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The effects of radiation on sperm swimming behavior depend on plasma oxidative status in the barn swallow (Hirundo rustica)
Abstract
Sperm are highly susceptible to reactive oxygen species (ROS) that can damage sperm DNA and structure, resulting in reduced fertilizing capacity. Exposure to radioactive contamination can also impair sperm swimming behavior and fertilizing ability, both through a reduction of sperm DNA integrity and via an increased generation of reactive oxygen species (ROS). However, the relationship between individual oxidative status and sperm swimming behavior has never been investigated in any wild population of animals exposed to radioactive contamination. We studied the motility of sperm collected from barn swallows, Hirundo rustica, breeding under different levels of radioactive contamination following the Chernobyl accident in 1986, in relation to individual oxidative status. We tested the hypothesis that the degree of impairment of sperm swimming behavior by radioactive contamination depended on plasma antioxidant capacity, the level of reactive oxygen metabolites (ROMs) and oxidative stress (sensu Costantini et al. 2006), a better oxidative status being associated with higher sperm motility. Sperm behavior parameters were subjected to principal component (PC) analysis, which extracted four PCs explaining 86% of the variance in sperm motility. PC2, representing sperm with high track velocity and ample lateral head displacement, was significantly predicted by the interaction between radiation level and either oxidative damage or oxidative stress. Contrary to our predictions, the highest values of PC2 were associated with relatively high radiation levels, particularly for high levels of either ROMs or oxidative stress. In addition, there was a tendency for values of PC3 (representing the percent of motile sperm) and PC4 (representing slow sperm with high beat cross frequency) to depend on the interaction between radiation level and total plasma antioxidant protection. Our results confirm the importance of oxidative status in determining the genetic and physiological outcome of exposure to radioactive contamination, complementing previous studies relating sperm abnormality to circulating levels of specific antioxidants. Our results also complement previous evidence that oxidative damage of sperm was negatively related to sperm motility, thus indicating a possible trade-off in quenching pro-oxidant compounds in the plasma and the seminal fluid.
... Also known as the single-cell gel electrophoresis test, the 'comet assay' is an inexpensive cytogenetic test at the level of individual cells that is applicable to virtually any cell line, and is frequently employed as a sensitive biomarker of a variety of categories of damage to the DNA molecule (Tice et al., 2000). The oxidative status of individual barn swallows was also related to the quality of their sperm, suggesting the potential for effects of radiation to be transmitted to the next generation (Bonisoli Alquati et al., 2011). Given its special place in indicating radiation effects across generations, studies on sperm motility in bird species are outlined separately. ...
... However, such oxidative burst might damage spermatozoa and impair sperm motility (Armstrong et al., 1999). Further, exposure to low dose radiation increase oxidative stress and results in impaired ejaculate quality and sperm motility (Cheburakov & Cheburakova, 1993;Møller et al., 2008b;Sakharov et al., 2009;Bonisoli Alquati et al., 2011;Møller et al., 2014). This suggests that in addition to a damaging effect on DNA integrity due to radiation, excessive ROS production in exposure to radiation may overwhelm the antioxidant defences, and cause infertility or impaired sperm quality (Bonisoli Alquati et al., 2011). ...
... Further, exposure to low dose radiation increase oxidative stress and results in impaired ejaculate quality and sperm motility (Cheburakov & Cheburakova, 1993;Møller et al., 2008b;Sakharov et al., 2009;Bonisoli Alquati et al., 2011;Møller et al., 2014). This suggests that in addition to a damaging effect on DNA integrity due to radiation, excessive ROS production in exposure to radiation may overwhelm the antioxidant defences, and cause infertility or impaired sperm quality (Bonisoli Alquati et al., 2011). ...
This chapter presents an overview of biomarkers and ecological indicators
used to measure radiation stress in invertebrates. Using examples, we will show
how and in what context the different biomarkers can be used and on which invertebrate
species. We will also describe how the biomarker techniques can be adapted
from other taxa including humans and developed for use in invertebrate species.
Biomarkers generally fall into two categories – biomarkers for exposure and effect.
Invertebrates have not frequently been used to investigate radiation-induced stress
but they offer great potential. Here, we present biomarkers that have been used in
different ecotoxicological contexts and are appropriate for measuring radiation
exposure: comet assay, micronucleus assay, cytochrome p450 and oxidative stress.
The majority of previous studies that have used biomarkers for environmental
stressors have been conducted on either mussel for aquatic systems or earthworms
in terrestrial systems. We also present an overview of how ecological indicators
benefit understanding of the consequences that radiation exposure to individuals
living in contaminated environments, focussing on alterations to reproduction and
behaviour.
... Also known as the single-cell gel electrophoresis test, the 'comet assay' is an inexpensive cytogenetic test at the level of individual cells that is applicable to virtually any cell line, and is frequently employed as a sensitive biomarker of a variety of categories of damage to the DNA molecule (Tice et al., 2000). The oxidative status of individual barn swallows was also related to the quality of their sperm, suggesting the potential for effects of radiation to be transmitted to the next generation (Bonisoli Alquati et al., 2011). Given its special place in indicating radiation effects across generations, studies on sperm motility in bird species are outlined separately. ...
... However, such oxidative burst might damage spermatozoa and impair sperm motility (Armstrong et al., 1999). Further, exposure to low dose radiation increase oxidative stress and results in impaired ejaculate quality and sperm motility (Cheburakov & Cheburakova, 1993;Møller et al., 2008b;Sakharov et al., 2009;Bonisoli Alquati et al., 2011;Møller et al., 2014). This suggests that in addition to a damaging effect on DNA integrity due to radiation, excessive ROS production in exposure to radiation may overwhelm the antioxidant defences, and cause infertility or impaired sperm quality (Bonisoli Alquati et al., 2011). ...
... Further, exposure to low dose radiation increase oxidative stress and results in impaired ejaculate quality and sperm motility (Cheburakov & Cheburakova, 1993;Møller et al., 2008b;Sakharov et al., 2009;Bonisoli Alquati et al., 2011;Møller et al., 2014). This suggests that in addition to a damaging effect on DNA integrity due to radiation, excessive ROS production in exposure to radiation may overwhelm the antioxidant defences, and cause infertility or impaired sperm quality (Bonisoli Alquati et al., 2011). ...
Birds are regarded as excellent bioindicators of anthropogenic environmental change, including changes due to the release of toxicants into ecosystems. Consistent with this, birds are among the best-studied groups of organisms under conditions of radioactive contamination. This includes the study of radionuclide transfer to their bodies as well as the estimation of the associated radiation doses. This paper reviews the literature on the use of birds in studies of radiation exposure, and the effects of low-dose, low-dose rate ionizing radiation on birds. A variety of effects have been documented on birds exposed to ionizing radiation under ecological conditions. These studies, mostly in the context of the nuclear accidents of Chernobyl and Fukushima, are organized based on the level of biological organization analyzed, from molecular and cytological studies, to physiological, behavioral and life-history effects. We also discuss the translation of these effects into consequences at the level of populations and communities, and examine how avian species vary in their exposure and susceptibility. We conclude by suggesting future avenues of research, including the development of molecular and –omics biomarkers that will increase the sensitivity of retrospective dosimetry, and aid the detection of low-dose effects.
... In stallion spermatozoa, Ghosh et al. [84] recently found that UV light induces lipid peroxidation irrespectively of the media and assays used. Additionally, the exposure to ionizing radiation, which arose after the nuclear power plant accidents of Chernobyl (Ukraine) in 1986 and Fukushima Daiichi (Japan) in 2011, has provoked a decline in richness and abundance of several animal species that may at least partly be mediated by the impact of oxidative stress on reproductive function [85,86]. To date, however, no negative effects on spermatogenic and sperm function have been observed in wildlife (in raccoons, Procyon lotor: [87]) and livestock (bull: [88]) inhabiting the contaminated areas closed to Fukushima, probably as a result of different exposure features and reduced multigenerational mutation accumulation in the latter compared to Chernobyl's fauna [85,89]. ...
... For instance, the incidence of aspermia is around 18% in birds breeding in Chernobyl compared to 3% found in control sites [186]. Interestingly, in the male barn swallow (Hirundo rustica), sperm length is shorter in individuals breeding in the radioactively contaminated area compared to the control site [185], the radiation levels being associated with oxidative stress and impaired sperm swimming pattern (i.e., high curvilinear velocity and lateral head displacement) in this species [86,187]. ...
Oxidative stress occurs when the levels of reactive oxygen species (ROS) overcome the antioxidant defenses of the organism, jeopardizing several biological functions, including reproduction. In the male reproductive system, oxidative stress not only impairs sperm fertility but also compromises offspring health and survival, inducing oxidative damage to lipids, proteins and nucleic acids. Although a clear link between oxidative stress and male fertility disorders has been demonstrated in humans and laboratory rodents, little information is available about the implications of impaired redox homeostasis in the male fertility of domestic and wild animals. Therefore, this review aims to provide an update regarding the intrinsic and extrinsic factors that are associated with oxidative stress in the male reproductive system and their impact on the reproductive performance of domestic and wild animals. The most recent strategies for palliating the detrimental effects of oxidative stress on male fertility are reviewed together with their potential economic and ecological implications in the livestock industry and biodiversity conservation.
... For the first time in an ecophysiological study in a radioactively contaminated natural environment, we combined the measurement of a crucial physiological process (carotenoid distribution) with an accurate estimation of the radiological dose received by each individual. We uncovered three main results: (1) high within-site variability in levels of TDR, (2) TDR levels were better explained by internal dose rate than external dose rate, (3) and no significant effects of the exposure to ionizing radiation on frog body condition or tissue carotenoid concentration, which is not comparable to findings from previous studies 21,25,35,61,62 . ...
... First, the biological consequences of the Chernobyl accident have been extensively studied but research was largely absent during the first decade following the disaster 84 . It is thus difficult to compare our results obtained from samples collected only 16 months after the Fukushima nuclear disaster with prior studies on carotenoid distribution 34,35 or others physiological parameters 21,34,61,62,84,85 conducted long after the Chernobyl accident. Long-term chronic exposure to radionuclides can, for example, lead to an accumulation of mutations over time 86 or an increased population sensitivity 87 that may not be present after short-term exposure. ...
The nuclear accident in the Fukushima prefecture released a large amount of artificial radionuclides that might have short- and long-term biological effects on wildlife. Ionizing radiation can be a harmful source of reactive oxygen species, and previous studies have already shown reduced fitness effects in exposed animals in Chernobyl. Due to their potential health benefits, carotenoid pigments might be used by animals to limit detrimental effects of ionizing radiation exposure. Here, we examined concentrations of carotenoids in blood (i.e. a snapshot of levels in circulation), liver (endogenous carotenoid reserves), and the vocal sac skin (sexual signal) in relation to the total radiation dose rates absorbed by individual (TDR from 0.2 to 34 µGy/h) Japanese tree frogs (Hyla japonica). We found high within-site variability of TDRs, but no significant effects of the TDR on tissue carotenoid levels, suggesting that carotenoid distribution in amphibians might be less sensitive to ionizing radiation exposure than in other organisms or that the potential deleterious effects of radiation exposure might be less significant or more difficult to detect in Fukushima than in Chernobyl due to, among other things, differences in the abundance and mixture of each radionuclide.
... ainsi qu'une réduction du nombre de spermatozoïdes et de leur mobilité(Bonisoli-Alquati et al., 2011). L'équation de recherche a fourni 1 publication qui a été retenue pour cette analyse. ...
After an indication of the numerous interveners who participated to this expertise study, and a presentation of the context, objective and methodology of this expertise, this report, based on a very large bibliography, discusses the various aspects of the '5G' deployment and the associated public controversy: situation of the deployment in France and abroad, problems raised, actors involved in the controversy, media content, health framework, and posture of the academic community. It describes international institutional positions with respect to health effects of the '5G' (by international bodies, foreign national institutions, and in the USA, Australia and New-Zealand, and Europe). In the next part, exposure data related to the '5G' are reported and compared: normative and regulatory framework, technological evolutions regrading the 5G bandwidth, assessment of the exposure level in the lower bandwidths. By referring to various public or scientific publications from different countries, it proposes a rather detailed overview of health effects related to the studied exposure (comments about scientific knowledge and acknowledgement, the different biological effects on the human body). Some recommendations, notably regarding the deployment of '5G', are finally presented. A second document presents the opinion of the ANSES (the French Agency for health safety) about the content of this report.
... Consequently, changes in chronic radioactive exposure can cause stress and reduce resources allocated to these reproductive traits (Congdon et al., 2001). Changes in swimming behavior and morphology of sperm in wild birds have been reported (Møller et al., 2008;Bonisoli-Alquati et al., 2011;Hermosell et al., 2013), but whether or not this effect is evident in mammals, with potential for translation to humans, is currently unknown. ...
Sperm quantity and quality are key features explaining intra- and interspecific variation in male reproductive success. Spermatogenesis is sensitive to ionizing radiation and laboratory studies investigating acute effects of ionizing radiation have indeed found negative effects of radiation on sperm quantity and quality. In nature, levels of natural background radiation vary dramatically, and chronic effects of low-level background radiation exposure on spermatogenesis are poorly understood. The Chernobyl region offers a unique research opportunity for investigating effects of chronic low-level ionizing radiation on reproductive properties of wild organisms. We captured male bank voles (Myodes glareolus) from 24 locations in the Chernobyl exclusion zone in 2011 and 2015 and collected information on sperm morphology and kinetics. The dataset is limited in size and there overall was a relatively weak correlation between background radiation and sperm quality. Still, some correlations are worth discussing. First, mid-piece segments of spermatozoa tended to be smaller in bank vole males from areas with elevated background radiation levels. Second, we demonstrated a significant positive relationship between background radiation dose rates and the proportion of static spermatozoa among males within and among study locations after 10 as well as 60 min of incubation. Our results provide novel evidence of damaging effects of low dose ionizing radiation on sperm performance in wild rodent populations, and highlight that this topic requires further study across the natural gradients of background radiation that exist in nature.
... The effect of gamma irradiation and the abnormal forms of sperm were correlated to the disruption of spermatogenesis and sperm DNA. Also, mammalians sperm membrane has a lot of non-saturated fatty acids which make it sensitive to lipid peroxidation of oxidative stress (Bonisoli-Alquati et al., 2011). ...
... Diets enriched with ω-3 PUFAs have been associated with increased fertility (Blesbois et al. 1997, Feng et al. 2015 and larger semen volume (Surai et al. 2000) compared to ω-6 rich diets; although one study showed that an ω-3-rich diet led to a slight decrease in sperm motility yet an increase in fertility (Kelso et al. 1997), and other studies have found no difference in sperm motility (Cerolini et al. 2003, Khatibjoo et al. 2018. However, these are captive birds on strictly controlled diets, and to our knowledge there are no studies on the impact of the nutritional content of wild bird diets on sperm quality; though sperm motility and swimming speed are negatively associated with oxidative stress in the ejaculate in wild great tits (Helfenstein et al. 2010) and with circulating levels of oxidative stress in wild barn swallows Hirundo rustica (Bonisoli-Alquati et al. 2011). Since an unbalanced fatty acid composition in the diet can aggravate oxidative stress, we hypothesise that a diet rich in ω-6 PUFAs could be detrimental for sperm quality in wild birds. ...
Sperm morphology varies enormously across the animal kingdom. Whilst knowledge of the factors that drive the evolution of interspecific variation in sperm morphology is accumulating, we currently have little understanding of factors that may constrain evolutionary change in sperm traits. We investigated whether susceptibility to sperm abnormalities could represent such a constraint in songbirds, a group characterized by a distinctive helical sperm head shape. Specifically, using 36 songbird species and data from light and scanning electron microscopy, we examined among‐species correlations between the occurrence of sperm head abnormalities and sperm morphology, as well as the correlation between sperm head abnormalities and two indicators of sperm competition. We found that species with more helically shaped sperm heads (i.e., a wider helical membrane and more pronounced cell waveform) had a higher percentage of abnormal sperm heads than species with less helical sperm (i.e., relatively straight sperm) and that sperm head traits were better predictors of head abnormalities than total sperm length. In contrast, there was no correlation between sperm abnormalities and the level of sperm competition. Given that songbird species with more pronounced helical sperm have higher average sperm swimming speed, our results suggest an evolutionary trade‐off between sperm performance and the structural integrity of the sperm head. As such, susceptibility to morphological abnormalities may constrain the evolution of helical sperm morphology in songbirds.
... Diets enriched with ω-3 PUFAs have been associated with increased fertility (Blesbois et al. 1997, Feng et al. 2015 and larger semen volume (Surai et al. 2000) compared to ω-6 rich diets; although one study showed that an ω-3-rich diet led to a slight decrease in sperm motility yet an increase in fertility (Kelso et al. 1997), and other studies have found no difference in sperm motility (Cerolini et al. 2003, Khatibjoo et al. 2018. However, these are captive birds on strictly controlled diets, and to our knowledge there are no studies on the impact of the nutritional content of wild bird diets on sperm quality; though sperm motility and swimming speed are negatively associated with oxidative stress in the ejaculate in wild great tits (Helfenstein et al. 2010) and with circulating levels of oxidative stress in wild barn swallows Hirundo rustica (Bonisoli-Alquati et al. 2011). Since an unbalanced fatty acid composition in the diet can aggravate oxidative stress, we hypothesise that a diet rich in ω-6 PUFAs could be detrimental for sperm quality in wild birds. ...
In a rapidly changing world, it is important to understand how urban environments impact wildlife. For example, supplementary feeding of birds, though well‐intended, might have unexpected negative effects on the health of individual animals. Sunflower seeds are commonly provided in garden bird feeders, but they contain high levels of linoleic acid (LA), an omega‐6 polyunsaturated fatty acid (PUFA). Omega‐6 PUFAs are associated with increased oxidative stress, which can damage cell membranes, and in particular sperm cells. We assessed the level of LA in the blood of two seed‐eating finch species, greenfinches Chloris chloris and hawfinches Coccothraustes coccothraustes, caught in and in environments with direct access to sunflower seed feeders (Norway), and compared these with the level of LA in a smaller number of individuals sampled in in a rural area with low incidence of sunflower seed feeders (Czech Republic). Furthermore, we investigated the relationship between the proportion of LA in the blood (as well as the proportion of 10 other fatty acids) and sperm quality (the frequency of sperm head abnormalities and sperm swimming speed). We found that both finch species, but particularly greenfinches caught near feeders, exhibited levels of LA that were considerably higher than those previously reported for other wild birds. We also found that the proportion of LA was positively correlated with the frequency of abnormal sperm heads (sperm missing the acrosome), while there was no significant effect of fatty acid composition on sperm swimming speed. Our results indicate that the sperm quality of finches may be negatively affected by a high intake of sunflower seeds, adding to a growing body of research showing that supplementary feeding may have detrimental side effects for urban animals. This is particularly relevant for the greenfinch, which is currently affected by disease and population declines.
... Similar effects on sperm morphology of small rodents have recently been reported (Kivisaari et al. 2016). found that barn swallow sperm swimming ability was negatively related to radiation levels while Bonisoli-Alquati et al. (2011) found that plasma oxidative status could predict sperm performance, further supporting the role antioxidants are known to play in protecting spermatogenesis from the effects of ionizing radiation. Overall these studies provide convincing evidence that spermatogenesis can be significantly impacted by low-dose radiation and the resulting male infertility may in part explain the smaller population sizes of many species that have been documented for the region (see below). ...
Significant progress has been made in the past decade towards a better understanding of the genetic, developmental and ecological consequences of low-dose ionizing radiation (LDIR) on natural populations. Here, we review key studies of animals
living under natural conditions in regions affected by the Chernobyl and Fukushima nuclear accidents. Most studies show significant genetic damage related to radiation exposure, with consequent effects on reproduction, development, fertility, and population growth rates. Of particular note are the findings of eye cataracts, tumors, smaller brain size, and fewer or abnormal sperm with the frequency of occurrence generally following a dose-response-like relationship with ambient radiation levels. All animal groups surveyed in Chernobyl showed smaller population abundances in regions of high radiation, although not all species responded to the same degree and a few species even give the appearance of having adapted to some degree. In the more radioactive regions of Fukushima Prefecture, Japan, bird abundances have steadily dropped since the time of the accident, with declines following a linear dose response based on a novel dose reconstruction approach. Overall, the parallels observed between radiation effects on animals in Chernobyl and Fukushima provide additional evidence for the significant ecological consequences of nuclear accidents, and ionizing radiation in general.
... This might indicate that, when exposed to chronic LDIR, males invest more in protection of sperm in order to limit reduction in fertility and so in the ability to successfully reproduce. Interestingly, previous studies of sperm motility in barn swallows showed that the relationship with individual oxidative status depended on environmental radiation, suggesting individuals prioritize protection of sperm when exposed to LDIR, at the expense of their plasma oxidative status (Bonisoli Alquati et al., 2011). The effect for eggs was opposite to that for sperm. ...
... A large fraction of sperm cells has abnormal morphology and behavior, preventing them from fertilization. The frequency of such abnormal sperm is known to increase with the level of background radiation (Møller et al. 2005b), and such sperm cells have inferior swimming behavior, which may prevent fertilization (Møller et al. 2008;Bonisoli-Alquati et al. 2011). A similar production of abnormal germ cells occurs in pollen, which likewise have high frequencies of abnormalities that prevent fertilization. ...
Ionizing radiation that consists of α, β and γ rays can directly damage
DNA and other molecules and as such result in somatic or germline mutations. The
consequences of ionizing radiation for living beings cannot be measured with a
Geiger counter because it will depend on external dose, internal dose, and the extent
of DNA repair. In addition it will depend on the environmental conditions under
which living organisms exist. We list environmental indicators of ionizing condition
that reveal immediate and long-term consequences ranging from changes in
DNA, over damaged cells and organs to altered gene function and development,
reduced fecundity and survival, and hence to negative population trends, and
altered communities and ecosystems and perturbed ecosystem functioning. We
test for consistency in biological indicator ability across spatial and temporal scales
relying on long-term field data collected at Chernobyl and Fukushima, and we
test for consistency in indicator ability among indicators. Finally, we address the
direct and indirect effects of ionizing radiation and we discuss the species or taxa
most susceptible to the effects of radiation.
... While such heterogeneity in effects of radiation on abundance may be expected simply for sampling reasons, statistically significant heterogeneity beyond sampling suggests that these are inherent species-specific characteristics. Indeed, interspecific differences for birds in frequency of cataracts (Mousseau et al., 2013), reductions in brain size (Møller et al., 2013), frequency of tumors and abnormalities (Møller et al., 2013), aspermy and sperm behavior (Møller et al., 2008, 2014 ) and levels of antioxidants (Bonisoli-Alquati et al., 2011; Galván et al., 2014) suggest that underlying physiological processes account for such heterogeneity. Although soil invertebrates, arachnids and insects constitute significant parts of biodiversity, and although small invertebrates are readily sampled in standard pitfall traps, there are so far no pitfall trap studies conducted in Chernobyl or Fukushima. ...
... Sperm behavior is also negatively affected by radiation exposure history . found that sperm swimming ability was negatively related to radiation levels while Bonisoli-Alquati et al. (2011) found that plasma oxidative status could predict sperm performance, further supporting the role antioxidants are known to play in protecting spermatogenesis from the effects of ionizing radiation. Overall, these studies provide convincing evidence that spermatogenesis can be significantly impacted by lowdose radiation and the resulting male infertility may in part explain the smaller population sizes of many species that has been documented for the region (see below). ...
Recent advances in genetic and ecological studies of wild animal populations in Chernobyl and Fukushima have demonstrated significant genetic, physiological, developmental, and fitness effects stemming from exposure to radioactive contaminants. The few genetic studies that have been conducted in Chernobyl generally show elevated rates of genetic damage and mutation rates. All major taxonomic groups investigated (i.e., birds, bees, butterflies, grasshoppers, dragonflies, spiders, mammals) displayed reduced population sizes in highly radioactive parts of the Chernobyl Exclusion Zone. In Fukushima, population censuses of birds, butterflies, and cicadas suggested that abundances were negatively impacted by exposure to radioactive contaminants, while other groups (e.g., dragonflies, grasshoppers, bees, spiders) showed no significant declines, at least during the first summer following the disaster. Insufficient information exists for groups other than insects and birds to assess effects on life history at this time. The differences observed between Fukushima and Chernobyl may reflect the different times of exposure and the significance of multigenerational mutation accumulation in Chernobyl compared to Fukushima. There was considerable variation among taxa in their apparent sensitivity to radiation and this reflects in part life history, physiology, behavior, and evolutionary history. Interestingly, for birds, population declines in Chernobyl can be predicted by historical mitochondrial DNA base-pair substitution rates that may reflect intrinsic DNA repair ability.
... Several factors are known to induce premature acrosome reaction in birds and mammals, including mutations [19], extracellular calcium and lead [20,21], and oxidative stress [22]. Interestingly, a link between oxidative stress and poor sperm performance has already been indicated in barn swallows from Chernobyl [11,23], so rsbl.royalsocietypublishing.org Biol Lett 9: 20130530 we speculate that premature acrosome reaction is caused by oxidative stress and accelerated sperm senescence [24]. There was no seasonal trend in the proportion of abnormal sperm (see electronic supplementary material, methods). ...
Interspecific variation in sperm size is enigmatic, but generally assumed to reflect species-specific trade-offs in selection pressures. Among passerine birds, sperm length varies sevenfold, and sperm competition risk seems to drive the evolution of longer sperm. However, little is known about factors favouring short sperm or constraining the evolution of longer sperm. Here, we report a comparative analysis of sperm head abnormalities among 11 species of passerine bird in Chernobyl, presumably resulting from chronic irradiation following the 1986 accident. Frequencies of sperm abnormalities varied between 15.7 and 77.3% among species, more than fourfold higher than in uncontaminated areas. Nonetheless, species ranked similarly in sperm abnormalities in unpolluted areas as in Chernobyl, pointing to intrinsic factors underlying variation in sperm damage among species. Scanning electron microscopy of abnormal spermatozoa revealed patterns of acrosome damage consistent with premature acrosome reaction. Sperm length, but not sperm competition risk explained variation in sperm damage among species. This suggests that longer spermatozoa are more susceptible to premature acrosome reaction. Therefore, we hypothesize a trade-off between sperm length and sperm integrity affecting sperm evolution in passerine birds.
... At low dose rates recorded in the Chernobyl area, in the order of 400 nGyh −1 , radiation effects on sperm motility in birds have been reported. Some of the studies on birds showed that differences in habitat structure are also responsible for altered concentration of antioxidants, together with the direct effects of oxidative stress induced by radiation [39][40][41]. ...
Humans are constantly exposed to ionizing radiation deriving from outer space sources or activities related to medical care. Absorption of ionizing radiation doses over a prolonged period of time can result in oxidative damage and cellular dysfunction inducing several diseases, especially in ageing subjects. In this report, we analyze the effects of ionizing radiation, particularly at low doses, in relation to a variety of human pathologies, including cancer, and cardiovascular and retinal diseases. We discuss scientific data in support of protection strategies by safe antioxidant formulations that can provide preventive or potential therapeutic value in response to long-term diseases that may develop following exposure.
... Previous ecological studies in Chernobyl have demonstrated fitness and developmental consequences because of radiation exposure in a variety of vertebrate and invertebrate species. Barn swallows (Hirundo rustica) in the Chernobyl area have shown increased mutation rates (Ellegren et al., 1997;Møller et al., 2010), increased frequency of partial albinism (Ellegren et al., 1997;Møller & Mousseau, 2001), sperm abnormalities (Møller et al., 2005, Møller et al., 2008aBonisoli-Alquati et al., 2011), increased DNA damage and oxidative stress (Bonisoli-Alquati et al., 2010a,b), reduced levels of circulating and stored antioxidants (Møller et al., 2005), elevated levels of fluctuating asymmetry (FA) in tail length (Møller, 1993a,b) and smaller brains in relation to radiation exposure. A study on stag beetles (Lucanus cervus) in Chernobyl found that males in highly contaminated sites had significantly elevated levels of FA in secondary sexual characters compared to males from control sites, which affected mating status as a larger portion of asymmetric than symmetric males were unmated (Møller, 2002). ...
Mutagenic and epigenetic effects of environmental stressors and their transgenerational consequences are of interest to evolutionary biologists because they can amplify natural genetic variation. We studied the effect of parental exposure to radioactive contamination on offspring development in lesser marsh grasshopper Chorthippus albomarginatus. We used a geometric morphometric approach to measure fluctuating asymmetry (FA), wing shape and wing size. We measured time to sexual maturity to check whether parental exposure to radiation influenced offspring developmental trajectory and tested effects of radiation on hatching success and parental fecundity. Wings were larger in early maturing individuals born to parents from high radiation sites compared to early maturing individuals from low radiation sites. As time to sexual maturity increased, wing size decreased but more sharply in individuals from high radiation sites. Radiation exposure did not significantly affect FA or shape in wings nor did it significantly affect hatching success and fecundity. Overall, parental radiation exposure can adversely affect offspring development and fitness depending on developmental trajectories although the cause of this effect remains unclear. We suggest more direct measures of fitness and the inclusion of replication in future studies to help further our understanding of the relationship between developmental instability, fitness and environmental stress.
... Other low dose-rate studies have found no changes in antioxidant concentrations either in plants (6) or birds (7), though the latter did observe a significant difference in metabolites produced by reactive oxygen (ROM). Recently, Bonisoli-Alquati et al. (8) found that "oxidative damage of sperm was negatively related to sperm motility" in birds exposed to radiation at Chernobyl, but that "the highest values [of high sperm motility] were associated with relatively high radiation levels". ...
It has been hypothesized that radiation-induced oxidative stress is the mechanism for a wide range of negative impacts on biota living in radioactively contaminated areas around Chernobyl. The present study tests this hypothesis mechanistically, for the first time, by modelling the impacts of radiolysis products within the cell resulting from radiations (low linear energy transfer β and γ), and dose rates appropriate to current contamination types and densities in the Chernobyl exclusion zone and at Fukushima. At 417 µGy h(-1) (illustrative of the most contaminated areas at Chernobyl), generation of radiolysis products did not significantly impact cellular concentrations of reactive oxygen species, or cellular redox potential. This study does not support the hypothesis that direct oxidizing stress is a mechanism for damage to organisms exposed to chronic radiation at dose rates typical of contaminated environments.
There has been considerable work to test the role of organismal oxidative stress as a mediator of reproductive trade-offs. Intense research focussed on whether parental effort in offspring rearing results in oxidative stress. Many other studies carried out comparisons between non-reproducing and reproducing individuals in a narrow range of taxa. By contrast, we have a very limited number of studies that tested whether pre-breeding oxidative stress constraints reproductive decisions and quality of parental care (and reproductive success as a consequence). In this chapter, I have examined how the need to manage oxidative stress has possibly influenced the evolution of reproductive strategies, from courtship to parental care. I have also illustrated (1) the impact of oxidative stress on fertility, (2) differences between sexes in the regulation of oxidative status homeostasis, and (3) oxidative benefits and costs of cooperative breeding. Finally, I have highlighted a number of weaknesses in experimental designs that have been used to test the oxidative cost of reproduction hypothesis, calling for novel and more realistic studies.
Birds are bioindicators of anthropogenic environmental stress, including the changes caused by radioactive contamination of the ecosystems. The early stage of development is the most radiosensitive period. Therefore, it is necessary to assess embryo's exposure dose when interpreting observed radiobiological effects in birds. This is especially true for areas contaminated with Ca-like ⁹⁰ Sr. The levels of radionuclide accumulation in the eggshell can be extremely high, which leads to chronic embryo exposure. The objective of the study is to develop a method to calculate the dose to a herring gull embryo exposed to ⁹⁰ Sr distributed in egg compartments (shell, embryo body, white and yolk). To achieve the set objective, the time-dependent Sr distribution in the egg compartments was described. Alongside with that, dosimetric modeling was carried out to obtain dose factors that convert the radionuclide activity in different compartments of an egg to the embryo doses at various stages of embryogenesis. It has been shown that the accumulated dose to the herring gull embryo can be calculated based on the data on ⁹⁰ Sr total activity in the egg using the dose conversion factor equal to 0.44 µGy Bq − 1 . Since the eggshell contains more than 90% of total ⁹⁰ Sr activity, the conversion from eggshell activity to the dose to the embryo would be practically the same as that from the total egg activity – 0.46 µGy Bq − 1 . The main dose fraction (~ 99%) accumulates at the last stage of embryogenesis (from 13 to 26 days).
Environmental disasters offer the unique opportunity for landscape-scale ecological and evolutionary studies that are not possible in the laboratory or small experimental plots. The nuclear accident at Chernobyl (1986) allows for rigorous analyses of radiation effects on individuals and populations at an ecosystem scale. Here, the current state of knowledge related to populations within the Chernobyl region of Ukraine and Belarus following the largest civil nuclear accident in history is reviewed. There is now a significant literature that provides contrasting and occasionally conflicting views of the state of animals and how they are affected by this mutagenic stressor. Studies of genetic and physiological effects have largely suggested significant injuries to individuals inhabiting the more radioactive areas of the Chernobyl region. Most population censuses for most species suggest that abundances are reduced in the more radioactive areas.
Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 52 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
This study was conducted to investigate effects of X-irradiation on motility and viability of canine spermatozoids in chilled semen samples over the storage period of 5 days. Diluted semen samples from 10 different dogs were divided into 2 aliquots, and 1 group of aliquots was exposed to X-irradiation by transporting it through airport security X-ray machine (HI-SCAN 100100 T). Evaluation of total and progressive spermatozoids motility was done by Sperm Class Analyzer (SCA) (Spain, 2011). To detect spermatozoa with a biochemically active plasma membrane, a hypo-osmotic swelling test was used. Assessment of spermatozoa with a structurally intact plasma membrane was done using SYBR-14/PI (Molecular Probes) fluorescent staining. Our study showed that the total and progressive motility (P > 0.05) and the percentage of canine spermatozoa with a functional (P ≤ 0.05, P ≤ 0.01) and intact (P > 0.05) membrane over the storage period of 5 days were lower in the samples exposed to X-irradiation compared with the control group.
The cost of reproduction is a central paradigm of life history theory. It states that high investment in current reproduction reduces survival or future fecundity. Reproduction is a demanding phase of animals’ lives, since they must produce, and, in species with parental care, protect and provision, their young. In sexually reproducing species, considerable resources are also invested in mate choice strategies, which combine to shape the cost of reproduction. We currently know very little about how costs of reproduction are actually incurred, since the majority of studies have focussed on the ultimate outcomes rather than the proximate mechanisms. It has been suggested that oxidative stress may be one key cellular mechanism underlying the costs of reproduction. This chapter examines how the need to manage oxidative stress has possibly influenced the evolution of reproductive strategies, from the tactics adopted to find a suitable mate to how much effort parents put in offspring rearing. This chapter also discusses the possible prominent role of hormesis in determining the extent to which (1) reproductive activity may be stressful or not and (2) mild stress may stimulate reproductive performance.
We investigated the relationships between radiocesium activity in the soil and litter and radiocesium concentration in the web spiders collected at two forest sites in Kawamata-cho, Fukushima Prefecture. Changes in radiocesium contamination levels of the web spider over two years (2012-2013) were also monitored. At both sites, the aggregated transfer coefficient（Tag）of radiocesium from the soil into spiders in 2013 was approximately 0.005, and the radiocesium contamination level of spiders depended on the contamination level of the soil. Compared to the web spiders collected in 2012 (1.5 y after the accident), the concentration of 137Cs in spiders collected in 2013 (2.5 y after the accident) decreased by 40-50％, which was lower than that expected based on the physical attenuation of 137Cs. Although the mean level of 137Cs contamination in spiders decreased, highly 137Cs contaminated spiders were still collected in 2013, and this implies a need for a long-term monitoring of radiocesium contamination of the spider.
Studies of the responses of birds and other organisms to the nuclear accidents at Chernobyl and Fukushima. Jpn J Ornithol 64: 71–76. (2015)
We investigated the radioactive cesium concentrations in Barn Swallow Hirundo rustica nests that were collected from large areas of Japan in 2011 in order to understand the pattern of radioactive cesium contamination emitted by the Fukushima Daiichi Nuclear Power Plant accident. We collected 197 nests from 21 prefectures and measured radioactive cesium (Cs-134 and Cs-137) levels in 182 nests. Radioactive cesium contamination of nests was found in 13 prefectures. Cesium concentrations (Cs-134+Cs-137) in nests ranged from 33 to 90,000 Bq/kg in the Fukushima area, and the average concentration level in Fukushima was higher than in the other areas. There was a significantly positive relationship between radioactive cesium concentrations in nests and in the soil around the each nest site.
al. (2007) in the reference list. AU3 Citation "De Peyester (1993)" has been changed to "De Peyester et al. (1993)". Please check if okay. AU4 Citation "Duffell (1985)" has been changed to "Duffel (1995)". Please check. AU5 Citation "Sigsgaard (1992)" has been changed to "Sigsgaard et al. (1992)". Please check if appropriate. AU6 Citation "Hoekstra and Chapagain (2008)" has been changed to "Hoestra and Chapagain (2008)". Please check if appropriate. AU7 Please check the term "locell" for correctness. AU8 Citation "Vikberg et al. (2002)" has been changed to "Viberg et al. (2002)". Please check if okay. AU9 Please cite IARC (2000), Manzini et al. (1966), Minton and Murray (1988), 2002/61/EY, 2003/3/EY in text. AU10 Duplicate entry of James (1985) has been deleted. Please check if okay. AU11 Please check if inserted publisher location for Hoestra and Chapagain (2008) is okay. AU12 Please provide publisher details for IARC (1993, 2000). AU13 Please confirm the year for IARC (2004). AU14 Please provide article title for Rantanen (2008), Shafik (2007).
Ionizing radiation produces oxidative stress, but organisms can adapt to their exposure with physiological adaptive responses. However, the role of radioadaptive responses in wild populations remains poorly known.
At Chernobyl, studies of birds and other taxa including humans show that chronic exposure to radiation depletes antioxidants and increases oxidative damage. Here, we present analyses of levels of the most important intracellular antioxidant (i.e. glutathione, GSH ), its redox status, DNA damage and body condition in 16 species of birds exposed to radiation at Chernobyl. We use an approach that allows considering the individual bird as the sampling unit while controlling for phylogenetic effects, thus increasing the statistical power by avoiding the use of species means as done for most previous comparative studies.
As a consequence, we found a pattern radically different from previous studies in wild populations, showing that GSH levels and body condition increased, and oxidative stress and DNA damage decreased, with increasing background radiation. Thus, when several species are considered, the overall pattern indicates that birds are not negatively affected by chronic exposure to radiation and may even obtain beneficial hormetic effects following an adaptive response. Analysis of the phylogenetic signal supports the existence of adaptation in the studied traits, particularly in GSH levels and DNA damage.
We also show that, under equal levels of radiation, the birds that produce larger amounts of the pigment pheomelanin and lower amounts of eumelanin pay a cost in terms of decreased GSH levels, increased oxidative stress and DNA damage, and poorer body condition. Radiation, however, diminished another potential cost of pheomelanin, namely its tendency to produce free radicals when exposed to radiation, because it induced a change towards the production of less pro‐oxidant forms of pheomelanin with higher benzothiazole‐to‐benzothiazine ratios, which may have facilitated the acclimation of birds to radiation exposure.
Our findings represent the first evidence of adaptation to ionizing radiation in wild animals, and confirm that pheomelanin synthesis represents an evolutionary constraint under stressful environmental conditions because it requires GSH consumption.
The Chernobyl accident of 1986 released vast quantities of radioactive materials and significantly contaminated about 200,000 square kilometers of land. The Chernobyl Forum Report, an initiative of the International Atomic Energy Agency, suggested that the effects of radiation on wildlife were negligible relative to the impacts of human habitation, but this position was based on the very limited data available prior to this 2006 report. The wildlife of this region has been the subject of extensive study since 2005; since then, research has found that many birds, insects, spiders, and mammals show significant declines as a probable consequence of exposure to radionuclides. The best-studied group, birds, shows a 50 percent decrease in species richness and a 66 percent drop in abundance in the most contaminated areas compared to areas with normal background radiation in the same neighborhood. In addition, mutation rates and developmental abnormalities are dramatically higher, and survival rates and fertility are lower, in regions of moderate to high contamination. These findings challenge reports in the popular media and the conclusions of the Chernobyl Forum Report and are of relevance today, given recent interest in returning contaminated lands to agriculture use and the renaissance of the global nuclear power industry.
Oxidative stress (OS) is widely believed to be responsible for generation of trade-offs in evolutionary ecology by means of constraining investment into a number of components of fitness. Yet the progress in understanding the true role of OS in ecology and evolution has remained elusive. Interpretation of current findings is particularly hampered by the scarcity of experiments demonstrating which of the many available parameters of oxidative status respond most sensitively to and are relevant for measuring OS. We addressed these questions in wild-caught captive greenfinches (Carduelis chloris) by experimental induction of OS by administration of the pro-oxidant compound paraquat with drinking water. Treatment induced 50% of mortality and a significant drop in body mass and an increase in oxidative DNA damage and glutathione levels in erythrocytes among the survivors of the high paraquat (0.2 g/L during 7 days) group. Three days after the end of the treatment, paraquat had no effect on peroxidation of lipids (plasma malondialdehyde), carbonylation of proteins (in erythrocytes), parameters of plasma antioxidant protection (TAC and OXY), uric acid or carotenoids. Our findings of an increase in one marker of damage and one marker of protection from the multitude of measured variables indicate that detection of OS is difficult even under most stringent experimental induction of oxidative insult. We hope that this study highlights the need for reconsideration of over-simplistic models of OS and draws attention to the limitations of detection of OS due to time-lagged and hormetic up-regulation of protective mechanisms. This study also underpins the diagnostic value of measurement of oxidative damage to DNA bases and assessment of erythrocyte glutathione levels.
Ion radiation or radiotherapy is used to treat male patients with oligozoospermia, azoospermia, temporarily infertility, or even permanent infertility. The present study aims to investigate the potential infertility mechanism of sperm in mice after carbon ion radiation (CIR). The caudal epididymal sperm of male mice whole-body irradiated with carbon ion beam (0.5Gy and 4Gy) were used 7 days after irradiation. A two-dimensional gel electrophoresis approach was employed to investigate the changes in protein expression in the caudal edididymal sperm. Spot detection and matching were performed using the PDQuest 8.0 software. The criteria used to select spots for the analysis were more than a threefold difference in protein quantities (normalized spot volume), which allowed the detection of six differentially expressed proteins. Protein identification was performed using MALDI-TOF-TOF. Six specific proteins were identified by searching the NCBI protein sequence database. Among these proteins, HSP 70-2, PLC, GPX4, β-tubulin, and GAPDHS were associated with sperm motility, which can affect fertility. β-tubulin is important in axoneme migration flagellar movement and regulation, and GAPDHS is related to sperm energy supply. We analyzed their expressions using immunoblotting and immunofluorescence. The changes in sperm protein expression after CIR are mainly associated with motility. These proteins are potential markers for the mechanisms of infertility in space or radiotherapy.
The Azores bullfinch is endemic to the island of São Miguel in the Azores archipelago and the sister species to the Eurasian bullfinch. Here we show that the spermatozoa of the two species have similar ultrastructure and gross morphology. Thus, the unusual and supposedly neotenous sperm morphology previously described for the Eurasian bullfinch appears to be an ancestral trait that evolved before the two taxa diverged. In addition, the coefficients of variation in total sperm length, both within and among males, were high in both species and exceed any previously published values for free-living passerines. Such high sperm-size variation is typically found in species with relaxed sperm competition. However, the high variance in mean sperm length among Azores bullfinches is surprising, because the trait has high heritability and this small, insular population shows clear signs of reduced genetic diversity at neutral loci. A possible explanation for this apparent contradiction is that the Azores bullfinch has retained more diversity at functional and fitness-related loci than at more neutral parts of the genome. Finally, we also present data on relative testis size and sperm swimming speed for the Eurasian bullfinch, and discuss the hypothesis that the small and putatively neotenous sperm in bullfinches has evolved in response to lack of sperm competition.
Microwave radiation resulted in degeneration, apoptosis or necrosis in germ cells at different stages. The molecular mechanisms by which microwaves induce spermatogenesis disorder have not been completely understood. Sertoli cells play crucial roles in mammalian spermatogenesis. Cytokines produced by Sertoli cells play pleiotropic roles in different conditions. At physiologically low concentration, TNFα, IL-1β and IL-6 behave as survival factors; while under pathological condition, these cytokines can induce apoptosis in testis. The effects of cytokines produced by microwave-radiated Sertoli cells on spermatogenesis are poorly understood. The purpose of this study was to determine the effect of cytokines produced by microwave-radiated Sertoli cells on the germ cells. We focused the effect of TNFα, IL-1β and IL-6 on the germ cells. The results showed that TNFα, IL-1β and IL-6 were increased in Sertoli cells after exposure to microwave radiation. These up-regulated cytokines can induce apoptosis and lipid peroxidation in the membrane of germ cells. In addition, germ cell apoptosis was associated with the up-regulation of Bax/Bcl-2 and caspase-3. These results suggest that cytokines produced by microwave-radiated Sertoli cells may disrupt spermatogenesis. Our data provided novel insight into the injury mechanism of germ cells induced by microwave radiation.
Recent studies have demonstrated that human spermatozoa are capable of generating reactive oxygen species and that this activity is significantly accelerated in cases of defective sperm function. In view of the pivotal role played by lipid peroxidation in mediating free radical damage to cells, we have examined the relationships between reactive oxygen species production, lipid peroxidation, and the functional competence of human spermatozoa. Using malondialdehyde production in the presence of ferrous ion promoter as an index of lipid peroxidation, we have shown that lipid peroxidation is significantly accelerated in populations of defective spermatozoa exhibiting high levels of reactive oxygen species production or in normal cells stimulated to produce oxygen radicals by the ionophore, A23187. The functional consequences of lipid peroxidation included a dose-dependent reduction in the ability of human spermatozoa to exhibit sperm oocyte-fusion, which could be reversed by the inclusion of a chain-breaking antioxidant, alpha-tocopherol. Low levels of lipid peroxidation also had a slight enhancing effect on the generation of reactive oxygen species in response to ionophore, without influencing the steady-state activity. At higher levels of lipid peroxidation, both the basal level of reactive oxygen species production and the response to A23187 were significantly diminished. In contrast, lipid peroxidation had a highly significant, enhancing effect on the ability of human spermatozoa to bind to both homologous and heterologous zonae pellucidae via mechanisms that could again be reversed by alpha-tocopherol. These results are consistent with a causative role for lipid peroxidation in the etiology of defective sperm function and also suggest a possible physiological role for the reactive oxygen species generated by human spermatozoa in mediating sperm-zona interaction.
The atlas contains maps of the deposition on Europe of caesium-137 which was released in the
Chernobyl accident in 1986. Maps are provided on three scales: European, national/regional and
local. Perspective is also provided on the current radiological significance of these deposits.
Avian spermatozoa are characterised by high concentrations of polyunsaturated fatty acids (PUFAs), in particular docosatetraenoic (DTA, 22:4n-6) and arachidonic (AA, 20:4n-6) acids. As a result they are vulnerable to lipid peroxidation, which i considered to be an important factor of male infertility. Antioxidant systems are expressed in spermatozoa and seminal plasma and build three major levels of antioxidant defense. The first level is based on the activity of superoxide dismutase (SOD) which is, in conjunction with glutathione peroxidase (GSH-Px), catalase and metal-binding proteins, responsible for prevention of free radical formation. The second level of defence is responsible for prevention and restriction of chain reaction propagation and includes chain-breaking antioxidants such as vitamin E, ascorbic acid, glutathione and some others. The third level of antioxidant defence deals with damaged molecules, repairing or removing them from the cell and includes specific enzymes such as lipases, proteases, DNA repair enzymes etc In the review, profiles of PUFAs and the two first lines of antioxidant defence in avian spermatozoa are characterised. Dietary manipulation of the breeder's diet (PUFA, vitamin E and selenium) as an effective means of modulating fatty acid composition and antioxidant system is also considered. Antioxidant properties of seminal plasma and efficiencies of inclusion of antioxidants into semer diluents are also characterised.
Los caracteres sexuales secundarios de los machos pueden brindar a las hembras información sobre la capacidad de fertilización del esperma de un macho. En algunos peces y aves, la coloración nupcial intensa se correlaciona con la capacidad de fertilización del macho, pero no se ha establecido un mecanismo que vincule la coloración con la calidad del esperma. Un mecanismo posible es que los pigmentos carotenoides, que colorean la piel y las plumas en muchos animales, estén presentes en el fluido seminal y sirvan como antioxidantes protectores del esperma. Empleamos cromatografía líquida de alto rendimiento para analizar muestras de esperma provenientes de cuatro especies de Malurus y detectamos bajas concentraciones (<1 μg ml−1) de carotenoides en algunas muestras. Los carotenoides xantófilos (incluyendo luteína y zeaxantina), que son típicamente de origen dietario, estuvieron presentes en el fluido seminal de M. cyaneus y M. splendens. En contraste, los quetocaroteniodes rojos (incluyendo astaxantina y cantaxantina), que son probablemente derivados metabólicos de precursores dietarios, estuvieron presentes en el fluido seminal de M. melanocephalus. Este trabajo es el primero en describir la presencia de carotenoides en el fluido seminal de aves y sugiere que, aunque los carotenoides estén en bajos niveles y por ende puedan tener actividad antioxidante limitada, puede haber variabilidad biológica en los carotenoides del semen de las aves sobre la cual podría actuar la selección.
Male secondary sexual characters can provide females with information regarding the fertilizing capacity of a male's sperm. In some fishes and birds, intense nuptial coloration is correlated with male fertilizing capacity, but no mechanistic link between coloration and sperm quality has been established. One plausible mech-anism is that carotenoid pigments, which color skin and feathers in many animals, are present in seminal fluid and serve as antioxidant protectors of sperm. We used high-performance liquid chromatography (HPLC) to analyze sperm samples from four species of Australian fairy-wren (Malurus) and detected low concentrations (<1 µg ml -1) of carotenoids in some samples. Xanthophyll carotenoids (including lutein and zeaxanthin), which are typically di-etary in origin, were present in the seminal fluid of Superb (M. cyaneus) and Splendid (M. splendens) Fairy-Wrens. In contrast, red ketocarotenoids (including astaxanthin and canthaxanthin), which are likely metabolically derived from dietary precursors, were present in the seminal fluid of Red-backed Fairy-Wrens (M. melanocephalus). This work is the first to report carotenoids in avian seminal fluid and suggests that, although carotenoids are at low levels and thus may have limited antioxidant activity, there may be biological variability in avian semen carotenoids on which selection could act. Carotenoides en el Fluido Seminal de Aves Silvestres: Variación Inter Específica en Malurus Resumen. Los caracteres sexuales secundarios de los machos pueden brindar a las hembras información so-bre la capacidad de fertilización del esperma de un macho. En algunos peces y aves, la coloración nupcial intensa se correlaciona con la capacidad de fertilización del macho, pero no se ha establecido un mecanismo que vincule la coloración con la calidad del esperma. Un mecanismo posible es que los pigmentos carotenoides, que colorean la piel y las plumas en muchos animales, estén presentes en el fluido seminal y sirvan como antioxidantes protectores del esperma. Empleamos cromatografía líquida de alto rendimiento para analizar muestras de esperma proveni-entes de cuatro especies de Malurus y detectamos bajas concentraciones (<1 µg ml -1) de carotenoides en algunas muestras. Los carotenoides xantófilos (incluyendo luteína y zeaxantina), que son típicamente de origen dietario, estuvieron presentes en el fluido seminal de M. cyaneus y M. splendens. En contraste, los quetocaroteniodes rojos (incluyendo astaxantina y cantaxantina), que son probablemente derivados metabólicos de precursores dietarios, estuvieron presentes en el fluido seminal de M. melanocephalus. Este trabajo es el primero en describir la presen-cia de carotenoides en el fluido seminal de aves y sugiere que, aunque los carotenoides estén en bajos niveles y por ende puedan tener actividad antioxidante limitada, puede haber variabilidad biológica en los carotenoides del se-men de las aves sobre la cual podría actuar la selección.
Summary
1. We investigated the relationship between radiation arising from the fall-out due to
the explosion of the nuclear reactor at Chernobyl, Ukraine, and body condition, rate of
reproduction and survival in a migratory passerine bird, the barn swallow
Hirundo rustica L., by comparing a contaminated region and a control region (Kanev) during 6 years between 1991 and 2004.
2. The fraction of nonreproducing adults was on average 23% in Chernobyl compared
with close to zero in Kanev and other European populations.
3. Body condition as estimated from body mass was similar in Chernobyl and Kanev.
Although laying date did not differ significantly between the two regions, clutch was
reduced by 7%, brood size by 14% and hatching success by 5% in the Chernobyl region
relative to the control area.
4. Annual adult survival, estimated from mark–recapture analyses, was on average 28%
in the Chernobyl region, but 40% in Kanev.
5. The relationships were generally confirmed in rank correlation analyses between
response variables and ambient radiation levels in different colonies.
6. The overall findings are consistent with the hypothesis that radioactive contamination
in the Chernobyl region has significant negative impact on rates of reproduction
and survival of the barn swallow. We hypothesize that these effects are mediated by antioxidants and/or mutations.
Key-words: antioxidants, body condition, clutch size, hatching success, Hirundo rustica, nonbreeding, population change, survival.
Comparative analyses have found that relative testis size is a strong predictor of the prevalence of sperm competition for many taxa, including mammals, yet underlying this pattern is the assumption that intraspecific variation in testis size is related to individual fitness. Because intraspecific variation in ejaculate investment underlies interspecific patterns, it is critical to understand the causes and consequences of intraspecific variation in ejaculate investment. We examined relationships between ejaculate investment (testis size and sperm length) and reproductive success, body size and condition in the yellow-pine chipmunk (Tamias amoenus), a small ground squirrel in which sperm competition occurs. We examined genetic estimates of male reproductive success from a wild population of yellow-pine chipmunks and determined that males with large testes had higher annual reproductive success than males with small testes. This result provides empirical support for the numerous comparative studies that indicate testis size is associated with the intensity of sperm competition. In addition, males in good condition had relatively larger testes than males in poor condition, but there was no evidence of sperm length being dependent on condition. Finally, contrary to many predictions, males that invested more in sperm production (relatively heavy testes) produced shorter sperm, not longer sperm, than males that invested less.
Sperm competition is expected to favour the evolution of traits that influence the performance of sperm when they compete to fertilize a female's eggs. While there is considerable evidence that selection favours increases in sperm numbers, much less is known about how sperm quality contributes towards competitive fertilization success. Here, we determine whether variation in sperm quality influences competitive fertilization success in the green swordtail Xiphophorus helleri, a highly promiscuous livebearing fish. We use artificial insemination as a method of controlled sperm delivery and show that sperm swimming velocity is the primary determinant of fertilization success when ejaculates from two males compete to fertilize a female's eggs. By contrast, we found no evidence that sperm length had any effect on siring success. We also found no evidence that pre- and postcopulatory sexual traits were phenotypically integrated in this species, suggesting that the previous observation that reproductive skew favours males with high mating rates is unlikely to be due to any direct association between sperm quality and male sexual ornamentation.
Ecology Letters (2010) 13: 213–222
Sperm cells are highly vulnerable to free radicals, and sperm quality and male fertility are critically affected by oxidative stress. Recently, sexual ornaments, particularly carotenoid-based colourful traits, have been proposed to depend on a male’s capacity to resist oxidative stress, and thus to signal sperm quality. We conducted an experimental test of this hypothesis on great tits Parus major, in which adults are sexually dichromatic in carotenoid-based breast plumage. We report the first evidence that ornaments and sperm quality may be linked through oxidative stress. When experimentally subjected to oxidative stress resulting from increased workload, less colourful males suffered a greater reduction in sperm motility and swimming ability, and increased levels of sperm lipid peroxidation compared to more colourful males. Moreover, the level of sperm lipid peroxidation was negatively correlated with sperm quality. Finally, carotenoid supplementation increased sperm quality of less colourful males, suggesting that pale males are deficient in carotenoid antioxidants.
The functional signi¢cance of elongated, narrow tips of the tail feathers of certain birds, so-called tail streamers, has recently been discussed from an aerodynamic point of view, and the e¡ects of sexual selection on such traits have been questioned. We review our long-term ¢eld studies using observational and experimental approaches to investigate natural and sexual selection in the barn swallow, Hirundo rustica, which has sexually size-dimorphic outermost tail feathers. Experimental manipulation of the length of the outermost tail feathers has demonstrated sexual selection advantages of tail elongation and disadvantages of tail shortening, with opposite e¡ects for natural selection in terms of foraging e¤ciency, haematocrit and survival. These ¢ndings are contrary to the prediction of a general deterioration from both shortening and elongation, if the tail trait was determined solely by its e¡ects on aerodynamic e¤ciency and £ight manoeuvrability. Patterns of sexual selection in manipulated birds conform with patterns in unmanipulated birds, and selection di¡erentials for di¡erent components of sexual selection in manipulated birds are strongly positively correlated with di¡erentials in unmanipulated birds. Age and sex di¡erences in tail length, and geographical patterns of sexual size dimorphism, are also consistent with sexual selection theory, but inconsistent with a purely natural selection advantage of long outermost tail feathers in male barn swallows. A.P.M. was supported by the Danish Natural Sciences Research Council, S.M. by a postdoctoral grant fromthe Spanish Ministry of Education, A.B. by a Marie Curie postdoctoral grant of the European Communities, and F.deL. by Spanish DGICYT (PB 95020). Peer reviewed
In species where males express carotenoid-based sexual signals, more intensely coloured males may be signalling their enhanced ability to combat oxidative stress. This may include mitigating deleterious oxidative damage to their sperm, and so be directly related to their functional fertility. Using a split-clutch in vitro fertilization technique and dietary carotenoid manipulation, we demonstrate that in non-competitive fertilization assays, male three-spined sticklebacks (Gasterosteus aculeatus) that are fed higher (but biologically relevant) levels of carotenoids had a significantly increased fertilization success, irrespective of maternal carotenoid intake. Furthermore, within diet groups, a male's fertilization success was positively related to the expression of his carotenoid-based nuptial coloration, with more intensely coloured males having higher functional fertility. These data provide, to our knowledge, the first demonstration that dietary access to carotenoids influences fertilization success, and suggest that females could use a male's nuptial coloration as an indicator of his functional fertility.
Evolutionary theory is firmly grounded on the existence of trade-offs between life-history traits, and recent interest has centred on the physiological mechanisms underlying such trade-offs. Several branches of evolutionary biology, particularly those focusing on ageing, immunological and sexual selection theory, have implicated reactive oxygen species (ROS) as profound evolutionary players. ROS are a highly reactive group of oxygen-containing molecules, generated as common by-products of vital oxidative enzyme complexes. Both animals and plants appear to intentionally harness ROS for use as molecular messengers to fulfil a wide range of essential biological processes. However, at high levels, ROS are known to exert very damaging effects through oxidative stress. For these reasons, ROS have been suggested to be important mediators of the cost of reproduction, and of trade-offs between metabolic rate and lifespan, and between immunity, sexual ornamentation and sperm quality. In this review, we integrate the above suggestions into one life-history framework, and review the evidence in support of the contention that ROS production will constitute a primary and universal constraint in life-history evolution.
Recent studies have demonstrated that human spermatozoa are capable of generating reactive oxygen species and that this activity is significantly accelerated in cases of defective sperm function. In view of the pivotal role played by lipid peroxidation in mediating free radical damage to cells, we have examined the relationships between reactive oxygen species production, lipid peroxidation, and the functional competence of human spermatozoa. Using malondialdehyde production in the presence of ferrous ion promoter as an index of lipid peroxidation, we have shown that lipid peroxidation is significantly accelerated in populations of defective spermatozoa exhibiting high levels of reactive oxygen species production or in normal cells stimulated to produce oxygen radicals by the ionophore, A23187. The functional consequences of lipid peroxidation included a dose-dependent reduction in the ability of human spermatozoa to exhibit sperm oocyte-fusion, which could be reversed by the inclusion of a chain-breaking antioxidant, alpha-tocopherol. Low levels of lipid peroxidation also had a slight enhancing effect on the generation of reactive oxygen species in response to ionophore, without influencing the steady-state activity. At higher levels of lipid peroxidation, both the basal level of reactive oxygen species production and the response to A23187 were significantly diminished. In contrast, lipid peroxidation had a highly significant, enhancing effect on the ability of human spermatozoa to bind to both homologous and heterologous zonae pellucidae via mechanisms that could again be reversed by alpha-tocopherol. These results are consistent with a causative role for lipid peroxidation in the etiology of defective sperm function and also suggest a possible physiological role for the reactive oxygen species generated by human spermatozoa in mediating sperm-zona interaction.
To analyze the prognostic value of the sperm cervical mucus penetration test (SCMPT), fresh semen samples of 99 male patients under infertility investigation were exposed to capillary tubes filled with freshly obtained cervical mucus (CM) of the patients' wives (WCM), fertile donors (DCM), and bovine CM (BCM). The quality of the human CM was standardized by oral administration of estrogens. The overall pregnancy rate after 6 months was 17.2% (17/99), and was significantly different in couples with poor and good SCMPT with WCM (1/44, 2.3% versus 16/55, 29%; P less than 0.001) in a prospective study. Human CM was superior to BCM as a penetration medium in providing more information about sperm function. The results suggest that in vitro sperm penetration testing with hormonally standardized CM of female partners adds an important dimension to sperm analysis with regard to fertility prognosis.
Paraquat (1,1'-dimethyl-4,4'-bipyridinium dichloride) was used as an intracellular generator of oxygen free radicals and was found to be highly mutagenic for Salmonella typhimurium. It caused both base-pair substitution and frameshift mutations. Paraquat was much more toxic and mutagenic in a simple nutritionally restricted medium than in a rich complex medium. The mutagenicity of paraquat was dependent upon the presence of a supply of both electrons and oxygen. Cells containing high levels of superoxide dismutase (superoxide:superoxide oxidoreductase, EC 1.15.1.1) were more resistant to the toxicity and the mutagenicity of paraquat than were cells containing normal levels of this enzyme. The mutagenicity of paraquat thus appears to be due to its ability to exacerbate the intracellular production of superoxide radicals.
Tools for performing model selection and model averaging. Automated model selection through subsetting the maximum model, with optional constraints for model inclusion. Model parameter and prediction averaging based on model weights derived from information criteria (AICc and alike) or custom model weighting schemes.
[Please do not request the full text - it is an R package. The up-to-date manual is available from CRAN].
Objective To determine the incidence of reactive oxygen species formation in semen of a population of patients consulting for infertility. Design The incidence of reactive oxygen species formation in whole semen and in washed spermatozoa was studied. The values obtained were correlated with semen parameters. The effect of the type of sperm washing on reactive oxygen species formation was also investigated. Setting Semen samples from patients consulting for infertility and control subjects were obtained by masturbation after 3 days of sexual abstinence. Reactive oxygen species formation was measured in whole semen, sperm suspension washed by Percoll gradients, or repeated centrifugations. Sperm motility parameters were measured by computer-aided sperm analysis. Patients, Participants Fertile control men and an unselected population of patients consulting for infertility. Interventions None. Main Outcome Measure Reactive oxygen species formation by fresh semen specimen or washed spermatozoa was measured in a computer-driven LKB 1251 Luminometer (LKB-Wallac, Turku, Finland). Results Reactive oxygen species formation was detected in 40% of the semen with spermatozoa from infertile patients, whereas none was found in 6 azoospermic men and 10 control men. The level of reactive oxygen species formation was inversely correlated to the semen volume, the percentage of motile spermatozoa, and sperm linearity both in semen and in Percoll-washed spermatozoa. Washing by repeated centrifugation-resuspension increased 20- to 50-fold sperm reactive oxygen species formation. This enhancement was caused by the centrifugation itself and by the removal of seminal plasma. Both morphologically normal and abnormal spermatozoa produced reactive oxygen species. Conclusion The data suggest that reactive oxygen species formation by spermatozoa may be a significant cause for male infertility.
To analyze the prognostic value of the sperm cervical mucus penetration test (SC-MPT), fresh semen samples of 99 male patients under infertility investigation were exposed to capillary tubes filled with freshly obtained cervical mucus (CM) of the patients' wives (WCM), fertile donors (DCM), and bovine CM (BCM). The quality of the human CM was standardized by oral administration of estrogens. The overall pregnancy rate after 6 months was 17.2% (17/99), and was significantly different in couples with poor and good SCMPT with WCM (1/44, 2.3% versus 16/55, 29%; P
This chapter gives results from some illustrative exploration of the performance of information-theoretic criteria for model selection and methods to quantify precision when there is model selection uncertainty. The methods given in Chapter 4 are illustrated and additional insights are provided based on simulation and real data. Section 5.2 utilizes a chain binomial survival model for some Monte Carlo evaluation of unconditional sampling variance estimation, confidence intervals, and model averaging. For this simulation the generating process is known and can be of relatively high dimension. The generating model and the models used for data analysis in this chain binomial simulation are easy to understand and have no nuisance parameters. We give some comparisons of AIC versus BIC selection and use achieved confidence interval coverage as an integrating metric to judge the success of various approaches to inference.
Models of sexual selection and monogamy the study organism male mating advantages benefits of mate choice determinants of tail ornament size advantages of early arrival options for unmated males parasites and sexual selection parental care and male ornamentation sperm competition and sexual selection sexual size dimorphism and female ornaments geographic variation in ornament size synthesis.
1. Oxygen is a toxic gas - an introductionto oxygen toxicity and reactive species 2. The chemistry of free radicals and related 'reactive species' 3. Antioxidant defences Endogenous and Diet Derived 4. Cellular responses to oxidative stress: adaptation, damage, repair, senescence and death 5. Measurement of reactive species 6. Reactive species can pose special problems needing special solutions. Some examples. 7. Reactive species can be useful some more examples 8. Reactive species can be poisonous: their role in toxicology 9. Reactive species and disease: fact, fiction or filibuster? 10. Ageing, nutrition, disease, and therapy: A role for antioxidants?
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Treatment of mice with high doses of radiation or certain cytotoxic drugs results in killing of spermatogonial stem cells, a prolonged period of reduced sperm production, and infertility. In this study, quantitative relationships between these parameters are shown to exist after radiation, Adriamycin (Adria Laboratories, Wilmington, Delaware) or thiotepa treatment. The same relationships are valid for the different cytotoxic agents tested.
The survival of spermatogonial stem cells was assessed by counts of repopulating tubule cross sections at five or eight weeks after treatment. Testicular sperm head counts, eight weeks after treatment, were also used as an assay of stem cell survival. These two assays are highly correlated, demonstrating that the sperm head count at eight weeks is directly related to stem cell survival.
Sperm production declines after cytotoxictreatment and partially recovers to a plateau level. The level of this recovery is correlated with stem cell survival. The restoration of fertility is related to the recovery of sperm production. Under the conditions employed, fertility returns when sperm production by the testis reaches about 10% of control levels. The duration of the sterile period is also highly correlated with stem cell survival.
These results strongly suggest that short‐term assays that measure survival of stem cells can be used to predict the duration and extent of sterility, regardless of the cytotoxic agent used.
The severe nuclear accident at Chernobyl in 1986 resulted in the worst reported accidental exposure of radioactive material to free-living organisms
1. In recent years, evolutionary ecologists have become increasingly interested in antioxidants and oxidative stress. Information on redox systems can provide new insights into our understanding of life-history variation and animal responses to environmental stressors.
2. A common approach of ecological studies to the study of antioxidant capacity of animals has been measurement of the total antioxidant capacity of serum or plasma. Some of these studies have suggested that most of the antioxidant capacity measured in plasma is made up of uric acid and, therefore, estimates of antioxidant capacity should be corrected for the concentration of uric acid.
3. Here, I show that (i) the correlation between plasma concentration of uric acid and plasma antioxidant capacity is method dependent and (ii) different assays for the quantification of circulating antioxidant capacity can provide information on different components of the antioxidant machinery.
4. To determine whether measurements of antioxidant capacity need to be corrected for the uric acid concentration in the sample, it is therefore important to take into account the biochemical properties of the assay used.
Radiation can reduce antioxidant levels dramatically because of the use of antioxidants to eliminate free radicals produced in the presence of radiation. Antioxidants are crucial biochemicals for elimination of free radicals, which can cause permanent damage to DNA and other molecules. If antioxidants are a limiting resource, we would expect individuals of species with a high expenditure of antioxidants to suffer the most from radiation. We tested this hypothesis by investigating interspecific variation in the relationship between abundance and level of radiation in breeding birds inhabiting forests around Chernobyl, Ukraine. We used bird point counts to estimate abundance of 57 species of birds at 254 locations where background radiation levels were quantified.
Migratory birds use large amounts of antioxidants during their annual migrations to neutralize free radicals, and migrants have depleted antioxidant levels upon arrival at their breeding grounds. Consistently, abundance decreased with increasing levels of radiation in species that migrated the longest distances.
Bird species with long dispersal distances may experience deficiencies in antioxidant levels because of physical activity but also because of exposure to novel antigens, implying that species with long dispersal distances should suffer the most from exposure to radiation. Indeed, the slope of the relationship between abundance and radiation decreased with increasing dispersal distance.
Female birds deposit large amounts of antioxidants in their eggs, with the total amount deposited often exceeding the total amount in a female's. Accordingly, the decrease in abundance with radiation level increased with relative egg size in different species.
Many bird species have plumage that is coloured by carotenoids, which cannot be recovered once deposited in feathers. Therefore, bird species with carotenoid‐based plumage should show stronger declines with increasing levels of radiation than species with melanin‐based or structural coloration. In accordance with this prediction, the decline in abundance with radiation was the strongest in species of birds with carotenoid‐based plumage.
Synthesis and applications . These findings highlight the importance of antioxidants for understanding the ecological consequences of radiation on the abundance of free‐living animals, showing that species using large amounts of antioxidants will be particularly susceptible to the effects of low‐level radiation.
Abstract Secondary sexual characters have been hypothesized to be particularly susceptible to the deleterious effects of mutation because the expression of such characters is usually influenced by many more metabolic pathways than are ordinary morphological characters. We tested this hypothesis using the elevated mutation rates in the barn swallow (Hirundo rustica) of the Chernobyl region of Ukraine as a model system. A great deal is known about the relative importance of different characters for male mating success in this species. The importance of phenotypic characters for male mating success was quantified based on a long-term study of a Danish breeding population, by expressing phenotypic differences between mated and unmated males as the difference between log-transformed mean values. For field samples from Ukraine we likewise expressed the difference in male phenotype between individuals living in a relatively uncontaminated area and individuals from the Chernobyl region as the difference between log-transformed mean values. The standardized difference in male phenotype between the two regions in Ukraine for the 41 different characters was strongly positively correlated with the standardized difference in male phenotype between mated and unmated males from Denmark. The standardized difference in male phenotype between the two regions in Ukraine was significantly positively associated with sexual size dimorphism. However, the standardized difference in male phenotype between mated and unmated males was a much better predictor of standardized difference in male phenotype between the two regions in Ukraine than was the standardized difference in sexual size dimorphism, expressed as the difference between log-transformed mean values for males and females. These findings are consistent with the hypothesis that traits most important for sexual selection are particularly susceptible to the effects of deleterious mutations.
The expanding research interest in the last two decades on reactive oxygen species (ROS), oxidative stress, and male infertility has led to the development of various techniques for evaluating oxidative DNA damage in human spermatozoa. Measurement of 8-hydroxydeoxyguanosine (8-OHdG) offers a specific and quantitative biomarker on the extent of oxidative DNA damage caused by ROS in human sperm. The close correlations of 8-OHdG level with male fertility, sperm function and routine seminal parameters indicate the potential diagnostic value of this technique in clinical applications. On the other hand, single cell gel electrophoresis (SCGE or comet assay) and terminal deoxynucleotidyl transferase (TdT) mediated dUTP nick end labeling (TUNEL) assay have also been demonstrated to be sensitive, and reliable methods for measuring DNA strand breaks in human spermatozoa. As certain technical limitations were inherent in each of these tests, it is believed that a combination of these assays will offer more comprehensive information for a better understanding of oxidative DNA damage and its biological significance in sperm function and male infertility.
Reactive oxygen species (ROS) have a negative impact on sperm DNA, leading to the formation of oxidative products such as 8-oxo-7,8-dihydroxyguanosine. This compound causes fragmentation and, thus, has a mutagenic effect. Patient treatment with oral antioxidant vitamins is, therefore, standard practice for male infertility, in an attempt to decrease formation of ROS and improve fertility. In this study, the DNA fragmentation index and the degree of sperm decondensation were measured using the sperm chromatin structure assay before and after 90 days treatment with antioxidant vitamins associated with zinc and selenium. Antioxidant treatment led to a decrease in sperm DNA fragmentation (-19.1%, P < 0.0004), suggesting that at least part of the decay was linked to ROS. However, it also led to an unexpected negative effect: an increase in sperm decondensation with the same order of magnitude (+22.8%, P < 0.0009). The opening of interchain disulphide bridges in protamines may explain this aspect, as antioxidant vitamins, especially vitamin C, are able to open the cystin net, thus interfering with paternal gene activity during preimplantation development. This observation might explain the discrepancy observed concerning the role of these antioxidant treatments in improving male fertility.
We investigated levels of DNA damage in blood cells of barn swallows (Hirundo rustica) inhabiting the Chernobyl region to evaluate whether chronic exposure to low-level radioactive contamination continues to induce genetic damage in free-living populations of animals. Blood samples were obtained from barn swallows collected at sites with different background levels of radiation, including a relatively uncontaminated area. The extent of DNA damage was evaluated using the alkaline (pH=12.1) comet assay, a robust and sensitive electrophoresis-based technique widely employed in research ranging from biomonitoring to clinical studies. We found that levels of DNA damage, as indexed by the extent of DNA migration, were increased in barn swallows living in areas surrounding Chernobyl when compared to swallows sampled at low-level sites. The results we obtained are consistent with previous findings on this same species, which showed that swallows breeding in areas heavily contaminated with radionuclides have increased mutation rates, higher oxidative stress and incidence of morphological aberrations and tumors. Overall, these results indicate that chronic exposure to radioactive contaminants, even 20years after the accident at the Chernobyl nuclear power plant, continues to induce DNA damage in cells of free-living animals.
The Chernobyl nuclear accident produced the largest unintended release of radionuclides in history, with dramatic consequences for humans and other organisms. Exposure to ionizing radiation is known to reduce circulating and stored levels of specific antioxidants in birds and humans, thus potentially increasing oxidative stress. However, overall effects of radioactive exposure on oxidative status have never been investigated in any free ranging vertebrate. We measured plasma antioxidant capacity and concentration of reactive oxygen metabolites in adult barn swallows (Hirundo rustica) from colonies with variable background radiation levels in the Chernobyl region in Ukraine and Belarus. We predicted that antioxidants would decrease while reactive oxygen metabolites would increase with exposure to increasing levels of radiation at the breeding sites. Consistent with this expectation, radiation level positively predicted plasma concentration of reactive oxygen metabolites, whereas no significant covariation was found with non-enzymatic plasma antioxidant capacity. An index of oxidative stress was also larger in barn swallows exposed to high contamination levels. Thus, radioactive contamination appeared to be responsible for the increased generation of reactive oxygen metabolites and the imbalance between reactive oxygen metabolites and non-enzymatic plasma antioxidant capacity.
DNA damage is a common feature of human spermatozoa with purported links to poor rates of conception, impaired embryonic development, an increased incidence of miscarriage and the appearance of various kinds of morbidity in the offspring including childhood cancer. However, difficulties in interpretation arise, because these associations are not consistently observed across all data sets. Such inconsistency reflects the inherent complexity of the reproductive process, large variations in sample size, differences in patient selection, inadequate study design as well as inter-individual differences in the type of DNA damage being detected and the effectiveness of repair mechanisms in the oocyte. This review considers the type, source and measurement of DNA damage in human spermatozoa. It also addresses the clinical utility of the information generated in such studies, and highlights areas where further research is needed to bridge the gap between an intriguing biological phenomenon and the evidence-based clinical management of male patients characterized by high levels of DNA damage in their spermatozoa.
The concept of trade-offs is central to our understanding of life-history evolution. The underlying mechanisms, however, have been little studied. Oxidative stress results from a mismatch between the production of damaging reactive oxygen species (ROS) and the organism's capacity to mitigate their damaging effects. Managing oxidative stress is likely to be a major determinant of life histories, as virtually all activities generate ROS. There is a recent burgeoning of interest in how oxidative stress is related to different components of animal performance. The emphasis to date has been on immediate or short-term effects, but there is an increasing realization that oxidative stress will influence life histories over longer time scales. The concept of oxidative stress is currently used somewhat loosely by many ecologists, and the erroneous assumption often made that dietary antioxidants are necessarily the major line of defence against ROS-induced damage. We summarize current knowledge on how oxidative stress occurs and the different methods for measuring it, and highlight where ecologists can be too simplistic in their approach. We critically review the potential role of oxidative stress in mediating life-history trade-offs, and present a framework for formulating appropriate hypotheses and guiding experimental design. We indicate throughout potentially fruitful areas for further research.
Although oxidative stress is a central topic in biochemical and medical research, the number of reports on its relevance in life-history studies of non-human animals is still low. Information about oxidative stress in wild birds may help describe functional interactions among the components of life-history traits. Currently available evidence suggests that oxidative stress may impart an important physiological cost on longevity, reproduction, immune response or intense physical activity. Given the gaps in our present knowledge, it is still premature to attempt to draw definitive conclusions and basic questions (e.g. how is oxidative stress generated and how do organisms cope with it?) have yet to be fully explored under natural conditions. Therefore, caution is needed in developing hypotheses or drawing general conclusions until additional data become available to perform more rigorous comparative analyses.
Aerobic incubation of human spermatozoa in the presence of catalytic amounts of ascorbate and ferrous ion results in rapid peroxidative breakdown of sperm phospholipids and fatty acids; most strongly affected are phosphatidyl ethanolamine, ethanolamine plasmalogen, and docosahexanoic acid. Both peroxidation of the endogenous sperm phospholipid and the concurrent loss of motility can be fully prevented, but not reversed, by an "antiperoxidant" factor present in human seminal plasma. Exogenously applied lipid peroxides are powerfully spermicidal. Washed human spermatozoa, at a concentration normally present in semen, treated with as little as 30 nmoles of lipid peroxide/ml become irreversibly immotile within a few minutes. The antiperoxidant factor present in human seminal plasma effectively counteracts the toxic effect of exogenous peroxidized fatty acids upon human spermatozoa, but is unable to restore motility lost by lipid peroxide action.
Mammalian spermatozoa are sensitive to oxygen-induced damages mediated by lipid peroxidation of the cell membrane. The aim of this study was to evaluate whether reactive oxygen species (ROS) could also induce axonemal damage. When Percoll-separated spermatozoa were treated with hydrogen peroxide, or the combination xanthine and xanthine oxidase (X + XO), there was a progressive decrease, leading to a complete arrest, in sperm flagellar beat frequency. Once demembranated in a medium containing magnesium adenosine triphosphate (Mg.ATP), ROS-immobilized spermatozoa still reactivated motility; however, the percentage and duration of motility obtained in these tests gradually decreased to zero in the next hour. In 50% of the cases, motility of intact spermatozoa spontaneously reinitiated after 6 to 24 hours of immobilization due to ROS treatment, although with percentages and beat frequencies lower than those of untreated spermatozoa. Studies using ROS scavengers (such as catalase, superoxide dismutase, and dimethylsulfoxide) indicated that hydrogen peroxide was the most toxic of the ROS involved, but that .O2- and .OH probably also played a role in immobilization of spermatozoa by ROS. The data suggest that ROS induce a chain of events leading to sperm immobilization, that axonemes are affected, and that limited endogenous repair mechanisms exist to reverse these damages.
To determine the incidence of reactive oxygen species formation in semen of a population of patients consulting for infertility.
The incidence of reactive oxygen species formation in whole semen and in washed spermatozoa was studied. The values obtained were correlated with semen parameters. The effect of the type of sperm washing on reactive oxygen species formation was also investigated.
Semen samples from patients consulting for infertility and control subjects were obtained by masturbation after 3 days of sexual abstinence. Reactive oxygen species formation was measured in whole semen, sperm suspension washed by Percoll gradients, or repeated centrifugations. Sperm motility parameters were measured by computer-aided sperm analysis.
Fertile control men and an unselected population of patients consulting for infertility.
None.
Reactive oxygen species formation by fresh semen specimen or washed spermatozoa was measured in a computer-driven LKB 1251 Luminometer (LKB-Wallac, Turku, Finland).
Reactive oxygen species formation was detected in 40% of the semen with spermatozoa from infertile patients, whereas none was found in 6 azoospermic men and 10 control men. The level of reactive oxygen species formation was inversely correlated to the semen volume, the percentage of motile spermatozoa, and sperm linearity both in semen and in Percoll-washed spermatozoa. Washing by repeated centrifugation-resuspension increased 20- to 50-fold sperm reactive oxygen species formation. This enhancement was caused by the centrifugation itself and by the removal of seminal plasma. Both morphologically normal and abnormal spermatozoa produced reactive oxygen species.
The data suggest that reactive oxygen species formation by spermatozoa may be a significant cause for male infertility.
A major portion of the toxicity of hydrogen peroxide in Escherichia coli is attributed to DNA damage mediated by a Fenton
reaction that generates active forms of hydroxyl radicals from hydrogen peroxide, DNA-bound iron, and a constant source of
reducing equivalents. Kinetic peculiarities of DNA damage production by hydrogen peroxide in vivo can be reproduced by including
DNA in an in vitro Fenton reaction system in which iron catalyzes the univalent reduction of hydrogen peroxide by the reduced
form of nicotinamide adenine dinucleotide (NADH). To minimize the toxicity of oxygen radicals, the cell utilizes scavengers
of these radicals and DNA repair enzymes. On the basis of observations with the model system, it is proposed that the cell
may also decrease such toxicity by diminishing available NAD(P)H and by utilizing oxygen itself to scavenge active free radicals
into superoxide, which is then destroyed by superoxide dismutase.
Adult male mice were given gonadal doses of 0-1200 rad acute X-irradiation and mated the same day. 531 sons, conceived within a week of the treatment, were tested for fertility and their testes examined cytologically for chromosome aberrations in spermatocytes. 55 57 of those diagnosed as semi-sterile and 35 40 of those diagnosed as sterile were judged to be heterozygous for one or more reciprocal translocations. Numbers of 0,1,2 | translocations per mouse showed a good fit to a Poisson distribution, in contrast to previous findings with spermatogonial irradiation. Although the dose response fitted a linear relationship, the power law equation of best fit had a doseexponent of 1.41. Further analysis along similar lines to those used previously in Drosophila by Catcheside, Lea and Haldane, which assumed random rejoining of breaks and direct proportionality between dosage and number of breaks, gave a close fit between the actual results and those expected if αq = 2.8 · 10-3/rad, where α is the mean number of breaks per nucleus and q is the proportion which rejoin or restitute. By combining these data with those for litter-size reduction in F1 (taken as a measure of induced dominant lethality) α was estimated to be 3.4 × 10-3 per rad. When compared with the value of 0.8 × 10-3 per rad obtained in Drosophila by Haldane and Lea, this suggested that mouse haploid nuclei are more radiosensitive to chromosome breakage than Drosophila haploid nuclei by a factor of about 4. The mean number of implants per pregnant female mated to cytologically abnormal males was about 15% lower than with normal males. This pre-implantation loss was thought to be mainly the result of a reduction in the rate of fertilization in this group rather than to early death of unbalanced zygotes. There was no evidence for the induction of any undetected types of chromosomal aberration or gene mutation which could cause intrauterin death in the progeny of F1 males.
The ability of samples of semen from individual male fowl to form the products of lipid peroxidation during 5 h aerobic incubation at 40 degrees C varied between 0 and 8 nmol malonaldehyde/10(9) spermatozoa. Formation of higher concentrations of malonaldehyde was associated with a partial or complete loss of fertilizing ability whilst the fertilizing ability of samples producing low or negligible concentrations of malonaldehyde remained unimpaired. The semen of birds which showed a tendency to form high concentrations of malonaldehyde was not readily identifiable as abnormal by assessment of sperm motility, morphology or ATP content. Nor was the loss of fertilizing ability during aerobic incubation associated with an obvious change in these characteristics.