Increased heavy metal and nutrient contamination does not increase fluctuating asymmetry in the seagrass Halophila ovalis

Fluctuating asymmetry (random differences between symmetric structures, FA) is one of the stress indices used recently to assess a subtle effect of environmental degradation on organisms and is expected to increase under stress conditions. In this study, we developed an original technique of measuring FA in seagrass, Halophila ovalis. We analysed five metric and meristic characters on leaves of the seagrass from a polluted and several control locations in a lagoon in Eastern Australia. The seagrass was sampled from three sites at each location. The analyses revealed significant spatial heterogeneity of samples in fluctuating asymmetry with the highest variability was observed among sites. There was no increase in FA of H. ovalis from polluted location. Possible explanations suggest that whether existing concentrations of heavy metals do not cause developmental stress in seagrass or their effect is compensated or even surpassed by effect of uncontrolled factors.     

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.’     

Effects of Short-Term Climatic Variations on Fluctuating Asymmetry Levels in Chironomus Riparius Larvae at a Polluted Site

We examined fluctuating asymmetry (FA) levels in fourth-instar larvae of Chironomus riparius(Diptera, Chironomidae) collected monthly from a polluted site in Galicia (NW Spain) where pollutant inputs are known to be roughly constant throughout the year. The site was selected because, despite this constancy in pollutant inputs, deformities in fourth-instar larvae were previously found to be more frequent and severe during cold periods and less frequent and severe during warm periods of the year, in accordance with the ‘time-of-exposure’ hypothesis. This hypothesis predicts that short-term climatic variations occurring throughout the year influence the frequency and severity of larval morphological alterations, by means of the control they exert on developmental time and, as a consequence, on the time larvae remain exposed to pollutants. We investigated whether FA levels in larvae were likewise in accordance with this hypothesis, but, contrary to our expectations, no significant differences in FA levels were detected either among months or among seasons, suggesting that FA is not influenced by normal climatic variations. However, climatic influences may be masked, and the observed constancy in FA levels over the sampling period may be a consequence of the action of a mixture of stressors which compensate each other.     

Confirmation bias in studies of fluctuating asymmetry

Fluctuating asymmetry (FA) represents small, non-directional deviations from perfect symmetry in morphological characters. FA is generally accepted to increase in response to stress; therefore, FA is frequently used in ecological studies as an index of stress experienced by an organism, in particular due to environmental pollution. We experimentally tested the hypothesis that the outcomes of studies based on FA measurements may have been influenced by confirmation bias, i.e. the tendency of humans to seek out evidence in a manner that confirms their hypotheses and beliefs. We collected 100 leaves of downy birch (Betula pubescens) from a single tree, grouped them haphazardly into ten samples, scanned every sample, and then asked each of 31 scientists (experienced in studying FA) to measure FA from the scanned images of all 100 leaves. Three groups of participants were provided with false information about the origin of each sample and about the hypothesis to be tested, and one group (control) was provided with true information. The participants who believed that the leaves originated from a heavily polluted site reported significantly higher values of FA when compared to the participants who believed that the leaves were collected from an unpolluted site. When the participants were told that half the samples originated from a polluted site and half from a clean site and were asked to attribute each sample to either of these sites based on leaf FA, the differences in FA between samples classified as ‘polluted’ and ‘unpolluted’ were much higher than the differences obtained from measurements of the same sets of samples made by the control group. We conclude that when scientists expected to find high FA in some samples, the results of their measurements confirmed their expectations. This effect, classified as confirmation bias, may considerably influence the outcomes of the research on FA. This confirmation bias can be avoided by using a blind method, where the person conducting measurements is not aware of the origin of samples being measured. We argue that the use of blind methods is critically important for any study addressing environmental or genetic impacts on FA.     

The distribution and abundance of soft-sediment macrobenthos around Casey Station, East Antarctica

Grab samples of shallow (5–35 m) marine benthic sediments and epi- and infaunal assemblages were taken from nearshore regions around Casey Station, Windmill Islands, East Antarctica. A hierarchical, spatially nested sampling design was used with locations (kilometres apart), sites (hundreds of metres apart) and plots (tens of metres). Two potentially impacted, polluted locations (adjacent to a sewage outfall and an old garbage tip) were compared with two control locations in an asymmetrical design. Significant differences in assemblages were found between locations and between sites within locations. Significant differences in the abundances of taxa at several taxonomic levels (species, family, order, phylum) were found at all three spatial scales. Significant differences were also detected between the polluted and control locations. Compared with other Antarctic locations, the assemblages were dominated by crustaceans (90–97% of individuals) and there was a paucity of polychaete fauna at the locations sampled. Accepted: 3 June 2000     

Lizards from Urban Areas Are More Asymmetric: Using Fluctuating Asymmetry to Evaluate Environmental Disturbance

The increase in human activities that leads to wildlife decline and species extinction poses an urgent need for simple indicators of environmental stress in animal populations. Several studies have suggested that fluctuating asymmetry (FA) can be an easy, direct measure of developmental instability because it is associated to environmental stress and, as such, it can be a useful indicator of population disturbance. We examined three different morphological traits in urban and rural populations of the common wall lizard (Podarcis muralis) to test whether anthropogenic disturbance causes an increase in FA. Compared to rural populations, urban ones showed higher levels of FA in all analyzed traits, thus providing evidence that FA can respond to anthropogenic disturbance. However, we also found significant differences in FA among traits, where femoral pores and subdigital lamellae, traits with a functional relevance, were more stable developmentally compared to supracilliar granules which have no evident function. Unsigned FA [abs(right-left)] exhibited significant, but weak, positive correlations among traits, indicating that developmental noise does not have a uniform effect across characters and thus questioning the view of developmental stability as an organism-wide property. The degree of signed FA (right-left) was more similar between structurally associated traits, possibly as an outcome of morphological integration. In conclusion, our results demonstrate that FA can be a reliable indicator of disturbance provided that it is analyzed on multiple traits simultaneously and examined at the population level.     

Developmental stability and morphological differences in Plantago major L. leaves under contrasting environmental conditions

Abstract

In the present study, an additional combination of end‐points was applied on the natural populations of the common plantain, previously estimated using morphometric assays. Here, besides measuring developmental instability (DI), by determining the level of fluctuating asymmetry (FA) and the total amount of phenotypic variability (PV), we tried to distinguish the three natural populations under contrasting environmental conditions using the morphological data. Results obtained using both FA indices were the same; higher asymmetry levels in the reference than in the polluted environments were detected for leaf width, vein distances within a leaf and lobe length. The one‐way analysis of variance results revealed that there were significant differences in PV values among populations analysed for each character. When all leaf traits were considered together, the PV median value was significantly higher in Crni Lug leaves compared with leaves from other sites. The multivariate analysis of variance results revealed the significant effect of environment on both FA₄ and PV values. The component scores of first factor (PC1) were significantly different between the Karaburma and Crni Lug populations. Besides, component scores of both PC1 and PC2 were significantly different between the Zemun and Crni Lug samples. The stepwise discriminant functional analysis results allowed us to identify a set of four variables, with a sufficient discriminating ability (75%).     

Does stress mess with rodents’ heads? Influence of habitat amount and genetic factors in mandible fluctuating asymmetry in South American water rats (Nectomys squamipes,Sigmodontinae) from Brazilian Atlantic rainforest remnants

Loss of developmental stability can lead to deviations from bilateral symmetry (i.e. Fluctuating Asymmetry ‐ FA), and is thought to be caused by environmental and genetic factors associated with habitat loss and stress. Therefore, levels of FA might be a valuable tool to monitor wild populations if FA serves as an indicator of exposure to stress due to impacts of habitat loss and fragmentation. In studies examining FA and habitat fragmentation, FA levels are often explained by loss of genetic variation, though few studies have addressed FA’s use as indicator of environmental impact. Here, we investigated whether habitat loss, genetic variation, and/or inbreeding affect the developmental instability in Brazilian Atlantic forest populations of a Neotropical water rat (Nectomys squamipes). We sampled individuals from eight sites within Atlantic forest remnants with different amounts of available forest habitat and assessed FA levels with geometric morphometric techniques using adult mandibles. We used observed heterozygosity (H_o) and inbreeding coefficient (F_is), from seven microsatellite markers, as a proxy of genetic variation at individual and population levels. Populations were not significantly different for shape or size FA levels. Furthermore, interindividual variation in both shape and size FA levels and interpopulational differences in size FA levels were best explained by chance. However, habitat amount was negatively associated with both interpopulational variance and average shape FA levels. This association was stronger in populations living in areas with <28% of forest cover, which presented higher variance and higher average FA, suggesting that Nectomys squamipes might have a tolerance threshold to small availability of habitat. Our work is one of the first to use FA to address environmental stress caused by habitat loss in small mammal populations from a Neotropical biome. We suggest that shape FA might serve as a conservation tool to monitor human impact on natural animal populations.     

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.     

Rhodnius prolixus and Rhodnius robustus–like (Hemiptera, Reduviidae) wing asymmetry under controlled conditions of population density and feeding frequency

Habitat change in Rhodnius spp may represent an environmental challenge for the development of the species, particularly when feeding frequency and population density vary in nature. To estimate the effect of these variables in stability on development, the degree of directional asymmetry (DA) and fluctuating asymmetry (FA) in the wing size and shape of R. prolixus and R. robustus–like were measured under laboratory controlled conditions. DA and FA in wing size and shape were significant in both species, but their variation patterns showed both inter-specific and sexual dimorphic differences in FA of wing size and shape induced by nutrition stress. These results suggest different abilities of the genotypes and sexes of two sylvatic and domestic genotypes of Rhodnius to buffer these stress conditions. However, both species showed non-significant differences in the levels of FA between treatments that simulated sylvan vs domestic conditions, indicating that the developmental noise did not explain the variation in wing size and shape found in previous studies. Thus, this result confirm that the variation in wing size and shape in response to treatments constitute a plastic response of these genotypes to population density and feeding frequency.     

Experience of applying plant and animal fluctuating asymmetry in assessment of environmental quality in terrestrial ecosystems: Results of 20-year studies of wildlife and anthropogenically transformed territories

The value of fluctuating asymmetry (FA) of trees and small mammals is considered as an indicator of developmental instability. The urban territories with recreation zones, sites with increased radiation background, and the areas affected by mining facilities have been analyzed as anthropogenically transformed areas. The following tree and small mammalian species are the objects of the study: Siberian silver birch (Betula platyphylla), spreading birch (B. divaricata), dwarf birch (B. exilis), shrub alder (Duschekia fruticosa), basket willow (Salix viminalis), northern red-backed vole (Clethrionomys rutilus), tundra vole (Microtus oeconomus), Laxmann’s shrew (Sorex caecutiens), and tundra shrew (S. tundrensis). In total, 60000 leaves have been measured and 3500 rodent sculls have been examined. The issues of selection of bioindicator species and the factors distorting the results of environmental quality assessment according to developmental instability are discussed. A statistically significant increase in FA of plants is recorded in urban territories as compared with the wildlife biotopes. A positive correlation of FA value with transport load, concentration of heavy metals in soil, and atmospheric air pollution is observed. The proximity to a roadway and the state of road pavement influence the FA value. The main source of pollution in the administrative center (Yakutsk) is motor vehicles; correspondingly, large streets and crossroads with a high transport load are the most polluted sites. As for the industrial center (city of Mirnyi), pollution spreads from the areas affected by mining to the residential area. The main pollution source in a small administrative center (city of Aldan) is the federal highway. It is recommended to concurrently use the FA characteristics of plant and animals in the area affected by the mining industry. Characteristic of this industry is withdrawal of large areas of natural landscapes; typically, transformed plots alternate weakly affected plots. The specific features of the effects of diamond, gold, and coalmining industries, as well as oil and gas field development, are discussed, which should be taken into account in sampling for bioindication. The problem of bioindication in the areas completely devoid of soil and plant cover can be solved by biotesting via assessment of bunching onion seed germination rate and the rate of mitotic aberrations. An increase in the FA level in trees and small mammals is observed in the areas transformed by the mining industry displaying a chronically increased radiation background and oil-polluted as a result of technogenic accidents. The use of FA index makes it possible to estimate the environmental quality and to compare the state of territories located under different natural and climatic conditions and influenced by multicomponent anthropogenic impacts differing in their strength and genesis, which interferes with their comparison.     

Ethoxyresorufin O-deethylase (EROD) activity and fluctuating asymmetry (FA) in Zosterisessor ophiocephalus (Teleostei, Gobiidae) as indicators of environmental stress in the Venice lagoon

The impact of environmental stress on the grassgoby, Zosterisessor ophiocephalus, wasstudied at both biochemical and morphologicallevels, by comparing three sites in the Venicelagoon (the Northern, Central and Southernbasins) which differ in terms of the degree ofanthropogenic disturbance, in particular withregard to organic sediment contamination. At abiochemical level, the hepatic ethoxyresorufinO-deethylase (EROD) enzyme activity wasmeasured as a biomarker of the degree oforganic pollution (in particular regardingcontamination by PCBs and Dioxins). At amorphological level, the amount of fluctuatingasymmetry (FA) with regard to four bilateraltraits (postorbital length; otolith area;minimum otolith diameter; maximum and minimumotolith radii) was measured as a long termindicator of developmental stress. The ERODactivity was higher in grass gobies from theCentral basin, whereas the amount of FA washigher in the gobies collected from theNorthern basin. Both measurements indicatedthat the Southern basin was affected by lowlevels of environmental stress (low ERODinduction and a lower amount of FA). Theresults were discussed in the light of both theenvironmental differences among the threebasins and the different levels of biologicalorganisation at which the two indicators act.     

Leaf developmental stability of Platanus acerifolia under urban environmental stress and its implication as an environmental indicator

The developmental stability indices, leaf width based fluctuating asymmetry (FA1), and lateral vein length based directional asymmetry (RDA1) of Platanus acerifolia were studied. All the leaves were sampled from 14 sites that were categorized based on different urban environmental stress levels (UESL) in Shanghai metropolitan, China. Besides, foliar stomatal density and stomatal length were also studied as the subsidiary indices to test the availability of developmental stability indices as the indicator under a stressful environment. Results showed seasonal variation of FA1 and RDA1 existed among the 14 sites, but the data showed significant negative correlation between FA1 and UESL (FA1 = 0.029 − 0.000 9UESL + 0.000 3UESL², r = 0.766 5, P = 0.001 4). However, a similar trend was not found between RDA1 and UESL. Furthermore, the significant correlation among FA1 and leaf stomatal length and stomatal density implied they could be used as indicators of urban stress levels on a small scale. It seemed that RDA1 was possibly a normal parameter during leaf development but it was unavailable for use as an indicator of urban stresses. __________ Translated from Chinese Journal of Ecology, 2005, 24(7): 719–723 [译自: 生态学杂志, 2005, 24(7): 719–723]     

Diversity of Bacteroides fragilis Strains in Their Capacity To Recover Phages from Human and Animal Wastes and from Fecally Polluted Wastewater

Great differences in capability to detect bacteriophages from urban sewage of the area of Barcelona existed among 115 strains of Bacteroides fragilis. The capability of six of the strains to detect phages in a variety of feces and wastewater was studied. Strains HSP40 and RYC4023 detected similar numbers of phages in urban sewage and did not detect phages in animal feces. The other four strains detected phages in the feces of different animal species and in wastewater of both human and animal origin. Strain RYC2056 recovered consistently higher counts than the other strains and also detected counts ranging from 10¹ to approximately 10³ phages per ml in urban sewage from different geographical areas. This strain detected bacteriophages in animal feces even though their relative concentration with respect to the other fecal indicators was significantly lower in wastewater polluted with animal feces than in urban sewage.     

Fluctuating feather asymmetry in relation to corticosterone levels is sex-dependent in Eurasian treecreeper (Certhia familiaris) nestlings

Fluctuating asymmetry (FA) has been widely used as a stress-related phenotypic marker of developmental instability. However, previous studies relating FA to various stressful conditions have produced inconsistent results and we still lack quantitative individual-level evidence that high FA is related to stress in wild vertebrate species. We studied how baseline plasma levels of corticosterone predicted FA of wing and tail feathers in free-living Eurasian treecreeper (Certhia familiaris) nestlings. We found a sex-specific association between corticosterone levels and FA: high corticosterone levels were related to an increased FA in male but not in female nestlings. These results suggest that in treecreepers, FA may correlate with individual stress hormone levels, male developmental trajectory being potentially more sensitive to stress than that of the female.     

Does fluctuating asymmetry constitute a sensitive biomarker of nutritional stress in house sparrows (Passer domesticus)?

Small random deviations from left–right symmetry in bilateral traits, termed fluctuating asymmetry (FA), are theoretically predicted to increase with environmental stress and believed to constitute a potential biomarker in conservation. However, reported relationships between FA and stress are generally weak and variable among organisms, traits and stresses. Here we test if, and to what extent, FA increases with nutritional stress, estimated from independent feather growth measurements, in free-ranging house sparrows (Passer domesticus). Ptilochronological feather marks showed significant heterogeneity among study plots, indicating that house sparrow populations were exposed to variable levels of nutritional stress during development. However, individuals from more stressed populations did not show increased levels of fluctuating asymmetry in tarsus or rectrix length, nor was there evidence for significant between-trait concordance in FA at the individual or the population level. Lack of support for FA in tarsus and rectrix length as estimator of nutritional stress in house sparrows may indicate that developmental instability is insensitive to nutritional stress in this species, poorly reflected in patterns of fluctuating asymmetry due to ecological or statistical reasons, or highly context-specific. Such uncertainty continues to hamper the use of FA as a biomarker tool in conservation planning.     

Primary productivity of the River Ely,South Wales,U.K.

The present study was carried out on the non-tidal reaches of the River Ely, South Wales, from October 1979 to October 1980. The seasonal variations of the chlorophyll-a content of the phytoplankton was unimodal with one maximum in May and a minimum in December. The chlorophyll-a content varied from 0.277 to 41.259 mg m^?3. The primary productivity showed a bimodal seasonal distribution with two maxima in May and September and lower values throughout the remainder of the year, particularly in winter. The value for the primary productivity varied from 0.269 to 24.302 mg C m^?3 h^?1. A positive correlation was obtained between chlorophyll-a content and primary productivity. The seasonal distribution of the dominant algal species and the saprobity of the River Ely were also studied. The diatom species almost showed a similar seasonal periodicity. Their concentrations were low during the winter months and high during most of the spring and summer months. Many of the dominant diatom species found in the phytoplankton populations were either considered by the other authors as saprobic (Nitzchia palea) or as inhabitants of eutrophic waters (Gomphonema parvulum, Navicula cryptocephala and Synedra ulna). Chlamydomonas spp. were the most abundant green algae followed by Chlorella vulgaris. The effect of sewage effluent disposal and cattle excreta at three of the sampling sites might partly explain the presence of high Chlamydomonas spp. populations at those sites. Physical factors (low flow rates, high transparency and water temperature) and organic pollution at some sampling sites seemed to play an important role in increasing the number of algal species during spring and summer. The non-tidal reaches of the River Ely were found to be β-mesosaprobic above and below Station 5 and α-mesosaprobic at the latter station and therefore, the river can be considered as polluted at Station 5 and mildly polluted at the others.     

Patterns of leaf asymmetry changes in Plantago major L. (ssp. major) natural populations exposed to different environmental conditions

In the present study, developmental stability of leaf traits was examined in three natural populations of Plantago major L. (ssp. major), representing two polluted environments (Karaburma and Zemun) and an unpolluted area (Crni Lug). Developmental stability was assessed as fluctuating asymmetry (FA). The magnitude of FA is believed to reflect differences in the ability of individuals to buffer their development in natural populations. We hypothesized that there are differences within characters and among characters in response to environmental conditions. Significant patterns of asymmetry correlations and asymmetry changes were detected both within characters and between characters. The manova results revealed a significant effect of individual and a significant individual × environment interaction on actual asymmetry (logL_i ? logR_i) and on the amount of asymmetry |(logL_i ? logR_i)| for leaf width and vein distances within a leaf. Over time, statistically significant and positive correlations of the FA values were detected for each trait separately per sample (population). For both leaf traits, there were differences for (logL_i ? logR_i) and |(logL_i ? logR_i)| asymmetry values among individuals within samples in response to yearly variations. Statistically significant and negative correlations for (logL_i ? logR_i) versus |(logL_i ? logR_i)| asymmetries were detected for both leaf traits. In summary, our results highlight the importance of differences in the ability of individuals to buffer their development under different environmental conditions and point to the concept that developmental stability is character specific.     

Seasonal and spatial patterns in cellular energy allocation in the estuarine mysid Neomysis integer (Crustacea: Mysidacea) of the Scheldt estuary (The Netherlands)

The seasonal and spatial patterns in cellular energy allocation of the estuarine mysid Neomysis integer (Leach, 1814) were investigated in the Scheldt estuary over a 2-year period. Using the recently developed cellular energy allocation (CEA) assay, energy reserves (protein, lipid and sugar) and energy consumption (as derived from the cellular respiration rate) were integrated into a general indicator of physiological stress. Total energy reserves were relatively unaffected by sampling season or location, whereas the individual energy reserve fractions of N. integer were differentially influenced by sampling location and season. Seasonal effects were apparent for mysid weight and were related to the population biology, whereas spatial effects on the weight of N. integer may depend on pollution-induced effects on cellular energy allocation in the two most upstream sites (Bath and Doel). These upstream sites coincide with the most polluted part of the sampled area and were characterized by a significant increase in energy consumption, resulting in a significantly lower CEA. Due to the recent amelioration in the oxygen concentration at these sites, it can be expected that N. integer will migrate further upstream, similar to what is observed in other European estuaries. It will, therefore, be important to assess the physiological consequences and potential population effects on mysids from these polluted areas in the Scheldt estuary. This study provides evidence that the CEA assay has potential under field conditions as an in situ biomarker of pollutant effects.