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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.

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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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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.

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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).

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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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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:

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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.

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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

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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.

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Conclusions

Society for Testing and Materials. Philadelphia: 136-158. Graham, J. H.; K. Roe; T. West. 1993b. Effects oflead and benzene on developmental stability of Drosophila melanogaster. Ecotoxicology. 2: 185-195. Graham, J. H.; J. M. Emlen; D. C. Freeman; J. Kieser. (in review). Developmental invariance, symmetry and the measurement of developmental instability. Hendrix, S. D. 1988. Herbivory and its impact on plant reproduction. In: J. Lovett Doust; L. Lovett Doust, eds. Plant reproductive Ecology: Patterns and strategies. Oxford University Press. Oxford: 246-266. Hutchings, S. S.; G. Stewart. 1953. Increasing forage yields and sheep production on Intermountain winter ranges. U.S. Department of Agriculture Circular 925. 63 p. Jagoe, C. H.; T. A Haines. 1985. Fluctuating asymmetry in fishes inhabiting acidified and unacidified lakes. Can. J. Zool. 63: 130-138. Kieser, J. A 1992. Fluctuating odontometric asymmetry and maternal alcohol consumption. Ann. Hum. BioI. 19: 513-520. Logan, J. A; F. P. Hain. 1991. Chaos and insect ecology. Virginia Agricultural Experiment Station, Virginia Polytechnic Institute and State University Information Series 91-3, Blacksburg, Virginia. 108 p. Maltby, L.; P. Calow. 1989. The application of bioassys in the resolution of environmental problems; past, present and future. Hydrobiologia. 188/189: 65-76. Mara, oR. L. 1995. Developmental stability in Acer rubrum. MS. Thesis. Wayne State University, Detroit, MI. 28 p. Markow, T. A; J. F. Martin. 1993. Inbreeding and developmental stability in a small human population. Ann. Hum. BioI. 20: 389-394. Mhatre, G. N. 1991. Bioindicators and biomonitoring of heavy metals. Journal of Environmental Biology. 12: 201-209. Moriarty, F. 1990. Ecotoxicology: The Study of Pollutants in Ecosystems. Second Edition, Academic Press, New York. Palmer, A R.; C. Strobeck. 1986. Fluctuating asymmetry: Measurement, analysis, patterns. Ann. Rev. Ecol. Syst. Peitgen, H.; H. Jurgen; D. Saupe. 1992. Chaos and fractals, New Frontiers of Science. Springer-Verlag, New York. Polak, M. 1994. Parasites increase fluctuating asymmetry of male Drosophila nigrospiraculla: implication for sexual selection. In: Markow, T., ed. Developmental Instability: Its origins, and evolutionary implications. Kluwer Academic Publishers, Dordrecht, The Netherlands: 257-268. Poirier, M. C. 1984. The use of carcinogen-DNA adduct antisera for quantitation and localization of genomic damage in animal models and human population. Environ. Mutag. 6: 879-887. Schroder, G. D.; S. Ross-Lewandowski; E. M. Davis. 1991. Evaluation ofthe toxic effects ofselected municipal wastewater effiuents on aquatic invertebrates. Environmental Technology. 12(9): 757-768. Shapiro, B. L. 1992. Development of human autosomal aneuploid phenotypes (with emphasis on Down Syndrome). Acta Zoological Fennnica. 191: 97-105. Shugart, L.; J. Kao. 1985. Examination of adduct formation in vivo in the mouse between benzo(a)pyrene and DNA of skin and hemoglobin of red blood cells. Environ. Health Perspect. 62: 223226. Siegel, M. I.; W. J. Doyle. 1975. The effects of cold stress on fluctuating asymmetry in the dentition of the mouse. J. Exp. Zool. 193: 385-390. Siegel, M. I.; W. J. Doyle; C. Kelley. 1977. Heat stress, fluctuating asymmetry and prenatal selection in the laboratory rat. Am. J. Anthrop. 46: 121-126. Tracy, M.; D. C. Freeman; J. M. Emlen; J. H. Graham; R. A Hough. 1995. Developmental instability as a biomonitor of environmental stress: An illustration using aquatic plants and macroalgae. In: F. M. Butterworth, ed. Biomonitors and Biomarkers as indicators of environmental change. Plenum Press. NY: 313-33'? Turner, W. A; D. C. Freeman; H. Wang. [In review]. The effects of electromagnetic fields from high voltage transmission lines on the regulation of growth in Glycine max L. [submitted to Nature]. Valentine, D. W.; M. E. Soule. 1973. Effect of p,p-DDT on developmental stability of pectoral fin rays in the grunion, Leuresthes tenuis. Fish Bull. 71: 921-926. Zakharov, V. M. 1992. Population phenogenetics: analysis of developmental stability in natural populations. Acta. Zool. Fennica. 191: 7-30.

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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.

References

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Alados, c. L.; J. M. Emlen; B. A Wachocki; D. C. Freeman. [In review]. Developmental instability in the fractal architecture of desert plant species: A tool to detect grazing. Submitted to the American Naturalist. Ali, F.; R. Lazar; D. Haffner; K. Adeli. 1993. Development of a rapid and simple genotoxicity assay using a brown bullhead fish cellline: Application to toxicological surveys of sediments in the Huron-Erie corridor. J. Great Lakes Res. 19: 342-351. Beacham, T. D.1990.Ageneticanalysisofmeristicandmorphometric variation in chum salmon (Oncorhynchus keta) at three different temperatures. Can. J. Zool. 68: 225-229. Cairns, J.; B. R. Niederlehner. 1992. Coping with the environmental effects of point-source discharges. Journal of Environmental Sciences. 4(1) :1-9. Carrano, A V.; L. H. Thompson; P. A Lindl; J. L. Minkler. 1978. Sister chromatid exchange as an indicator of mutagenesis. Nature. 271: 551-553. Clarke, G. M. 1993. Fluctuating asymmetry ofinvertebrate populations as biological indicators of environmental quality. Environmental Pollution. 82: 207-211. Clarke, G. M. 1995. Relationships between developmental stability and fitness: Application for conservation biology. Conservation Biology. 9: 18-24. Clary, W. P.; Holmgren, R. C. 1982. Desert Experimental Range: Establishment and contribution. Rangelands. 4 :261-264. Emlen, J. M.; D. C. Freeman; J. H. Graham. 1993. Nonlinear growth dynamics and the origin of fluctuating asymmetry. In: Developmental Instability: Origins and Evolutionary Significance. In: Markow, T., ed. Kluwer Academic Publishers. Dordrecht, The Netherlands: 79-98. Escos, J.; C. L. Alados; J. M. Emlen. (in press). Developmental instability in the pacific hake parasitized by the myxosporean Kudoa. Trans. Amer. Fish. Soc. Freeman, D. C.; J. H. Graham; J. M. Emlen. 1993. Developmental stability in plants: symmetries, stress, and epigenetic effects. In: Developmental Instability: Origins and Evolutionary Significance. In: Markow, T., ed. Kluwer Academic Publishers. Dordrecht, The Netherlands: 99-122. Graham, J. H.; J. D. Felley. 1985. Genomic coadaptation and developmental (stability within introgressed populations of Enneacanthus gloriosus and E. obesus (Pisces, Centrarchidae). Evolution. 39: 104-114. Graham, J. H. 1992. Genomic co adaptation and developmental stability in hybrid zones. Acta. Zool. Fennica. 191: 121-131. Graham, J. H.; D. C. Freeman; J. M. Emlen. 1993a. Developmental instability: a sensitive indicator of populations under stress. In: Environmental Toxicology and Risk Assessment, ASTM STP 1179. In: Landis, G.; Hughes, G.; Lewis, M. A, eds. American

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