, and synchronize pop-
ulation dynamics across landscapes (Shugart 1984,
Turner et al. 1989). Thus analytical treatment of plant
demography is restricted largely to annuals (reviewed
in Watkinson 1986 and Pacala 1989) or to dynamics
within single generations of perennials (Hara 1984,
1985, Clark 1990).
Lack of a tractable model that applies to the de-
mography of perennial plants makes it unclear how
population structure depends on local dynamics and
disturbance regimes. It appears likely, for example, that
the way in which disturbance probability changes with
plant age should influence population dynamics (Pick-
ett and White 1985, Clark 1989, Cohen and Levin
1991). Recent field studies have focused on determin-
ing how this probability changes over time (Johnson
1979, Romme 1982, Johnson and Van Wagner 1985,
Foster 1988, Baker 1989, Clark 1989), and there has
been some speculation concerning effects on popula-
tion structure (Johnson 1979, Clark 1989). Such ques-
tions might be addressed with forest "gap" models
(Botkin et al. 1972, Shugart 1984) and the appropriate
experimental design. But there exists no analyzable
model to investigate the consequences of disturbance
regimes for structure at the scale of the metapopulation.
Specifically, how should densities and age classes be
distributed in the "shifting mosaic" landscape that de-
velops in forests that may rarely experience large ex-
ogenous disturbances (Watt 1947, Bormann and Li-
kens 1979)? How does this population structure evolve
following larger disturbances? How do dynamics with-
in local cohorts influence metapopulation structure?
What type of structure is to be expected in landscapes
ranging from those that experience infrequent distur-
bances to those characterized by frequent disturbance?
What constitutes an "intermediate disturbance re-
gime" (Connell 1978, Huston 1979) for a shifting mo-
saic landscape, and what are its implications? How
does the structure of a population change at local and
regional scales en route to regional dominance or ex-
tinction of a species? The answers to these questions
represent an important step toward understanding per-
sistence and species coexistence, for it is the age and
density structure of a population that determines
whether a species can persist. Moreover, interpreting
effects of fluctuating environments and climate change
requires a theory that establishes the population struc-
ture to be expected in the absence of these sources of
variability.
Here I present a stochastic model of plant population
dynamics to describe and analyze this mosaic structure.
The model contains somewhat more complexity than
is typically included in analytical population models
to accommodate the inherently stochastic nature of
plant populations and the mix of spatial and temporal
scales. I nonetheless strive to retain the simplicity nec-
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Ecology, Vol. 72, No. 3
essary for analysis and understanding. Population dy-
namics of perennial plants are necessarily stochastic
because populations often consist of cohorts that date
from the occurrence of a regeneration niche (Grubb
1977, Harper 1977, Spurr and Barnes 1980). I focus
on the distribution of regeneration niches, which occur
stochastically in time and space and can be quantified
in natural assemblages, and on subsequent thinning on
those patches as individuals increase in size. The model
structure is similar to that contained in gap models
(Botkin et al. 1972, Shugart 1984) in assuming a mosaic
of different-aged patches.
The products of this theory are probability distri-
butions of patch age classes, of cohort densities, and
of plant age classes. Patch age classes are an important
component of population structure, because cohorts
may pass through a predictable sequence of stages that
determine many ecosystem attributes, such as leaf area
(Waring and Schlesinger 1985), primary production
(Sprugel 1984, 1985), nutrient cycling (Vitousek and
Reiners 1975, Pastor and Post 1986), and gap area
(Oliver 1981, Clark 1991 b). Plant density approaches
a point equilibrium nowhere on this shifting mosaic
landscape, so distributions of densities are a useful
means for summarizing population size. Age structure
depends on distributions of patches and their densities;
without knowledge of the mosaic structure, it is im-
possible to represent age structure in a fashion that
permits analysis of the factors that produce it. Results
have application to questions of landscape patterns of
disturbance, succession, life history, and spatial and
temporal heterogeneity.
THEORETICAL DEVELOPMENT
The landscape consists of a mosaic of patches, each
supporting a cohort of plants that became established
a yr ago. Disturbances serve as regeneration niches
(sensu Grubb 1977); they occur episodically, resulting
in adult mortality and the initiation of a new cohort
of small individuals at high density, with patch age a
being reset to zero. The model does not depend on
assumptions regarding why disturbances occur (e.g.,
whether they are considered "allogenic" vs. "autogen-
ic" [Runkle 1985]). Between disturbances on any given
patch, plants increase in size, and density x(a) decreas-
es at rate dx(a)/da. The structure of this metapopula-
tion is summarized by distributions of (a) patch age
classes w(a), (b) cohort densities J(x), and (c) plant age
classes fj(a).
Disturbances can occur at two spatial scales (Fig. 1).
Type r disturbances are sufficiently small that the pop-
ulation that becomes established on the patch can be
treated as a single cohort. Type r disturbances are nest-
ed within a landscape that may experience a second
disturbance process s that affects larger areas of age t.
A type s patch contains many type r patches, each of
age a ' t (Fig. 1). An example would be a landscape
that experiences a gap-phase process r and fire regime
 June 1991 PLANT DENSITY
type-r disturbance
type-s disturbance
E0 t t 0 gap simulation models, simplifies the analysis. I discuss
t=0 t=0
a =0
lype-r disturbance lypes disturbance
Temporal domain
FIG. 1. Model of a shifting mosaic population that ex-
periences two superimposed and interdependent disturbance
processes. A small-scale type r process (e.g., canopy gap for-
mation) is nested within a larger type s process (e.g., fire
occurrence) (above). Type s disturbances synchronize type r
patches. On any given patch, recruitment is episodic, followed
by thinning (center). The occurrence of disturbances that allow
recruitment occurs stochastically with probability that may
increase with time since the last disturbance (below).
s. In this case, process r describes a shifting mosaic gap
process that develops with time t since the last fire s.
I begin with the simplest case by solving for the
structure of this mnetapopulation that is composed of
a mosaic of patches created by a type r (e.g., "gap")
disturbance process. The analysis explores how a sin-
gle-species metapopulation is influenced by local and
regional processes. I then generalize this result to in-
clude a disturbance process s that synchronizes type r
patches across broader portions of a landscape for an
early- and late-successional species. Several assump-
tions are used to simplify the analysis:
1) The location of a given patch relative to others
on the landscape does not influence its dynamics.
2) Dispersal is high and seed production is uninflu-
enced by local cohort dynamics.
3) Thinning within a patch is deterministic and
driven by plant growth.
4) Disturbances destroy existing adults, and they
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AND AGE STRUCTURE 1121
create regeneration opportunities. Because patches are
out of phase, the landscape is a mosaic of different-
aged patches.
5) Disturbance can be described as a stationary re-
newal process (Clark 1989).
Assumption (1) is partially relaxed in a later section,
The shifting mosaic with large-scale disturbances, where
type r patches are nested within type s patches. As-
sumption (2), an assumption my model shares with
how the decrease in propagule availability at low den-
sities is likely to affect model predictions. Assumption
(3) is a reasonable way to simplify local dynamics in
view of the ways in which thinning rates compensate
for initial density (Harper 1977). Thinning rate de-
pends on growth of the individual plants within the
cohort (Harper 1977, Aikman and Watkinson 1980,
Norberg 1988). Although densities of seeds and seed-
lings are highly variable, densities tend to converge to
this thinning equation from a range of initial densities
as a result of the response of thinning rate to crowding
(Harper 1977, Westoby 1984, Clark 1990, 1991 b). As-
sumption (5) is a stationarity assumption, which says
that the distribution of disturbance events does not
depend on the time at which we observe the process.
This assumption is partially relaxed in the section, The
shifting mosaic with large-scale disturbances, where type
r disturbances depend on the elapsed time since the
last type s disturbance.
The shifting mosaic structure (the type r process)
Metapopulation structure across this landscape de-
pends on the rate of thinning within each patch and
on the age distribution of patches. Per capita mortality
rates in crowded even-aged plant cohorts tend to be
nearly constant following canopy closure and before
40
c ~~crown area 7+ > aM203
100 - - + 0
0 30 60 90 120 150
Age (a)
FIG. 2. The relationship between exclusive crown area
projection A and density x in a Picea stand. Data points are
indicated by squares. Stand densities move horizontally to-
ward the thinning line until the canopy closes, at which point
densities follow the exponential model, until plants approach
maximum size. Dashed lines are fitted values to the model
from Clark (1990). The crown-area projection A is predicted
from the same parameter values using the relation 1 /x(dx/
da) = - 1/A(dA/da) (Clark 1991 b).
 1122 JAMES S. CLARK Ecology, Vol. 72, No. 3

K () 100 (d)

id2 -l 50

C', 0 ~~~~~~~~~~~~~~~~~~~~(e)

(b)

_ D E[Ar]

F- 0 40 80 0 2 0

0.2

o(C) ((n x

E[Ar]

0.0

0 0.0- I
0 40 80 0 11

Age (a) Density (x(a))

FIG. 3. Relationships used to derive the distribution of densities across a shifting mosaic landscape having constant
disturbance probability that increases with age: (a) survivorship of the local cohort; (b) the rate of change in density; (c) the
probability that a randomly selected patch is of age a; (d) the inverse of (a), i.e., the age of a patch when density is x; (e)
distribution w, (a) from (c) solved in terms of density x; (f) the probability that a randomly selected patch supports den-
sity x.

plants approach maximum size (Harper 1977, Peet and
Christensen 1980), because of the effect of individual
plant growth on population thinning (Clark 1990). As
growth rates of plants decline, so too do density-de-
pendent mortality rates (Fig. 2). At this time when
density-dependent mortality is decreasing, density-in-
dependent mortality is on the rise, and canopy gaps
begin to appear. The extent to which density-depen-
dent vs. density-independent factors dominate in older
cohorts, however, will vary with species. I therefore
make the simplifying assumption that a local cohort
thins at per capita rate Xp,
x(a) = Ke- Pa, (1)
where the coefficient K has units of density and incor-
porates the plant-height: crown-breadth ratio of the
species (Norberg 1988, Clark 1990; Fig. 3a).
Age distribution of patches. -The age distribution of
patches is equivalent to the age distribution of cohorts,
because we have thus far assumed that plants become
established immediately following patch formation, i.e.,
a disturbance. This distribution is the proportion of
the landscape occupied by age class a, termed the "re-
currence time." For a process that began in the distant
past, the distribution of recurrence times tends to
wr (a) = [S(a) (2)
(Cox 1962), where Sr(a) describes the survivor function
for the disturbance regime, and E[Aj is the time A,
expected to elapse between disturbances (Fig. 3c). Sr(a)
is the probability that a patch will survive at least a yr
without another disturbance and can be estimated from
disturbance history data (Johnson and Van Wagner
1985, Clark 1989).
Distribution of cohort densities. -The distribution of
cohort densities can be derived using the age distri-
bution of patches together with the fact that the thin-
ning Eq. 1 establishes a relationship between patch age
and stand density. Let the age at which a patch supports
density x(a) be a(x) (Fig. 3d). Then the recurrence time
can be solved in terms of density through the inversion
or[a(x)]= Xr(X) (Fig. 3e). The second ingredient needed
for a distribution of densities is the proportion of time

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June 1991 PLANT DENSITY AND AGE STRUCTURE 1123

a(x) during which density actually is x, given by the cv[X]

reciprocal of the thinning rate

da (X + Xp) 1 ____- r (8)

A(X) = dx(a) (3) X, L2XA + Xr (Xr + X,)2j

where X is an observed value of x. The variability of

(Appendix I). The distribution of densities across the patch densities is maximized at intermediate distur-
landscape then is the product of wr(x) and A(x): bance frequencies, as can be demonstrated from the
variance
f;(x) = r(X) zA(x) (4)
XrK2 Xr2K2
(see Fig. 3f and Appendix I).
Var[X] = 2XA + Xr (Xa + Xr )2
For example, consider a species that regenerates im-
mediately following patch formation and thins accord- Setting a Var[X]/8Xr = 0 yields
ing to Eq. 1. Further assume that patch formation (dis-
turbance) has constant probability Xr, with survivor '\* (XP +Xr* )3
function Sr(a) = e-Ara and expected interval between
Xr* =(2XP + Xr *)2 (9)
the formation of new patches E[Ar] = 1/Xr. From Eq. which contains a root Xr* where variance is maximized
2, the distribution of recurrence times,
(Fig. 5).
Distribution of cohort age classes. -The age class dis-
w,(a) = Xre-Aa, (5)
tribution contains two components, the age distribu-
tion of patches Wr(a) and the plant density on patches
is exponential. Solving for a in Eq. 1 yields
of age a,

ln In K
Lx(a)1
fp(a) A)r(a)x(a) (10)
a(x) =-
Wr(a)x(a) da

which is substituted in Eq. 5 to give

fp(a) is the probability that a randomly selected plant
is of age a. For the exponential recurrence time given
W(x) = Xrexp[-Xra(x)] = X- by Eq. 5, the representation of age class a is solved as
\K

The time spent at a given density is determined from

fp(a) = (Xr + Xp)exp[-a(Xr + Xp)], ( 11)
the derivative of Eq. 1, which is used in Eq. 3 to give which is a simple exponential distribution with param-
A(x) = [Xpx(a)]- -'. The appropriate substitutions in Eq. eter (Xr + XP) (Fig. 4a-c). This distribution has expec-
4 yield the probability density function tation E[AP] = (Xr + Xp)-I and coefficient of variation
cv(AP) = 1, where AP is the age of a plant selected
randomly from this metapopulation.
0 Xr (_) O < X < K
Local and regional effects on landscape structure. -
JPX \K/
f(x) = (6) The structure on this mosaic population, which is char-
acterized by the simplest possible stochastic distur-
10 otherwise bance process (i.e., constant probability), displays dy-
namics that will prove robust over the more complex
f(x) is the frequency of density x (Fig. 3f). That Eq. 6 treatments that follow. It is therefore worth considering
is a probability density function is shown by integrating some of these dynamics at this stage.
rK
Increasing thinning rate XP has the effect of decreasing
over (0, K), ff(x) dx = 1. This distribution is increas-
the average age (Fig. 6b) and density (Fig. 6a) of the
metapopulation and the less obvious consequence of
ing for Xr > Xp (Fig. 4a), uniform for Xr = X, (Fig. 4b),
increasing the coefficient of variation on densities (Fig.
and decreasing for Xr < Xp (Fig. 4c). The mth moment
of x is 6c). At the scale of a single cohort, lower densities are
characteristic of older stands (Fig. 3a). At the meta-
population scale, however, high thinning rates cause
E[Xm] = XrK
low densities to be associated with young stands (Fig.
mXP + Xr'
6a, b). Despite the fact that thinning rate has no effect
having expectation on the distribution of patch age classes, the average
tree is younger.
E[X] rK ( 7) Although the model assumes deterministic local dy-
XP + Xr
namics, it is worth noting that higher thinning rates do
and coefficient of variation not necessarily increase variability within individual

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 1124 JAMES S. CLARK Ecology, Vol. 72, No. 3

(a1) (b) (c)

0.06-

> 0.03-

0.00 "-;
0 50 100 0 50 100 0 50 100

0.2- Density (x) )

20.1

0.0
Plant age (a)
0.10

4- 0.05

U-

.- 0 20 40 60 0 20 40 60 0 20 40 60
Patch age (a)

>b (d) (e) (f)

Z 0.06-
0
._

o < 0 03 <:

a- 0.00-1
0 50 100 0 50 100 0 50 100
Density (x)

0.1

0.0

Plant age (a)

0.10_

0051

0.00
0 20 40 60 0 20 40 60 0 20 40 60
Patch age (a )

10 20 50

Expected interval,E[Ar]
FIG. 4. Distributions of density fix) and cohort age classes f,(a) on a shifting mosaic landscape having six different
disturbance regimes, characterized by patch age classes wr(a). The distributions of density are given by Eq. 8. Figure shows
examples using two different shape parameter values, c,(c, = 1, above, and c, = 3, below) and three values of the expected
interval, E[Aj]: E[AjI = 10, left, E[AjI = 20, center, E[Aj] = 50, right. The thinning rate used here is XP = 0.05.

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June 1991 PLANT DENSITY
40
E[X]
7 -- - - - --- oX]
c 20 /
2Ip
0 I I a power transformation of the time scale using a Wei-
0.0 0.1 02
Disturbance frequency (2r)
FIG. 5. The maximum density variance at "intermediate"
disturbance frequencies X,. Expected density E[X] increases
with X,, as young, dense stands account for a greater propor-
tion of the metapopulation. Coefficient of variation simul-
taneously decreases, however, as the population becomes more
homogeneous, resulting in an intermediate maximum for
standard deviation on density a[fX.
cohorts, because that variability depends on the degree
of density compensation (Clark 1991b). If within-co-
hort thinning rates were density and age independent
with rate parameter Xp, for example, then higher mor-
tality rate would indeed cause increased variability as
described by the coefficient of variation for this bi-
nomial process, exp[ 2p] /1K (1 - e-APa). If density
compensation is high, however, thinning rates are re-
sponsive to random variability in local mortality (Fig.
2), and variance in cohort densities is constrained. The
binomial case does not hold, because mortality risk of
plants depends on whether neighboring plants have
survived. Indeed, given that XP is positively related to
plant growth rate and that higher growth rates increase
density compensation (Clark 1991b), then high thin-
ning rate is likely to attend decreased variability within
cohorts, until density compensation declines late in
stand development. Thus, increased thinning rates do
not necessarily increase within-patch variability, al-
though they do increase among-patch variability.
At the metapopulation scale, the parameter of the
exponential age distribution is not equal to the mor-
tality rate, but is greater than the mortality rate in an
amount equal to the disturbance frequency (Eq. 11).
Although thinning rate XP drives expected density and
age in the same direction (i.e., 8E[X]/8XP and 8E[Ap]/
aP are both negative for all x and a, respectively) (Fig.
6), the frequency of regeneration opportunities X, drives
expected density and age in opposite directions (Fig.
4a-c). More frequent regeneration opportunities in-
crease the expected density while decreasing the ex-
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AND AGE STRUCTURE 1125
pected age. Density variance is maximized at inter-
mediate disturbance frequencies (Fig. 5). In general,
higher thinning rates XAP increase variability across the
landscape, while more frequent regeneration oppor-
tunities (higher Xr) render the metapopulation more
uniform.
Changing disturbance probability. -These analytical
results for constant disturbance probability aid under-
standing of the more complex structure that arises from
more flexible (and realistic) disturbance distributions.
These flexible distributions are analyzed here to estab-
lish what implications, if any, age-dependent distur-
bance probability holds for population structure.
Changing disturbance probability is accomplished by
bull distribution Sr(a) = exp[-(Xra)cr]. The correspond-
ing distribution of patch age classes is
1
Wr(a) = exp[-(Xra)cri (12)
E[Ar]
where Cr is a dimensionless shape parameter, E[Ar] =
r( 1/c, + 1)/Xr is the expectation of the Weibull distri-
bution, and r() is the gamma function. The moments
of Wr(a) are derived in Appendix II. Increasing Cr de-
scribes a probability of disturbance that increases with
time since the last disturbance. Solving for a(x) from
Eq. 12 and making the appropriate substitutions in Eq.
4 results in the distribution of cohort densities
f(W X exp t-IX nt-2
0 < X K. (13)
Eq. 6 is a special case of Eq. 13, where Cr = 1. The age
distribution from Eq. 10 can be written as
fp(a) = exp[-(a - a] (14)
f exp[-(Xra)cr- Xa] da
For Cr = 1, this expression is equivalent to Eq. 11.
Although we cannot solve for fp(a), nor for the mo-
ments of f(x), the structure represented by these dis-
tributions can be analyzed to determine how local dy-
namics and the landscape disturbance regime affect
local and metapopulation structure. The mode of den-
sity distribution Eq. 13 occurs where df(x)/dx = 0,
given by
{KexpL-I) Cr1) IX 0 C
f ,(X Crl(cr-
X= Cr =1 Xp > Xr
l K C =1Xp < Xr
(15)
For X , Xr, this mode occurs near K/2. The rate at
which local populations thin (XP) influences the regional
 1126 JAMES S. CLARK Ecology, Vol. 72, No. 3

(a) Density (x) (b) Age (a)

loo- 20-

802\ ~~~~E[X] I E[Ap]

40-

(c) (d)
2- 2-
CV[X] CV[Ap]
.n 1.5 1.5

o I /I -- .....

U 0.5- 0.5-

U 0.0 0.2 0.0 0.1 0.2

Mortality rate Ap
FIG. 6. Effect of local mortality rate on metapopulation structure. Both density (a) and expected age (b) decrease with
increasing mortality rate. The coefficient of variation on density increases (c), however, while that for age is unaffected by
mortality rate (d).

density structure according to summarized by parameters X, and cr. As in the previous

8f(x) _ cAc, - 1ex(Ac)
aXP XAE[Ajx
where A = (X,/Xp)ln(K/x). Increasing thinning rate de-
creases the expected density, having a positive effect
on the representation of lower density cohorts and a
negative effect on higher density cohorts. This sensi-
tivity to thinning rate is greatest at intermediate den-
sities xP, where
X = K exp( cr-/cr) (16)
The densities most sensitive to thinning rate XP, when
Xp is high (low), are rare and greater (less) than the
modal density for the landscape. When thinning rates
are in the range of the disturbance frequency, local
population dynamics have their strongest influence on
the densities that are among those most commonly
observed at the metapopulation level and little effect
on densities that are infrequent (very low or very high).
All else being equal, the landscape density of the meta-
population will be lower and the coefficient of variation
higher for greater Xp. As with the exponential case,
kurtosis is lowest and skewness O when XP X r.
The effects of the regional disturbance regime are
exponential case, increased disturbance frequency de-
creases the expected patch age and variance, but the
coefficient of variation on patch ages is independent of
the rate at which these patches are formed X, (Appendix
II). For a given disturbance rate constant (i.e., constant
r), increased c, has the effect of reducing the variance
on patch ages, despite the fact that patches are still out
of phase. Compare for example wr(a) distributions in
Fig. 4b vs. e. This effect on patch ages results, in turn,
in distributions of densities having higher modal den-
sities, higher mean, and lower variance. Increasing c,
decreases expected plant age when disturbance is fre-
quent (Fig. 4a vs. d) and vice versa (Fig. 4c vs. f).
Increased c, decreases variability in age structure, and
it reduces kurtosis. Thus, reducing the variance on patch
ages has effects that are different from either of the
effects observed by changing thinning rates or distur-
bance frequency alone.
The shifting mosaic with large-scale
disturbances
In order to generalize population dynamics to in-
clude large-scale type s disturbances, it is necessary to
simplify the shifting mosaic structure and to incor-
porate the dependency of type r disturbances on time
t since the last type s disturbance (Fig. 1). In the last

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 June 1991 PLANT DENSITY AND AGE STRUCTURE 1127

(a) 20-( a ) 20- ~~~~species 2

-) 10 Id
10

0-

0 20 40

Time (t)

time since fire (t)

( 0b3) 5 15 25 35 45

0 20 40 0 20 40 0 20 40 0 20 40 0 20 40

Cohort age (a)

FIG. 7. Contrasting density and age structure of early- (1) and late- (2) successional species as a function of time since the
last large (type s) disturbance. (a) Density of species 1 increases, then decreases following disturbance, while that of species
2 increases. (b) The variance on age increases for both species over time, but distributions are skewed in opposite directions.
As time since the last large disturbance becomes remote, the age distribution of species 2 approaches the limiting exponential
distribution, given by the broken line.

section, I claimed that the patch age distribution was rt

given by the survivor function divided by the expected
interval in Eq. 2. In fact, Eq. 2 is a special case of a
time-dependent process
w,(a, t) = m,(t - a)Sr(t),
Xk(t) = K m,(t - a)S,(a)Sk(a) da. (17)
By direct analogy to the type r case (Eq. 4), the distri-
bution of densities across a landscape of type s patches
is

where mj(a) is the renewal density (Cox 1962), the f(Xk) = WS(Xk) A (Xk)A
expected number of disturbances to occur on a land-
scape a yr following the last type s disturbance. As the where WS(xk) is the recurrence density for the type s

time since the last type s disturbance becomes remote, process. The age class distribution on a single type s

m,(t - a) tends to I/E[ArI, yielding Eq. 2. The renewal patch changes with time t,

density is related to S,(a) as Mr(t -a)Sr(a)Sk(a)

fk(a, t)= , (18)
d
(t) =: - dt Si (t), m,(t -a)S,(a)Sk(a) da

where -dSi/dt lit is the probability that the ith dis- and that for a landscape of type s patches at elapsed
turbance occurs on (t, t + At) and So(t) = SQ) (e.g., time T since the type s process began is
Cox 1962). This relationship can be used together with
the assumption that type s disturbances are much larger
fTw,(t)fk.(a, t) dt
To

than type r disturbances (so much so that type r dy-

namics can be treated deterministically) to derive and
analyze population structure across this larger land-
scape. The recruitment rate 1k(t) of species k on a type
s patch is proportional to the renewal density,
k(t) = Kmr(t)-
The density of species k on a single type r patch at time
t following occurrence of the most recent type s dis-
turbance is
gkT(a) T t (19)
fT J sw(t)fk(a, t) da dt
I subsequently use this approach in analytical and nu-
merical examples to demonstrate effects of local (thin-
ning and small disturbances) and regional (large dis-
turbances) processes on metapopulation structure.
An analytical example. -Consider the simplest case
of constant probability of type r and type s distur-

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 1128 JAMES S. CLARK Ecology, Vol. 72, No. 3

0.4 0.4 024

3 .2- . 0.2-

0.000_ .
0 10 20 0 10 20 0 10 20
Density (x)

0.3 0.1E 0.2

C
C
0.2-
f 0.1 - .. , 0.1
Plant age (a) 0.2- 0.2-
o 1

c 02 0.0
Plantc age 0.0
(a 0.2 0) 0.0

O 0 4 20 40 0 20 40
.0

D A .A .2>_OZn L

C 0 10 20 0 10 20 0 10 20
Density (x )
0.3 0.3- 0.3-

0.21 Plant age (a) 0.2] .2

s0.1- t 0.1- 0.1-

0.0 0.0 0.0

0 20 40 0 20 40 0 20 40
Patch age (a)
10 20 50

Expected interval, E[Ts]

FIG. 8. Dynamics of two species across a landscape where large disturbances are distributed as co(t) and where dynamics
on any given patch are as shown in Fig. 7. Distributions of densities fix), cohort age classes g(a), and patch age classes wo(t)
are shown for two values of C5 and four different expected intervals between disturbances E[TS]. X,* and X2* (upper right-
hand graph) represent the upper integration limit for density distributions, analogous to K in Eq. 6.

bances. The age distribution of type s patches is giv- with corresponding rate equation
en by

dXk = KXr - Xk (XP + Xr).

Us(t) = X~e-'~,,

and type r disturbances are occurring at constant rate Solving for time t in terms of density and substituting
mr(t) = Xr. The density of species k at time t is solved in w,(t) gives a recurrence density
from Eq. 17 as

Xk(t) = r [1 - e-t(P+Xr] WS(Xk) = \ 1 - X A(XP? X|)1T7\

X~p ? Xr

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June 1991 PLANT DENSITY AND AGE STRUCTURE 1129

0.4 terministic type r dynamics. It is the distribution of

densities across type s patches. The age distribution on
0.2 a single type s patch is solved from Eq. 18 as

0.0
0 10 20 fk(a, t) (= ? Xr)e-at(xp+Xr) 0 < a < t
X1* X2*
This result tends to the type r case (Eq. 11) as type s
disturbances become rare,

0.3-
0X31 lim fk(a, t) = (XA + X )ea(AP+xr)
t woo0

This limiting result also applies to cases of more com-

plex recruitment patterns, provided that recruitment
rate tends to some nonzero value with time since the
0.2-
last type s disturbance (Fig. 7). I made some analytical
headway with the landscape age distribution (Eq. 19),
0.1 -

X (a +X~e a ( +X r) jT e Xstd
0.0- gkMa =SP + Xr)ea(p- F es dt d,
0 2b 40 1 - e'~~~s j0 1 ~~ - P Xr

which tends to

0.2- I eo east dt
gk-(a) = Xs(Xp + Xr)e-a(Xp+xr) eO it- tcit
i1-it1
as T becomes large.
A numerical example.-The assumptions of con-
0 10 20
stant disturbance probability can be relaxed to accom-
modate recruitment rates and small-scale disturbances
0.3-
that depend on large (type s) disturbances. I use the
example of fire for this large disturbance, but the model
0.2- 1
could be applied to other disturbances, such as large
blowdowns. To illustrate the effect of these interacting
disturbance processes, I consider two species that differ
in the time t at which they begin to colonize a site
0.0,
0.2- following the most recent type s disturbance. These
species are an early-successional species 1 and a late-
0.1 - successional species 2. Species 1 finds regeneration
F.IG.8 oniud niches following some large catastrophic disturbance
that results in mortality of many adults, whereas spe-
* ( ) 20 406 cies 2 finds increasingly more regeneration niches with
time since this catastrophic disturbance. This second
100 species might be a gap colonizer, because canopy gaps
FIG. 8. Continued. tend to be rare until early-successional species attain
maximum size. If the recruitment rates for species k
is given by 3k(t), where k is either 1 or 2, then these
trends in recruitment rates are described by dfj(t)/dt
< 0 and df2(t)/dt - 0. To limit the number of sub-
scripts, I represent the thinning and recruitment rates
of both species by single parameters XP and K, respec-
The product of this quantity and the reciprocal of dXk/ tively.
dt (see Eq. 3) yields the probability density function In this example, I assume that the distribution of
type s patch ages can be described by a Weibull dis-
tribution with recurrence time
f(Xk) = X+ [1 Xk ( X

s(t)= E[T] exp[-(Xst)cs], (20)

O?Xk? KXr
Thi d + X,
where E[Ts] is time expected to elapse between type s
This distribution differs from Eq. 6 in assuming de- disturbances, and Ts is an observed interval between

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 1130 JAMES S. CLARK
disturbances. The Weibull distribution has been shown
to fit disturbance history data (Johnson 1979, Baker
1989, Clark 1989). The density of regeneration niches
for the early-successional species 1 decreases with time.
For simplicity I assume this decrease is exponential,
being proportional to
$,(t) = e-Pt.
Let the increase in regeneration niches for species 2 be
its complement:
:2(t) e-Pt.
For species 1, the effects of regional disturbance re-
gime, represented by XA and cs, are qualitatively similar
at this scale to those of X, and c, at the finer scale
(compare density distributions in Fig. 4 with those for
species 1 in Fig. 8). For species 2, the effects are op-
posite. Increasing intervals between large disturbances
have the effect of shifting the mode of the early-suc-
cessional species 1 to lower densities and the late-suc-
cessional species 2 toward high density (Fig. 8). As the
density of the early-successional species decreases, the
distribution becomes more platykurtic and subse-
quently more leptokurtic, as it becomes extinct in most
stands. The density distribution of the late-successional
species also becomes initially more platykurtic, as the
mode shifts toward higher densities, and it then be-
comes more leptokurtic and negatively skewed. Both
species exhibit the maximum variation in densities at
intermediate times since the last large disturbance.
Age distributions are J-shaped for both species (Fig.
8). These landscape age class distributions are a com-
posite of the age class distributions (Eq. 18) of the
individual sites (Fig. 7b), with the relative contribution
of the distributions at different times since fire deter-
mined by the recurrence time of the fire regime. The
age distributions of both species have low expectation
when disturbances are frequent, because all patches are
of young age, and thus cohorts are necessarily young.
Species 1 always has a component of older individuals,
because it begins to reproduce sooner after the large
disturbance. For the early-successional species, results
demonstrate the widely observed J-shaped distribu-
tions that result from landscape surveys actually com-
posed of local distributions having modes >0 (Hough
1932, West et al. 1981; Fig. 7b). Age class distributions
g, (a) for this species approximate the age distributions
w,(t) of the patches themselves to an extent determined
by the degree to which recruitment can continue with
time since the last disturbance. The age distribution of
species 1 becomes increasingly uniform where distur-
bance is infrequent, as total density declines. This is
because young patches account for a smaller proportion
of the total landscape. These results agree with the
regional syntheses of West et al. (1981), where com-
posite distributions of older stands were increasingly
platykurtic and positively skewed.
Species 2 maintains the J-shaped character because
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Ecology, Vol. 72, No. 3
recruitment of young age classes continues. When dis-
turbances are infrequent (A, << X,) the landscape dis-
tribution of age class of the late-successional species
approaches an exponential distribution with parameter
X, (Fig. 8).
DISCUSSION
One of the most popular concepts of forest dynamics
to emerge in recent years is that of the "shifting mo-
saic" (Watt 1947, Bormann and Likens 1979, Peet
1981, Shugart 1984). The so-called old-growth forest
consists of a patchwork of small cohorts, each having
a unique history that depends on the episodic occur-
rence of disturbances. Processes exogeneous to the stand
are not required to introduce heterogeneity, because
variability is produced by the plants themselves. On
any given piece of ground the dynamics consist of re-
cruitment phases followed by periods of thinning. These
local dynamics are produced by simulation models of
small patches that clearly show this two-phase process
(e.g., Shugart 1984:Fig. 5.4). Only when the output
from a large number of patches is averaged do recruit-
ment and mortality appear somewhat constant.
In this paper, I derived the structure of a "shifting
mosaic" metapopulation, and I examined the effects
of local population dynamics and of regional distur-
bance regimes on that structure. The local dynamics
are represented by changing age and density, which
depend on growth rates of individual plants within
small cohorts. The regional disturbance regime is de-
scribed by a distribution of events that result in adult
mortality and the initiation of new cohorts. The struc-
ture of this metapopulation is summarized by distri-
butions of cohort (patch) age classes, plant age classes,
and cohort densities. This highly idealized class of
models serves to isolate several important relation-
ships.
Effects of local dynamics
The link between growth of plants and cohort mor-
tality rates (Clark 1991a) can be used together with
results presented here to demonstrate implications of
local dynamics for metapopulation structure. The fast-
er plants grow, the more rapidly they thin. This effect
of growth rate on mortality is obvious in all forestry
yield tables (reviewed in Clark 1991 b), and it is com-
monly observed in populations of herbaceous plants
(reviewed in Harper 1977). This negative effect of
growth rate on density has effects at the metapopula-
tion level, influencing not only expected values, but
also population heterogeneity. The directions and mag-
nitudes of these growth-rate effects depend on the scale
at which the population is observed.
Growth rates may have opposing effects on within-
vs. among-cohort variability. High growth rate and
attendant high thinning rate results in low expected age
and density of this shifting mosaic metapopulation (Fig.
6a, b). At the same time, the coefficient of variation
June 1991 PLANT DENSITY AND AGE STRUCTURE 1131
on plant age is unchanged (Fig. 6d), but that of density
is increased (Fig. 6c). The faster plants grow, however,
the greater may be the adjustment of density-depen-
dent mortality rates to stochastic variability in mor-
tality rates (Clark 1991 b). It is therefore possible that
higher growth rates result in more predictable thinning
curves. The implication is that increased growth rate
can increase local homogeneity while at the same time
rendering the metapopulation more heterogeneous.
Where large-scale disturbances episodically synchro-
nize patch dynamics across large areas, higher thinning
rates imply lower density and lower age for early-suc-
cessional and late-successional species (Fig. 8).
The effect of disturbance regime
The general patterns in age structure across a gra-
dient from high to low regeneration-niche frequency
range from high-density young stands to a mix of den-
sities and age classes to low-density stands dominated
by older individuals. Constant disturbance probability
results in an exponential age structure with parameter
(Xr + X,) (Fig. 4a-c). Disturbance frequency "substi-
tutes" for mortality rate in the age distribution (Eq.
1 1), and more frequent disturbance has an effect similar
to higher mortality rate. This represents an important
result, because exponential age distributions appear to
commonly arise in real forests (e.g., Hough 1932, Leak
1965, 1975, Van Wagner 1978), and the parameter of
the distribution is shown here to be the sum of two
potentially very different sources of mortality, the
"thinning rate," which is largely a consequence of com-
petition, and the "disturbance frequency," which can
contain a component that is exogeneous to the local
stand dynamics and which may affect much larger ar-
eas. Moreover, while one component (Xr) of this pa-
rameter tends to be associated with recruitment, the
other (X,) is not.
For density distributions, however, more frequent
disturbance has effects opposite of those produced by
increased thinning rate; as disturbance becomes more
frequent, density increases, and the metapopulation
becomes more homogeneous (Fig. 4). Infrequent re-
generation niches (e.g., Fig. 4c) produce distributions
of densities with a mode near zero, positive skewness,
and low variance. Many plants become old and se-
nescent before the next regeneration niche becomes
available. Where mortality and regeneration-niche time
scales are roughly equivalent (Fig. 4b), the mode occurs
at intermediate densities, skewness may approach zero,
and variance is high. These stands consist of both young
and old cohorts at high and low densities, respectively.
Where regeneration niches occur frequently (Fig. 4a),
densities are high, skewness is negative, and variance
is again low. Where the agent responsible for the re-
generation niche also destroys mature individuals, as
is often the case, these frequent disturbances result in
a transient phase of young individuals at high density
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that will not reach reproductive maturity before the
next disturbance occurs (see below, Intermediate dis-
turbance and the link to life history theory). The simple
distributions presented here likely overrepresent ju-
venile classes for species that are rare. A partial anti-
dote to the high variability of juvenile classes would
be to ignore them entirely, as is done in gap simulation
models, and simply focus on structure of the remaining
population.
Increasing disturbance probability with age
Results presented here support earlier speculation
(e.g., Johnson 1979) that the shape of the disturbance
distribution (represented by parameter c) has impor-
tant effects on population structure. The simplest case
of constant disturbance probability has been advocated
on the basis of some empirical studies (Van Wagner
1978) and is assumed in most stochastic population
models.
It appears in forests, however, that the probability
both of gaps (Kohyama 1987, Suzuki and Tsukahara
1987, Foster 1988) and of fire (Heinselman 1973, John-
son 1979, Romme 1982, Baker 1989, Clark 1989) often
increases with time since the last such event. This in-
creasing probability is described here by parameter Cr
or cs > 1. As a result of the more precipitous rise in
disturbance probability that occurs with large Cr, dis-
turbances tend to occur with higher probabilities at a
certain age, and the variance on disturbance intervals
declines. For example, stands of some early-succes-
sional tree species tend to fall apart at senescence, with
gap area increasing rather suddenly as growth rates of
trees decline. The population effect of increased Cr de-
pends on the relationship between thinning rate (XP)
and expected disturbance interval (E[ArI) and on the
scale at which the population is observed. In fact, the
influence of time-dependent disturbance probability
on age structure changes qualitatively from species
having low thinning rate (XP << 1 /E[ArI) to those having
high thinning rate (XP > 1/E[ArI). A clustering of high
disturbance probabilities at particular ages (i.e., Cr >
1) within a shifting mosaic metapopulation has the
effects of decreasing the expected age and increasing
the expected density for populations characterized by
low thinning rates relative to the expected disturbance
interval (compare Fig. 4a and d). This response occurs
despite the fact that the expected disturbance interval
is held constant. However, the coefficient of variation
decreases for both age and density.
At high thinning rates (XP > 1/E[ArI, e.g., 50-yr in-
tervals in Fig. 4), increasing parameter Cr increases both
the expected age and density (compare Fig. 4c and f),
but the coefficients of disturbance intervals within
patches (increasing cr) results in decreased variance on
patch age classes, which in turn decreases the coefficient
of variation on plant densities and on plant age classes
of long- and short-lived species. Despite the fact that
 1132 JAMES S. CLARK
patches are out of phase with one another, the increas-
ing predictability of patch age produces younger and
denser metapopulations of populations having low
thinning rates, older and denser metapopulations of
populations having high thinning rates, and more ho-
mogeneous metapopulations regardless of thinning rate.
Superimposed and interdependent
disturbance processes
On many landscapes, several types of disturbances
that provide regeneration niches for different types of
species may operate at vastly different scales. An ob-
vious example is fire, which may occur over a spatial
scale that is large, and treefalls, which occur on the
same piece of ground, albeit at different times (e.g.,
Spies and Franklin 1989). Moreover, the occurrence
of treefalls themselves depends on occurrence of fire,
because only when trees that regenerate following fire
become large will treefall produce the canopy gaps re-
quired for regeneration by a gap species (Peet and
Christensen 1980, Oliver 1981, Peet 1981). Early-suc-
cessional species, such as Betula papyrifera, Pinus
banksiana, P. resinosa, P. contorta, and Populus spp.,
may colonize soon after such a disturbance at high
density and subsequently thin. Other species, such as
Acer saccharum, Tilia americana, and Fagus grandi-
folia, germinate beneath a closed canopy and maintain
low metabolic rates until a gap in the canopy results
in increased resources that allow "recruitment" to the
canopy. Different sizes and types of gaps may favor
different species (Connell 1979, Runkle 1982, Brokaw
1985, Canham 1988). Although this description is
oversimplified, it captures a general pattern that has
been observed so consistently that it serves as a basis
for prevailing concepts of "succession," "regeneration
niche," and "gap-phase replacement."
On a large disturbed area where occurrence of re-
generation niches depends on time since this large dis-
turbance, the age distributions of early- and late-suc-
cessional species are skewed in opposite directions (Fig.
7b). Across a landscape of such large disturbances,
however, both distributions are positively skewed, with
the early-successional species having a longer "tail"
(Fig. 8). The structure of an early-successional popu-
lation responds to an increase in disturbance frequency
in a fashion qualitatively similar to a gap species on a
simple shifting mosaic (Fig. 4): density increases and
age decreases. Increasing time between large distur-
bances results in a metapopulation containing few old
and low-density stands of early-successional species.
The age class distribution approaches that of the dis-
turbance regime itself, with the regional population
exhibiting high spatial variability (compare g(a) and
W,(t) distributions in Fig. 8). On any given disturbed
area, a late-successional species eventually assumes a
limiting exponential distribution with the parameter
equal to the thinning rate plus the frequency with which
canopy gaps occur (Eq. 11; Fig. 7b). Thus, the empirical
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Ecology, Vol. 72, No. 3
observation of exponential age-class distributions in
"late-successional" species (Leak 1965, 1975) repre-
sents the limiting distribution of a more general rela-
tionship that accommodates recruitment and mortality
from both sources. Both species display maximum
variance on stand densities at intermediate disturbance
frequencies (Fig. 8, see next section).
The effects of variance in the intervals on large-scale
disturbances (compare c, = 1 vs. c, = 3 in Fig. 8) also
depend on thinning rate, in addition to whether a spe-
cies is early vs. late successional. If such disturbances
are rare, this variance has little effect on population
structure (e.g., E[T5] = 100, c, = 1 vs. c, = 3 in Fig. 8).
For long-lived species, or when such disturbances are
more frequent (e.g., E[Tj] = 10 in Fig. 8), however,
decreasing the variance on expected disturbance inter-
val decreases the expected age and density of late-suc-
cessional species, and it increases the density and de-
creases the age of early-successional species. The
coefficient of variation on densities is decreased, while
the variance is maximized at intermediate frequencies
for both species.
It is therefore important to consider the time-de-
pendence of disturbance probability for disturbances
that occur frequently, and it is of diminishing impor-
tance for disturbances that are rare relative to the time
scale of the thinning process. Examples of disturbances
that occur with sufficient frequency that this time-de-
pendence is important include gap processes and fire
in some temperate forests. Thus, the relative time scales
for cohort thinning and disturbance frequency, and the
temporal correlation in the mosaic landscape both have
important consequences for population structure. The
effects of both of these considerations are complex and,
in some cases, unexpected. An understanding of the
representation of density and age classes and of meta-
population heterogeneity requires knowledge of the time
development of cohort densities and changing distur-
bance probability at several temporal and spatial scales.
Intermediate disturbance and the link to
life history theory
In a companion paper (Clark 1991 a) I showed that
the probability that a plant will be reproductively ma-
ture at the time of the next recruitment opportunity s
is maximized at "intermediate" disturbance frequen-
cies. This intermediate frequency is one having expec-
tation that is greater than the maturation time a, and
less than the longevity a2, which is correlated with
maturation time (Loehle 1988), i.e., a2 = aao . Because
many tree species that occur in temperate forests share
similar life histories, this intermediate disturbance fre-
quency is also expected to maximize species diversity.
Given the focus on population structure taken here (as
opposed to life history optimization in Clark 1991 a),
it is reasonable to ask whether such an "intermediate"
disturbance frequency also exists that maximizes re-
productive potential from the standpoint of population
 June 1991 PLANT DENSITY AND AGE STRUCTURE 1133

1.0- density of reproductive individuals suggests (1) an in-

ternal consistency of the theory of population dynamics
E[x]
on a mosaic landscape (i.e., the individual perspective
0.8-
does not yield results different from a population per-
spective), (2) a close link between optimal life history
0.6 reproductive fraction from an individual perspective and the mosaic struc-
0 06 ture of a metapopulation, and (3) a specific definition
for the "intermediate disturbance hypothesis" as one
0.4- that maximizes both the reproductive potential of in-
dividual plants and the reproductive portion of the
metapopulation. As disturbance becomes less frequent,
0.2- Xr
the reproductive fraction of the population increases,
but more local populations go extinct (Fig. 9); the pop-
0.0- ulation consists of increasingly larger and older indi-
0 40 80 120 160 200 viduals within lower density stands. At the other end
of the spectrum are populations nearing extinction be-
Expected interval
cause mortality agents occur too frequently. These
FIG. 9. Comparison of predictions for the optimal life stands consist of individuals that are too young to re-
history from Clark (199la) with that for maximum density
produce, and they occur at high density only because
of reproductive individuals from theory presented here. The
reproductive fraction xr (solid curve) is the product of ex- they are young and thus small. Thus, the high-density
pected density E[x] and the fraction of the population that is stage that occurs when disturbance is frequent is a tran-
of reproductive age (broken curves). This product is equal to sient phenomenon, because the seed source rapidly di-
the optimal maturation time r from Clark (1991a), when
minishes with this loss of reproductive individuals from
density is measured in units of K, i.e., r = X,/K. The maturation
the population.
time is a, = 30 and thinning rate is XP = 0.01.
The maximum among-cohort variability in density
classes also occurs when disturbance frequency is in

structure. Instead of maximizing the reproductive the range of thinning rate (Figs. 4, 5, 8). This conclusion

probability ? discussed in Clark (1991 a), one candidate applies to the simple shifting mosaic (Fig. 4), and to
both early- and late-successional species on the more
for maximization here is the density of reproductive
individuals Xr, which includes all individuals of the age complex landscape that experiences large-scale distur-

interval (a, iaa). This density can be derived as the bances, despite the fact that disturbance frequency is

product of expected density E[X] and the proportion
of the population that is of reproductive age,
raa2
xr = E[x] J fp(a) da.
For the exponential case, expected density is given by
Eq. 7. The fraction of the population that is reproduc-
tively mature is derived form Eq. 11 as
Zaa2
J fp(a) da = exp[-(Xr + Xp)a1]
-exp[-(Xr + Xp)aal]. (24)
The density of reproductive individuals is thus
driving the density distribution of early- and late-suc-
cessional species in opposite directions (Fig. 8). Thus,
at a range of spatial scales, the approximate equiva-
lence of these time scales maximizes variability, and
it coincides with the relationship where persistence is
predicted to be most likely. The turnover of species
along disturbance gradients (e.g., Huston 1979, Tilman
1988) derive at least in part from this relationship be-
tween time scales. These relationships are important
in view of the frequent regional changes in forest tree
composition that have occurred in temperate zones just
over the last 10 000 yr (Wright 1974, Davis 1981, Pay-
ette and Filion 1985, Jacobson et al. 1987).
Population dynamics as a mosaic

There is often a concern in population theory that

pXrK {exp[-(Xr + Xp)a1] - exp[-(Xr + Xp)aa1j}.
Xp + Xr
This result is proportional to s for the same disturbance
regime, given by Eq. 10 in Clark (199 la), i.e.,
Xr = K?,
and so is maximized at the same disturbance frequenc,
(Fig. 9).
The fact that the disturbance regime that maximize
reproductive probability is also that which producer
the age and density structure containing the maximum
deterministic results might be modified in some qual-
itative way upon the introduction of random or time-
dependent variability in demographic parameters such
as birth or death rates. A number of studies show that
this type of variability may produce unexpected results
in some models (Abrams 1984, Chesson 1984), while
in others the main effect of limited stochasticity is to
simply replace a fixed-point equilibrium with a prob-
ability distribution having expectation in the neigh-
borhood of that point equilibrium (May 1973, Turrelli
1981). For many applications, it is reasonable to ignore

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 1134 JAMES S. CLARK
this random component of birth and death rates, be-
cause the effect of variation appears obvious or because
variation in the system under consideration is deemed
insignificant (it may be small in magnitude, or depen-
dencies may be weak).
The type of stochasticity treated here cannot so easily
be ignored as it represents the basic demography that
characterizes many populations of perennial plants. This
variation is that which results from the uncertainty
associated with the timing of recruitment events. Even
if all environmental variables could be held constant,
a survey of stem densities and age classes across any
landscape would generate a frequency distribution, be-
cause of the discrete nature of individual plants, be-
cause plants are constantly increasing in size, and be-
cause increasing individual size for a population of
sessile organisms necessitates decreasing density with
time. As plants approach maximum size, growth slows
and density is reduced to a point where canopy gaps
begin to appear. It is at this point that recruitment rate
increases. Variability is produced by the population
itself The result is a metapopulation that is a collection
of cohorts (Watt 1947, Bormann and Likens 1979),
each possessing a unique history and thus structure.
In order to address this process, I have treated the
metapopulation as a mosaic of local populations. Plant
densities, competitors, and resources do not approach
a constant density anywhere on a landscape, recruit-
ment is confined to short periods, and a long history
of observation implicates the importance of the dis-
tribution of regeneration niches on landscapes (e.g.,
Grubb 1977). Taller plants preempt more light and
larger root systems may permit control of a dispro-
portionate amount of belowground nutrients. The es-
tablishment of a seedling is most strongly dependent
on the occurrence of "safe sites" (Harper 1977) or "re-
generation niches" (e.g., Watt 1947, Grubb 1977). "The
vast majority of tree species are dependent either on
fire, flooding, or windthrow to provide suitable seed-
beds for their establishment" (Spurr and Barnes 1980:
71). Different species utilize different regeneration
niches, and it is the availability of regeneration niches
that poses an important limiting factor on a popula-
tion's success.
Competition influences the probability of surviving
until that next recruitment opportunity occurs. A strong
competitor can insure local extinction of a weaker com-
petitor for the same regeneration niche by increasing
that competitor's mortality rate to an extent where it
does not survive to reproductive maturity or until the
next recruitment opportunity. Thus, theory presented
here places competition within the context of survi-
vorship of established cohorts within patches of finite
area.
Finally, the occurrence of these opportunities for re-
cruitment (gaps) often depends on the dynamics of the
overstory, so it might also be viewed as one component
of competition. A more complete model might gen-
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Ecology, Vol. 72, No. 3
erate the distribution of regeneration niches from the
assemblage itself, with the occurrence of each type of
regeneration niche influenced by the size and density
of each species within the assemblage. I view this ap-
proach as less useful at the level of analytical models
because of its complexity, the lack of information on
direct and higher order effects of species combinations
on the disturbance regime, and the problem of under-
standing how the assemblage interacts with exogenous
factors to affect the distributions of disturbances such
as blowdowns, fires, and landslides. Moreover, the gap
process in temperate forests may be relatively insen-
sitive to species composition (see Runkle 1985, Clark
1991 a). This approach is also more applicable to real
situations, because the distributions of disturbances
and plant survivorship can be quantified in forests
without understanding all of the dependencies of that
disturbance occurrence on the physical environment
and biotic factors. These simple analytical results pro-
vide a perspective for complementary numerical mod-
els that assume a similar structure but contain more
complexity.
ACKNOWLEDGMENTS
For their helpful discussions and/or reviews of the paper I
thank P. Abrams, H. Caswell, P. Chesson, P. Munholland, S.
Pickett, D. Royall, D. Tilman, H. E. Wright, and three anon-
ymous reviewers. This research was supported by a fellowship
from the Graduate School of the University of Minnesota,
and NSF grants BSR-8715251 and BSR-8818355. Limno-
logical Research Center contribution number 377 and New
York State Education contribution number 608.
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APPENDIX I
The effect of thinning rate on the distribution of densities
Consider a cohort of plants that are rapidly growing (and
thus, rapidly thinning) soon after a regeneration niche be-
comes available (a = 1). The high thinning rate dictates that
the population actually spends a small fraction of a year at a
given density x. In contrast, at some later time a > 1 plants
are thinning less rapidly (Fig. 1). The "fraction" of time a(x)
actually spent at a given density is much greater in an amount
determined by the thinning rate. This result is demonstrated
as follows:
Define discrete probability density functions U and V such
that
U(x) = Pr[u - 1 x(a) < u]
and
Vla(x)] = Pr[v - 1 a(x) < v],
where u and v are values of density and age, respectively (Fig.
A. 1). U is the probability that a randomly selected patch
supports density x. V is the probability that a randomly se-
lected patch is a yr old. We wish to solve for U(x) and to
establish its relationship to the continuous distribution fix).
U(x) is the product of two events, the probability that a
random patch is of an age a(x), i.e., that age at which the
patch supports density x, and the portion of age a(x) at which
density actually is x,
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Ecologyv Vol. 72, No. 3
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U(x) = Vla(x)] a(u - 1) - a(u)
v - (v - 1)
The quotient in Eq. 1. 1 is the relative proportion of the age
interval (v - 1, v) at which density is between u - 1 and u
(Fig. A. 1). During the remainder of the interval (v - 1, v)
density is not between u - 1 and u. Expanding a(x) in a
Taylor series about (v - 1) and ignoring all terms of order
-2, we can write
a(u) = (v - 1) + d [U - x(v - 1)] + O(X2),
dx
and
da
a(u - 1) = (v - 1) + da [(u - 1) - x(v - 1)] + O(X2),
where o(x2) represents all terms of order -2. Substituting in
Eq. 1. 1 yields
da u - 1 - u
U(X) = Vja(x)] v-(v-1
= V(a)
Given that w(a) is the limiting distribution for V(a), then i\(x)
= I da/dx I and fix) is the continuous analogue of U(x).
June 1991 PLANT DENSITY AND AGE STRUCTURE 1137

APPENDIX II
x(v-1)
Derivation of moments for the distribution of patch ages
U
Given the distribution of patch ages (recurrence times)
::::..
LI-i..... .
::::x a..).a
.......)..
.-]) v
Bl I:::: ..:::::::.
wr(a) = / exp[-(Xa)j],
F(1 /c 1 1)
......... .........:::::::: ::: :.::::::::.
........... ................. ::.. :........:....- .....
::::::::::::::: ........... ...::: ..::: ................... .

the mth moment of wr(a) is written as

........ .... ...., 11 - ...... :-0: . ?
x(v) . .. , ...'-.EE-. I .,,-.---.
. . . ... . . . . . . . . . . . .

Exam] =J amzr(a) dal

v-1 a(u) a(u - 1)v

r it amexp[-(Xra)1'] da.
::- i v :::::::::::~:Ez
The substitution u = (XAa)' yields

_ _ _ _ _ OC (M fi)

FIG. A. 1. Geometric interpretation.... of. th contribution

-cro Ic I) u c e-u du.
XjmcrF(l/c + 1) J

The integral expression is now a gamma function with pa-

enced in Appendix I.~ ~ ~~..........I.............
rameter . Using this fact, together with the property
c

r(a + 1) = ar(a), the mth moment is written as

? - V
rV
zM + I0

Age a Xr-ro 1c)

FIG. A. 1. Geometric interpretation of the contribution of yielding expectation
thinning rate to the distribution of cohort densities. The co-
hort thins at a rate that is approximated by the slope of the E[Ar r (2/c)
shaded triangle. Labeled values of density and age are refer- Xrr(i/c)'
enced in Appendix I. and coefficient of variation

rJ /( c) - F2(2/c)
cv[Ar] = r(2/c) F(31c[ - F(l/c) J

By use of well-known properties of the gamma function, it

can be shown that these results collapse to the exponential
for c = 1, i.e., E[ArI = I/Xr and cv[Ar] = 1, and that c = 2

decreases this expectation to E[Ar] =

XrVgr

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