Fluctuating asymmetry as an ecological indicator of heavy metal stress in Lythrum salicaria

Fluctuating asymmetry (FA), a measure of random deviation of organismal traits from perfect bilateral symmetry, can be induced by environmental and/or genetic stress. We have conducted a replicated experiment to test the effect of a locally abundant heavy metal pollutant, lead, on the FA of a common wetland invasive species, Lythrum salicaria (purple loosestrife). The exposure to lead significantly reduced the shoot length, number and length of leaves as well as the biomass, but increased FA of L. salicaria leaves. The investigation suggests that FA in L. salicaria may be used as an ecological indicator to identify environmental stress caused by certain heavy metal pollutants. However, more studies are needed for the use of FA in L. salicaria as a comprehensive tool for biomonitoring of a wider array of environmental pollutants.     

Fluctuating asymmetry in the otoliths of larval fish as an indicator of condition: conceptual and methodological aspects

Developmental instability, measured as fluctuating asymmetry (FA) in bilateral traits, has been used widely as an indicator of genetic or environmental stress in a variety of plant and animal taxa. FA arises as small deviations from perfect bilateral symmetry which reflect 'mistakes' in developmental processes resulting from the inability of the genotype to buffer itself effectively against environmental perturbations. Recently, it has been proposed that FA in the otoliths can be used as an indicator of condition in larval fish. This paper reviews the conceptual and methodological aspects of FA relevant to its potential use as a measure of well-being. Its simplicity makes FA an attractive tool to measure developmental precision and condition. However, there are several pitfalls, such as measuring error or potentially size dependence. Subtle asymmetries, i.e. between sides variation of a trait at the individual level, may not always be indicative of condition and should be interpreted with caution. The past-growth record of otoliths may provide a powerful means of studying the development of asymmetries at the level of the individual.     

Fluctuating asymmetry as a bio-marker to account for in conservation and management of cave-dwelling species

The applicability of fluctuating asymmetry (FA) in conservation biology as a bio-marker and an early warning system have been examined in various groups of animals. However, cave-dwelling invertebrates have gotten little attention and yet caves have no biological management. Thus, developing a bio-marker to identify early responses of cave-dwelling species to stress provides a valuable tool to account for in future conservation and management programs. We examined whether FA can be used as a bio-marker of relaxed selection for cave-dwelling invertebrates. Specifically, we compared FA levels of pedipalps and two segments of chelicerae (chelicel1 and chelicel2) between cave and surface habitats and among populations in a troglophilic harvestman specie, Paranemastoma sillii sillii (Herman, 1871). Under the assumption that cave environment exerts relaxed selection we hypothesised that cave-dwelling harvestmen express higher degree of FA than surface-dwelling harvestmen. Because female and male harvestmen use the pediplaps differently, we assumed sex-specific selective pressures and further examined the effect of sex and habitat (cave vs surface) and sex interaction on FA levels. We hypothesised no differences in the levels of FA among harvestman cave populations, because of the idea that relaxed selection is responsible for higher levels of FA in cave-dwelling harvestmen rather than environmental stress. We found significant habitat sex interactions in the FA of the pedipalp. Interactions of population and sex had a significant effect on pedipalp and chelicel2 FA. These results partially support the idea that FA responds to differences in the strength of selection. Although we cannot fully disentangle the mechanisms of natural selection affecting FA and the study of trait asymmetry should be combined with studies of other sources of stress (i.e. genetic stress, predation, prey availability) we conclude that FA could be a bioindicator to be used as a tool in conservation and management of cave.     

Fluctuating asymmetry of leaves is a poor indicator of environmental stress and genetic stress by inbreeding in Silene vulgaris

Fluctuating asymmetry (FA) is often used as a measure of developmental instability and has been proposed as an indicator of both environmental and genetic stress. However, the empirical evidence for the effects of stress on FA in plants is inconsistent, and there are few controlled experimental studies. We analyzed different distance- and shape-based measures of the fluctuating asymmetry of the leaves of clonally replicated self- and cross-pollinated lineages of Silene vulgaris (Moench) Garcke (Caryophyllaceae) grown under a control and seven different stress treatments (drought, copper, simulated herbivory, and two levels of nutrient deficiency and of shade). Overall, FA differed among stress treatments, but was not generally higher under stress and even reduced in some treatments. Different measures of FA were only weakly correlated. Inbreeding increased only one measure of leaf FA, and only under high stress intensities. Our findings suggest that in S. vulgaris leaf fluctuating asymmetry does not serve as an indicator of environmental stress or of genetic stress by inbreeding.     

Bilateral asymmetry in skeletal growth and maturation as an indicator of environmental stress.

This study examined the efficacy of bilateral asymmetry in epiphyseal union as an indicator of environmental stress affecting the skeleton. We compared the extent of asymmetry in the postcranial skeleton between two cemetery samples excavated from Medieval Kulubnarti, Sudanese Nubia. Past studies have strongly suggested that these ancient Nubians experienced environmental stress-the early Christian period (550-750 AD) population to a greater extent than the late Christian period (750-1450 AD) population. We hypothesized that if bilateral asymmetry is a reflection of stress, then it should be present or greater in the more stressed population, the early Christian period population, while absent or found to a lesser extent in the less stressed population, the late Christian period population. We computed two mean values, representative of right-side and left-side epiphyseal union, for each individual in both cemetery samples, and tested for significant differences. Bilateral asymmetry was significant in the combined cemetery sample of 90 individuals (P < 0.019). When cemetery samples were tested separately, bilateral asymmetry was significant for the early Christian period sample (P < 0.001), but not for the late Christian period sample. There were no differences attributable to sex. Finally, we discuss why we conclude that environmental stress was favored over a biomechanic explanation as the cause for asymmetry. To the extent that our results support previous findings that early Christian period individuals were more affected by environmental stress than late Christian period individuals, it is reasonable to consider bilateral asymmetry in skeletal growth and maturation a good indicator of environmental stress.     

Fluctuating asymmetry and exogenous stress in fishes: a review

Fluctuating asymmetry (FA), which has been examined in a variety of plants and animals, is widely promoted as a useful bioindicator of exogenous stressors in habitats, whether of natural or anthropogenic origin. Wildlife managers and researchers often use a specific group of organisms as an indicator of the health of a given habitat. The purpose of this review is to demonstrate that FA can be an effective fish biomonitoring tool by presenting a vote counting meta-analysis of 81 fish FA studies published between 1966 and the first half of 2009. The vote counts were analyzed with the G test for independence to determine whether the probability of observing significant morphological asymmetry is determined by character type, exogenous stressor type, or fish order. The information obtained from these papers and their analysis is then used to outline areas in which FA studies can be improved: (1) carefully considering character choice; (2) distinguishing between asymmetry types; (3) determining the level of measurement error in between-sides character variation; (4) determining baseline FA levels in populations; (5) increasing the number of laboratory studies which corroborate field observations of FA; (6) conducting true replications of studies to validate previous findings. Only with more critical experimental design and data analysis can FA be used as a powerful tool for assessing environmental degradation.     

Fluctuating asymmetry does not reflect environmental stress during incubation in an oviparous lizard

Abstract

We analysed the relationship between incubation regime and fluctuating asymmetry in a cohort of juvenile lizards (Oligosoma suteri) incubated under laboratory conditions. We found no relationship between incubation temperature or water potential and the level of asymmetry in two cranial traits, although previous research showed profound effects of incubation temperature on gross morphology and hatching success. Our results suggest that fluctuating asymmetry is not a reliable indicator of developmental stress in this species.     

Fluctuating asymmetry and stress in a medieval Nubian population

Fluctuating asymmetry is commonly used as a bioindicator of developmental stress. This study addresses asymmetry under nutritional/systemic stress in the human craniofacial skeleton and its utility as an indicator of developmental instability. Crania from the diachronic Christian cemeteries at Kulubnarti (Sudanese Nubia) were chosen as a model for nutrition/systemic stress. Previous studies indicate that individuals from the Early Christian cemetery were subjected to greater developmental stress when compared with individuals from the Late Christian cemetery. Therefore, crania from the Early Christian cemetery should display a greater magnitude of fluctuating asymmetry than crania from the Late Christian cemetery. Thirty adult crania of comparable age and sex were selected from each population. Landmark coordinates were digitized in two separate trials and averaged to minimize error. Euclidean distance matrix analysis (EDMA) was used to measure and compare the magnitude of fluctuating asymmetry in each sample. Results indicate that crania from the Early Christian cemetery display greater amounts of fluctuating asymmetry than those from the Late Christian cemetery, as predicted. The degree of fluctuating asymmetry for each linear distance is highly correlated between the cemeteries, suggesting that all humans may share common patterns of fluctuating asymmetry in the skull. In contrast, there is little correlation between magnitude of fluctuating asymmetry and length of linear distance, between-subject variability, or measurement error. These results support the hypothesis that poor nutrition/systemic stress increases developmental instability in the human skull and that increased fluctuating asymmetry constitutes morphological evidence of this stress.     

Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future

The role of developmental instability (DI), as measured by fluctuating asymmetry (FA), in evolutionary biology has been the focus of a wealth of research for more than half a century. In spite of this long period and many published papers, our current state of knowledge reviewed here only allows us to conclude that patterns are heterogeneous and that very little is known about the underlying causes of this heterogeneity. In addition, the statistical properties of FA as a measure of DI are only poorly grasped because of a general lack of understanding of the underlying mechanisms that drive DI. If we want to avoid that this area of research becomes abandoned, more efforts should be made to understand the observed heterogeneity, and attempts should be made to develop a unifying statistical protocol. More specifically, and perhaps most importantly, it is argued here that more attention should be paid to the usefulness of FA as a measure of DI since many factors might blur this relationship. Furthermore, the genetic architecture, associations with fitness and the importance of compensatory growth should be investigated under a variety of stress situations. In addition, more focus should be directed to the underlying mechanisms of DI as well as how these processes map to the observable phenotype. These insights could yield more efficient statistical models and a unified approach to the analysis of patterns in FA and DI. The study of both DI and canalization is indispensable to obtain better insights in their possible common origin, especially because both have been suggested to play a role in both micro- and macro-evolutionary processes.     

Bone histology as an approach to providing data on certain key life history traits in mammals: Implications for conservation biology

The knowledge of the life histories of wild mammals is of crucial importance in the field of conservation management. The endangered status of many species calls for faster data collection that can be used in risk assessment and, ultimately, for designing conservation policies. This study is pioneering the potential of bone histology to provide data on life history traits crucial for conservation biology in long-lived mammals. Long bone cross-sections show pronounced annual cycles of growth arrest allowing application of skeletochronology (counts of lines of arrested growth ‘LAGs’). Consequently, the number of LAGs within the primary fast-growing bone tissue up to the outer cortical slow-growing bone tissue corresponds to the age at first reproduction; whereas the age at death can be estimated by the total number of rest lines throughout the whole of bone cross-section. Furthermore, the diameters of successive growth rings as well as the osteocyte lacuna density may shed light on growth rates. We use the endangered desert dwelling antelope Addax nasomaculatus as a case study. By analyzing different ontogenetic stages in five Addax individuals (three captive and two wild specimens) from a museum collection, we show that bone histology may be a reliable tool for determining certain key life history traits. In our sample, the wild Addax female attained reproductive maturity at three years, whereas the male specimens, both the captive and the wild ones, reached maturity at four years. This is congruent with data from other large antelopes with male-biased size dimorphism, but differs slightly from data on sexual maturity previously published for wild Addax. Moreover, quantification of osteocyte lacunae in both adult males provides a higher cell density in the captive one than in the wild one suggesting the strong effect of constant resources supply in individuals from zoos on growth rates. While age at first reproduction and longevity are essentials parameters to carry out demographic models, growth rates may allow evaluation of the health status of wild populations. This approach may provide useful data on life history traits when applied to bones collected in the wild.     

Fluctuating asymmetry of sexual and nonsexual traits in stalk‐eyed flies: a poor indicator of developmental stress and genetic quality

It has been proposed that females use fluctuating asymmetry (FA) in sexual ornaments to assess male quality. FA of sexual traits is predicted to show greater sensitivity to stress than FA of nonsexual traits, and to be heritable. We used a half‐sib mating design and manipulation of larval food environment to test these predictions on stalk‐eyed flies, Cyrtodiopsis dalmanni, in which females prefer males with larger eyespans. We measured size and FA of eyestalks and of two nonsexually selected characters, wing length and width. We found no evidence of an increase in FA under larval food stress in any of the individual traits, although trait size decreased under stress. We combined FA across traits into a single composite index, and found that males reared in the most benign larval environment had significantly higher composite FA than males reared on other media. There was no such effect in females. Heritability of FA was not significantly different from zero in any of the traits, in any of the environments, although trait sizes showed high heritability. We conclude that FA in sexual and nonsexual traits is a poor indicator of developmental stress and genetic quality.     

Fluctuating asymmetry as an indicator of elevation stress and distribution limits in mountain birch (<Emphasis Type="Italic">Betula pubescens</Emphasis>)

Fluctuating asymmetry (FA) has been suggested as a useful indicator of elevation stress and, hence, distribution limits in plants. However, no plant studies have been carried out to test (i) whether FA shows a gradual increase towards the alpine distribution limit and (ii) whether FA responds to elevation stress independent of other stressors which is necessary for FA to be a useful indicator in this context. To test these two hypotheses, this 2-year field study investigated the dose–response relationship between elevation stress and FA in mountain birch (Betula pubescens) under contrasting levels of insect attack in northern Norway. The results showed that FA increased linearly from sea level towards the tree line in both years independent of insect attack, which had no observable effect on FA, i.e. insect attack did not appear to disturb the FA-elevation relation. Thus, in mountain birch, FA appeared to be a reliable indicator of elevation stress. Further investigation is now needed in order to develop this hypothesis.     

Leaf fluctuating asymmetry of common plantain as an indicator of habitat quality

Abstract

Although developmental instability (DI), measured as fluctuating asymmetry (FA), is expected to be positively related to environmental stress and negatively to habitat quality, the pattern found here was the reverse. Developmental instability of leaf traits (leaf width and vein distances within a leaf) was estimated (using two indices of FA: FA₄ and σ_i ²) and compared between three populations of Plantago major L. (Plantaginaceae) from northern Serbia. Two of the populations are from chronically polluted areas (Karaburma & Zemun), while Crni Lug is from an unpolluted, natural area. Results obtained using both FA indices were the same; higher asymmetry levels in the unpolluted area than in the polluted sites, were found for both traits. Between the two polluted sites, FA values were significantly higher in Karaburma site for vein distances within a leaf. Concerning differences in FA₄ values between samples, in two cases, results are similar to those found for σ_i ² values, for vein distances within leaf. These are the first quantitative data on P. major indicating that (i) plants living in the stressful sites are more symmetrical and (ii) leaf FA for plant species with wide ecological distribution such as P. major should be considered as an ‘index of habitat quality.’     

Wing shape versus asymmetry as an indicator of changing environmental conditions in insects

Abstract In insects, the fluctuating asymmetry of bilaterally symmetrical traits has been suggested as an indicator of environmental stress because asymmetry is expected to increase when stressful conditions disturb the normal development of organisms. However, the extensive literature on asymmetry–stress associations is indeterminate. Here we contrast changes in asymmetry with changes in an alternate stress indicator, the shape of insect wings. The development of wing shape involves numerous genes that act throughout egg-to-adult development, so stresses that act at a specific time could alter shape in specific ways. Shape changes, as measured by the Procrustes technique, were considered in five data sets: exposure of Drosophila melanogaster (Meigen) to multiple stresses involving ethanol, low nutrition and cold shocks; exposure of a chironomid ( Chironomus tepperi (Skuse)), a blowfly ( Lucilia cuprina (Wiedemann)), and lightbrown apple moth ( Epiphyas postvittana (Walker)) to pesticides; and development of C. tepperi under saline conditions. All these conditions influenced viability and development time. In none of these cases was a change in symmetry of wing size or wing shape detected. In contrast, in four of the five data sets there was a change in wing shape. These results suggest that wing shape may be altered more commonly by stress than trait asymmetry. Wing-shape monitoring may be useful in detecting stressful environmental conditions during development, at least under controlled conditions.     

Fluctuating dental asymmetry: Variation among skeletal populations

Recent investigations have shown that nongenetic, environmental factors can adversely affect dental growth and produce bilateral asymmetries in tooth size. When asymmetries do not favor either side, i.e., absence of directional asymmetry, the condition is termed fluctuating asymmetry. Fluctuating asymmetry of the mesiodistal and buccolingual dimensions of the total permanent dentition was compared among human skeletal populations which differ socio-economically and nutritionally. Odontometric data were collected from prehistoric hunters (Indian Knoll site), later aboriginal farming groups (Campbell and Larson sites), and a modern cadaver population (Hamann-Todd). The magnitude of asymmetry is expressed by the familiar correlation coefficient, r. The proportion, then, of intra-individual variation due to fluctuating asymmetry is equal to 1-r. With Wilcoxon's signed ranks test on the correlation coefficients no significant sex difference was shown within populations. Among groups, though, Indian Knoll was the most odontometrically asymmetrical; moreover, within Indian Knoll, the taller and ostensibly better nourished individuals had larger, less asymmetrical teeth than the shorter individuals. These results suggest that environmentally mediated growth disturbance may be sensitively reflected by dental asymmetry. A population exhibiting other signs of severe growth disturbance, e.g., enamel hypoplasia and Harris lines, was the most dentally asymmetrical.     

Fluctuating dental asymmetry as a measure of odontogenic canalization in man

Fluctuating odontometric asymmetry was evaluated in 202 Lengua Indians and in 125 contemporary caucasoids using Euclidean map analyses, rescaled asymmetry values, and Naperian logarithmic transformations. Both populations showed bimodal distributions of canalizing ability, with significantly more Lengua Indians being less well canalized. Student t-tests indicated that significant interpopulation differences in rescaled asymmetry values centered around maxillary mesiodistal dimensions. Analyses of variance failed to show significant levels of sexual dimorphism in the magnitude of asymmetry for both populations. It is concluded that even in a relatively stress-free population, there exist some individuals who are less well canalized than others. When a population is subjected to elevated levels of parasitic and nutritional stress, the number of less-well-canalized individuals increases significantly.