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Developmental Instability as a Bioindicator
of Ecosystem Health
D. Carl Freeman
John M. Emlen
John H. Graham
Robert L. Mara
Mary Tracy
C. L. Alados
natural population cycles. Thus, long term studies might be
needed to evaluate potential problems. Even studies spanning a decade might be misleading for species that live for
decades to centuries, or that have persistent seed banks.
Furthermore, the responses to climatic or other changes
need not be proportional to the. change itself. Ecologists are
only beginning to come to grips with the nonlinear aspects of
species and climatic interactions that can lead to compl~x
cycles, thresholds, multiple equilibria (see Logan and Haln
1991), and vegetation inertia (see Tausch this volume).
Nonlinear responses may also occur in measures of fitness, i.e. survivorship and reproduction. These parameters,
however are for obvious evolutionary reasons highly buffered, and hence may not respond demonstrably, or consistently to stressors. Stephen Hendrix, in his review of the
effects of herbivory on plant reproduction, documented a
number of cases where 30 to 50% defoliation did not influence seed production. In other cases, similar amounts of
defoliation were devastating. Ecologists are only beginning
to study these differing buffering abilities, but such differences greatly complicate the use of life history features as
measures of stress.
Despite these obvious defects in ecological indicators,
managers must make decisions in a timely fashion. The e~a
of 50 year grazing studies (Clary and Holmgren 1982) IS
past. How can we determine if populations, and thus communities and ecosystems, are being subjected to undue
stress? How can we evaluate the efficacy of management
without resorting to long term ecological studies? The temptation is to say that if management cannot afford to understand the dynamics of a given system, then the next best
thing is to conduct comparative ecological studies. However,
Robin Tausch (this volume), has argued that temporal or
spatial comparisons of communities are virtually meaningless because it is impossible to determine if the control and
experimental communities share a common history, potential, or equilibrium (if any). Indeed, the notion that there is
a magic composition that communities should attain belies
both climatic and ecological dynamics, and is, in any case,
normally beyond our ability to objectively determine.
We suggest that ecologists and land managers need to
adopt a new strategy. The old strategy of range improvement, i.e. remediation and restoration, using the aforementioned ecologically important but lagging indicators of stress,
is costly, time consuming, and perhaps self-deceiving. A
more sensitive, surrogate measure for fitness, is needed.
Such a measure would provide time to correct or ameliorate
Abstract-Ecologically important parameters such as species diversity, productivity, survivorship or fecundity are often used as
indicators of a population's or community's well being (or, conversely, stress). However, ecological indicators are lagging indicators of stress, documenting problems that have already occurred.
Here we advocate the use of developmental instability as a leading
indic~tor of stress and illustrate its use with a variety of examples.
The use of leading indicators provides managers with the time
necessary to head off problems before costly restoration or remediation efforts are required.
Land managers have, since the 1960's, become increasingly concerned with the perpetuation and preservation of
plant communities, and thus must a·ssess the well being of
natural plant populations. Classical ecological parameters
are often used to indicate stress e.g. species diversity, productivity, biomass, yield, population density, survivorship,
and various life history and reproductive parameters (Maltby
and Calow 1989; Moriarty 1990; Mhatre 1991; Schroder and
others 1991; Cairns and Niederlehner 1992). Unfortunately,
ecological indicators are lagging indicators of stress. By the
time declines in diversity, survivorship, or fecundity show a
community or population to be stressed, managers have few
options as the resource has already been, at least partially,
degraded. At that point, managers can modify human use,
engage in costly remediation and restoration projects, or
watch as the situation worsens. Here, we advocate the use of
developmental instability as a leading indicator of stress,
and illustrate a variety of developmentally invariant features that may be used.
Ecological indicators are difficult to measure, particularly
for long lived species such as most shrubs. Furthermore,
ecological indicators respond to variations in climate and
In: Barrow, Jerry R.; McArthur, E. Durant; Sosebee, Ronald E.; Tausch,
Robin J., comps. 1996. Proceedings: shrubland ecosystem dynamics in a
changing environment; 1995 May 23-25; Las Cruces, NM. Gen. Tech. ~ep.
INT-GTR-338. Ogden, UT: U.S. Department of Agriculture, Forest Sel'Vlce,
Intermountain Research Station.
D. Carl Freeman, Robert L. Mara, and Mary Tracy are with the
Department of Biological Sciences, Wayne State University, Detroit, MI
48202. John M. Emlen is with the National Biological Service, Northwest
Biological Science Center, 6505 Northeast 65th St., Seattle, WA 98115. John
H. Graham is with the Department of Biology, Berry College, Mount Berry,
Georgia 30149. C. L. Alados is with the Instityto Pirenacio de Ecologia, CSIC.
Avda Montanana 177. Aptdo 202.50080 Zaragoza, Spain.
170
the problem before costly restoration measures had to be
implemented.
Measures of stress, based upon genetic or physiological
parameters are generally not efficacious for routine monitoring of populations, because, while valuable in their own
right, they are expensive, time consuming, restricted in
their application to a few species, and unresponsive to a wide
range of stressors. Genetic measures of stress, such as the
rates of mutation, sister chromatid exchange, micronuclei
formation, unscheduled DNA synthesis, adduct formation,
or chromosomal aberrations, have been shown to respond to
various stressors and ionizing radiation (see Carrano and
others 1978; Kantor and Schwartz 1979; Poirier 1984;
Shugart and Kao 1985; Shapiro 1992; and Ali and others
1993, for an introduction to this literature), but it is unlikely
that such indicators respond to grazing, parasites, and other
biotic stressors.
In our experience, physiological measures of stress, such
as water potential, and the rates of photosynthesis, respiration, and stomatal conductance are extremely sensitive.
These measures, however, may respond to a gust of wind or
a passing cloud. This extreme sensitivity to transitory events
makes it difficult to conduct comparative studies, or to
assess integrated effects over time, particularly in environments that are spatially or temporally heterogeneous. Thus,
while they yield valuable insights by establishing cause and
effect relationships, we do not, however, advocate their use
as a routine first stage monitor.
the list of stressors known to influence developmental instability (above) shows that all yield the same result-greater
instability. Thus, developmental instability is used to determine if populations are healthy or if the situation is improving (management is working) or worsening.
Developmental instability is the failure of a genotype to
consistently produce the same phenotype in a given environment (Zakharov 1992; Graham and others 1993a). To determine the phenotype that would have been produced in the
absence of stress we use developmentally invariant traits,
i.e. traits that do not normally change during the course of
development (see Graham and others 1993a and in review
for a discussion of developmental invariance). Such invariance defines one or more forms of symmetry. Thus, the
degree of asymmetry, for normally symmetrical traits, is a
measure of developmental instability; the symmetrical state
is the idealized phenotype expected in the absence of stress.
Deviations away from this idealized phenotype indicate that
development has been disturbed.
Measuring asymmetry, in principle, amounts to examining the within individual variance for a given trait (Graham
and others 1993a), i.e., the repeated parts within the individual required to compute a variance. Repeated parts share
the same genotype and developmental history, and to the
extent that they experienced the same environment, should
be identical. Not all repeated parts are equally well suited
for estimating developmental instability. Clearly, sun and
shade leaves (on the same plant) are repeated parts, yet they
differ because they experienced different environments.
Thus, examining size related differences among such leaves
would be inappropriate, but the left and right sides of each
leaf should still be fairly similar as the two sides of the same
leaf can reasonably be expected to have experienced similar
environments.
Developmental Stability _ _ __
Here, we advocate the use of developmental instability as
a means of assessing the well being of natural populations.
Developmental instability is more sensitive than traditional
measures ofstress (Graham and others 1993a,b; Clarke 1993,
1995); applicable to virtually any multicellular organism;
based upon the responses of indigenous organisms, in situ,
rather than a transplanted lab pet, and thus is relevant to
the population under consideration; it is responsive to a wide
range of stressors including grazing (Alados and others in
review), heat/cold (Siegel and Doyle 1975; Siegel and others
1977; Beecham 1990), chemical stressors (Valentine and
SouIe 1973; Jagoe and Haines 1985; Kieser 1992; Graham
and others 1993b), electromagnetic radiation (Turner and
others in review), parasites (Polak 1994; Mara 1995; Escos
and others in press), aneuploidy (Shapiro 1992), inbreeding
(Markow and Martin 1993), and hybridization between
disparate taxa (Graham and Felley 1985; Graham 1992).
Virtually all of these are known sources of stress that can
befall shrubs. Developmental instability is evident only
when the buffering capacity of the organism has been exceeded (thus the organism integrates the information); it is
inexpensive to use (calipers are sufficient), and requires a
limited sample size (40 individuals per species per site).
Developmental instability is ideally suited for detecting
stress in the field. The use of developmental instability is
similar to taking one's temperature. If body temperature
deviates from 98.6 OF, a person is presumed ill. We do not,
however, know the cause of the illness; further investigation
is required. Neither can the cause of stress be identified by
examining developmental instability. A cursory glance at
Types of Symmetry _ _ _ _ __
Plants exhibit a variety of symmetries that can be used to
assess developmental instability; the pinnate leaves of most
plants are bilaterally symmetrical. Palmate leaves, such as
those of maples, can display both bilateral and radial symmetry. Flowers are commonly categorized based upon symmetry as being either bilaterally or radially symmetrical.
How well the flowers fit these idealized phenotypes is rarely
ascertained, but potentially could be quite informative.
Leaves on many species change size as one moves up the
stem. This is a form of translational symmetry with scaling.
In some species the relationship between leaf size and node
number is simple, but in others it may follow complex
patterns. Finally, the branching of stems, roots, and leaf
veins often exhibit a symmetry across scale. Thus, if one
removes a branch from a tree, the branch resembles a young
tree. Similarly, part of a root may resemble the whole. This
type of symmetry is known as self symmetry. We illustrate
the use of each of these symmetries in estimating developmental instability.
Bilateral Symmetry
Bilateral symmetry usually varies in one of three ways. In
fluctuating asymmetry, one side may be slightly larger than
171
the other, but which side is larger fluctuates between the left
and right side. In this case, symmetry is the normal condition. In directional asymmetry one side is consistently larger
than the other. This is the case with the two sides of the
human heart, and the two sides of a lateral soy bean leaflet.
Antisymmetry occurs when one side is normally larger than
the other, but which side is larger varies among individuals,
as with fiddler crab claws.
Fluctuating asymmetry is estimated as the variance in a
measure on the left and right sides, or as the absolute value
of the difference between measures on the left and right side.
Where the difference between the sides increases, with, say,
leaf size, it may be necessary to scale the difference to the
mean, i.e. var [(R-L)I(R+L)] (see Palmer and Strobeck 1986;
Graham and others 1993a for a complete discussion).
We have examined fluctuating asymmetry of leaves of
Epilobium angustifolium growing at various distances from
a chemical production facility in northern Russia (fig. 1). We
similarly examined the fluctuating asymmetry of lateral
leaf lobes of morning glory (Convolvulus arvensis), and of
the location of leaflets on black locust leaves (Robinia
pseudoacacia) growing at various distances from a chemical
production facility in Ukraine (figs. 2-4). In all three cases,
leaves became more symmetrical as one moved away from
the chemical production facility.
Traits that are directionally asymmetric or antisymmetric also may be used. However, one must first specify the
relationship between the sides before examining the asymmetry (Graham and others in review). For example, in their
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0
4
3
5
6 '7 8
2
1
DISTANCE FROM CHEMICAL FACILITY (km)
Figure 2-The fluctuating asymmetry of the length
of the lateral leaf lobes of Convolvulus arvensis
was compared among plants growing at various
distances away from a chemical production facility in
Ukraine. Twenty plants were examined per site
(means and 95% confidence intervals are shown)
and the degree of fluctuating asymmetry varied
significantly among sites F2,27 = 16.69, P < 0.001.
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3
4
SITES FROM CHEMICAL FACILITY
5
6
Figure 1-The left and right leaf blade widths of
Epilobium angustifolium were measured to the
nearest 0.01 mm. Measurements were made at
the midlength of each leaf. The sites sampled
were at various distances from a chemical production facility in Northern Russia. Site 1 is on the
facility premises. Sites 2, 4, and 5 are 2,9, and 20
km from the facility, respectively. Twenty plants
were sampled per site. Means and 95% confidence intervals are shown. The degree of fluctuating asymmetry differed significantly among
the sites, Fa,76 = 4.83, P < 0.01.
Figure 3-The fluctuating asymmetry in the origin of
the lateral leaflets of Robinia pseudoacacia was
compared for plants growing at various distances
away from a chemical production facility in Ukraine.
Ten plants were examined per site. The top leaf is
from the control site, and the bottom is a leaf from the
facility premises.
172
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study of the effects of electromagnetic fields on soy beans,
Turner and others (in review) found that the lateral leaflets
ofsoy beans are normally strongly directionally asymmetric.
The distal side of each lateral leaflet is smaller (fig. 5) than
the proximal side. However, the relationship clearly changes
as one moves away from the high voltage power line (fig. 5).
In fact, the asymmetry in the widths of the two sides of the
lateral leaflet was least under the power line. The change in
the regression coefficients as well as the residual about the
regression line indicate that development has been disrupted (Graham and others in review).
2
0.2
·1
0
1
4
2
3
5
6
7
DISTANCE FROM CHEMICAL FACILITY (km)
Rotational Symmetry
8
9
Figure 4-The degree of asymmetry in the origin of
lateral leaflets of Robinia leaves differed significantly
among the sites (F 2,B72 = 16.56, P < 0.001). Means
and 95% confidence intervals are shown.
Rotational asymmetry can be used in three ways to assess
developmental instability. First, one can examine the degree to which a full circle is occupied, this amounts to
examining the sum of all of the angles. Secondly, one can
examine the variance in the angles between structures. And
finally one can examine the variance in measures of the
structures themselves. Mara (1995) has shown that the
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o
20
40
60
80
100
DISTANCE FROM HIGH VOLTAGE LINE (M)
120
3~--------------------------------------~
1992
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-20
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20
40
60
eo
100
120
DISTANCE FROM HIGH VOLTAGE LINE (M)
173
Figure 5-The width of the distal side, "0" of the lateral leaflets of
soy beans (Glycine max) is normally smaller than the proximal side
liE". Here we have regressed the width of the proximal side against
that of the distal side for soy beans growing at three different
distances (0, 50, and 100 M) from a 765kv electric transmission line.
Two different fields were sampled in two different years. Here we
have plotted the slopes and intercepts as a function of the distance.
Note the consistent change in these parameters as one moves away
from the high voltage line.
leaves of red maples infected with gall forming mites(Vascates quadripedes) occupied less of a complete circle,
regardless of whether or not the leafitselfwas infected, than
leaves of trees that were not infected (fig. 6). We have shown
elsewhere (Freeman and others 1994) that angles between
the veins in the leaves ofNorway maple were more acute and
variable for trees growing near a chemical production facility in northern Russia, than those growing some 20 km from
the facility. Finally, lupines have compound palmate leaves.
Lupines exposed to the drift of herbicides and pesticides
from orchards exhibited more than four times the within leaf
variance for leaflet length than did plants far removed from
agriculture (F1,68 = 6.21, P < 0.02, Freeman unpublished
data).
Translational Symmetry
Translational symmetry implies that something stays the
same as one moves from place to place. In some plants such
as Elodea (Tracy and others 1995), the size of mature leaves
and internodes does not vary with node number, and thus
shows true translational symmetry. In this case, the appropriate measure of developmental instability is the within
individual variance, which was found to increase as a result
of pollution (fig. 7). In other species, internode lengths, and
diameters, or measures of leaf size change in predictable
ways with node number as one moves up the stem; this is
translational symmetry with scaling. Scaling relationships
may be linear, parabolic or more complex. Alados and others
(in review) examined the developmental instability ofinternode lengths in Chrysothamnus greenii across a gradient of
grazing intensity, and found the internode lengths to fit the
following equation:
TOTAL VEIN ANGLES
en 1
ttl
a:
o
IIJ
C
1
In (internode length) = a In (node number)
- b (node number).
control
low
high
TREATMENT
unlnfected
Developmental instability, estimated as the standard error
of the regression, was found to decrease with increased
grazing intensity (fig. 8). These results appear counterintuitive. However, the results make sense when one realizes that Chrysothamnus itself is not often grazed, while its
Figure 6-Leaves of red maples infected
with gall forming mites exhibited less complete circles in terms of total vein angles, than
did uninfected leaves.
z
Q
0.26
0.24
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a:
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0 0.18
a:
0
a: 0.16
a:
w
aa: 0.14
i!S
z
~
0.12
(lJ
UnpOlluted
0.1
Heavily POlluted
Figure 7-Translational asymmetry of internode lengths in Elodea canadensis was compared among sites in southeastern Michigan.
Plants from the polluted site showed a significantly greater within plant variance than plants
collected from the control site (F = 20.764,
P < 0.001). Seventy-five plants were examined
per site.
CONTROL
MEDIUM
GRAZING INTENSIlY
Figure 8-The standard error of the regression of
internode length on node number for Chrysothamnus greenii (see text for the allometric formula)
decreases as grazing intensity increases.
174
HIGH
others 1994; Freeman and others 1994; Graham and others
1993a,c for a discussion of developmental instability and
fractals; Peitgen and others 1992 is an excellent introductory text on fractals, chaos and related phenomena).
To estimate the dimension filled by Fucus individuals, we
employ a box counting procedure (fig. 10). To do this, overlay
the individual with grids of different size boxes and count the
number of boxes in which at least part of the Fucus occurs.
We then regress the natural log of number of occupied boxes
against the natural log of the length of the box. The absolute
value of the slope of the line is the fractal dimension. This is
a measure of the space filled by the individual. Developmental instability is the degree to which the individual failed to
fit the idealized phenotype, and is measured as the standard
error of the regression. Under nonstressful conditions all
points should lie on the regression line. In the case of Fucus
growing offthe coast of Washington, Tracy and others (1995)
found that the standard error of the regression increased
significantly with pollution (fig. 10).
competitors are heavily grazed (Hutching and Stewart 1953).
in the highest grazing treatment, Chryothamnus expenences the least competition, while in the ungrazed control treatment, Chrysothamnus is stressed by competition.
Th~s,
Self Symmetry
Self symmetry is symmetry across scale, and is common in
branching structures. Here, we illustrate the use of self
symmetry to estimate developmental instability using the
brown alga Fucus (fig. 9; Tracy and others 1995). Fucus
exhibits dichotomous branching, and each branch resembles
the whole alga; this species exhibits symmetry across scale.
Notice also that the individuals in figure 9A and 9B do not
completely fill the planes defined by their thalli. The alga
clearly fills more space than a straight line (dimension one)
connecting any two points on its body, but less space than the
whole plane (dimension 2). The alga, in fact has a fractional
dimension, and approximates a fractal (see Emlen and
~ig~re
9-Top: Fucus furcatus latifrons collected from a relatively unpolluted
Puget Sound, Washington, appears to have a normal thallus. Bottom:
Fucu~ furcatus latifrons collected from a heavily polluted site in Puget Sound,
Washington shows a breakdown in self symmetry.
site
In
175
300
B
ISlopel- Fractal Dimension - 1.38
100
10
1
10
2
Logs
~ar----------------------------------~
0.
c
c
D
0.
0
.,
e
e
iii
C)
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'0
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CD
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0.4
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0.
!
Unpolluted
1.
I
~ 1.
1.
Polluted
1.fT---:-:--'::-~~----r------~-----1
Heavily Polluted
Unpolluted
Figure 10-(A) Grid overlays are used to calculate a fractal dimension using the box counting method.
In this hypothetical example, the relative box sizes (s) are 1,2,4, and 8. The number of occupied boxes
in each grid N(s) are: 205 in size 1, 71 in size 2, 24 in size 4, and 12 in size 8.
(8) The double log plot is computed from the hypothetical box counting example. The fractal
dimension = absolute value of the slope of the line defined by the log of total boxes occupied versus the
log of box size.
(C) Variability about the regression line used to determine the fractal dimension of Fucus at each
collection site is assessed using the standard error of the regression. The mean and 95% confidence
interval is shown. A significant difference occurs among sites (X2 = 11.157, P < 0.001 ).
(D) The fractal dimension of Fucus differed significantly among sites (X2 =37.03, P < 0.01). Data is
shown as the mean and 95% confidence intervals.
176
Polluted
Heavily POlluted
Conclusions
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-------------------------------
Most ecological parameters are lagging indicators of stress;
indicating problems only after they have already occurred.
By using such indicators, managers cannot catch early
symptoms of deterioration, and must instead continually
play catchup, trying to restore already damaged lands.
Developmental instability, as a leading indicator, can signal
trouble before it reaches the point of apparent demographic
consequences. By using such a leading indicator of stress,
managers should be able to better manage lands at lower
economic costs.
Acknowledgment _ _ _ _ _ __
This manuscript was facilitated by financial assistance
from the Intermountain Research Station, Shrubland Biology and Restoration Research Work Unit, Provo, UT.
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