Large-scale changes in marine and terrestrial environments drive the population dynamics of long-tailed ducks breeding in Siberia.

Migratory animals experience very different environmental conditions at different times of the year, i.e., at the breeding grounds, during migration, and in winter. The long-tailed duck Clangula hyemalis breeds in the Arctic regions of the northern hemisphere and migrates to temperate climate zones, where it winters in marine environments. The breeding success of the long-tailed duck is affected by the abundances of predators and their main prey species, lemmings Lemmus sibiricus and Dicrostonyx torquatus, whose population fluctuation is subject to climate change. In the winter quarters, long-tailed ducks mainly eat the blue mussel Mytilus edulis. We examined how North-west Siberian lemming dynamics, assumed as a proxy for predation pressure, affect long-tailed duck breeding success and how nutrient availability in the Baltic Sea influences long-tailed duck population size via mussel biomass and quality. Evidence suggests that the long-tailed duck population dynamics was predator-driven on the breeding grounds and resource-driven on the wintering grounds. Nutrients from fertilizer runoff from farmland stimulate mussel stocks and quality, supporting high long-tailed duck population sizes. The applied hierarchical analysis combining several trophic levels can be used for evaluating large-scale environmental factors that affect the population dynamics and abundance of migrants from one environment to another.

Effects of climate variation on bird escape distances modulate community responses to global change.

Climate and land use are rapidly changing environmental conditions. Behavioral responses to such global perturbations can be used to incorporate interspecific interactions into predictive models of population responses to global change. Flight initiation distance (FID) reflects antipredator behaviour defined as the distance at which an individual takes flight when approached by a human, under standardized conditions. This behavioural trait results from a balance between disturbance, predation risk, food availability and physiological needs, and it is related to geographical range and population trends in European birds. Using 32,145 records of flight initiation distances for 229 bird species during 2006-2019 in 24 European localities, we show that FIDs decreased with increasing temperature and precipitation, as expected if foraging success decreased under warm and humid conditions. Trends were further altered by latitude, urbanisation and body mass, as expected if climate effects on FIDs were mediated by food abundance and need, differing according to position in food webs, supporting foraging models. This provides evidence for a role of behavioural responses within food webs on how bird populations and communities are affected by global change.

Reduced colonization by soil invertebrates to irradiated decomposing wood in Chernobyl.

Soil is inhabited by a range of microbes, invertebrates and vertebrates that disintegrate and decompose dead wood and leaf litter. These communities can be perturbed by ionizing radiation from natural radiation sources or from radiation originating from nuclear accidents such as those at Chernobyl, Fukushima and Three Mile Island. We used experimental manipulations of wood quality due to differences in exposure to ionizing radiation among tree trunks and ambient radiation levels of the soil to test the hypothesis that radioactively contaminated wood would result in a negative correlation between the abundance of soil invertebrates colonizing slices of wood and level of radioactive contamination. We extracted soil invertebrates underneath decomposing wood using mustard powder diluted in water. The abundance of soil invertebrates extracted was highly repeatable at study sites and decreased with increasing ambient radiation and total dose measured with thermoluminescent dosimeters (TLDs). Four 10 cm thick slices of ca. 70-year old Scots pines (Pinus sylvestris) were deposited at 20 sites and the invertebrate taxa and their colonization and their abundance was assessed annually during 2014-2017. There were more soil invertebrates under uncontaminated than contaminated slices of wood. In addition, there were more soil invertebrates in areas with less ambient radioactivity, and there was an interaction effect between contamination of wood and ambient radiation implying that the role of contamination differed among slices. Finally, there was an increase in the abundance of soil invertebrates under wood slices during 2013-2017 implying that the abundance of soil invertebrates increased over time. These findings imply that the abundance of soil animals colonizing wood slices was dependent on background radiation, radioactive contamination of wood and the interaction between contamination of wood and ambient radiation.

Escape from predators and genetic variance in birds.

Predation is a common cause of death in numerous organisms, and a host of antipredator defences have evolved. Such defences often have a genetic background as shown by significant heritability and microevolutionary responses towards weaker defences in the absence of predators. Flight initiation distance (FID) is the distance at which an individual animal takes flight when approached by a human, and hence, it reflects the life-history compromise between risk of predation and the benefits of foraging. Here, we analysed FID in 128 species of birds in relation to three measures of genetic variation, band sharing coefficient for minisatellites, observed heterozygosity and inbreeding coefficient for microsatellites in order to test whether FID was positively correlated with genetic variation. We found consistently shorter FID for a given body size in the presence of high band sharing coefficients, low heterozygosity and high inbreeding coefficients in phylogenetic analyses after controlling statistically for potentially confounding variables. These findings imply that antipredator behaviour is related to genetic variance. We predict that many threatened species with low genetic variability will show reduced antipredator behaviour and that subsequent predator-induced reductions in abundance may contribute to unfavourable population trends for such species.

Viability and expression of sexual ornaments in the barn swallow Hirundo rustica: a meta-analysis.

Sexual selection results in the evolution of exaggerated secondary sexual characters that can entail a viability cost. However, in species where sexual ornaments honestly reflect individual quality, the viability cost of secondary sexual characters may be overwhelmed by variation in individual quality, leading to expect that individuals with the largest secondary sexual characters show higher, rather than lower viability. Here, we used meta-analyses to test whether such expected positive relationship between sexual ornamentation and viability exists in the barn swallow Hirundo rustica, which is one of the most studied model species of sexual selection under field conditions. We found a mean positive effect size of viability in relation to the expression of secondary sexual characters of 0.181 (CI: 0.084-0.278), indicating that in this species the more ornamented individuals are more viable, and therefore of high quality. Analyses of moderator variables showed similar effects in males and females, the H. r. rustica subspecies rather than others and tail length rather than other secondary sexual characters. Future research emphasis on other subspecies than the European one and secondary sexual characters than tail length may help identify the sources of heterogeneity in effect sizes.

Morphological constraints on changing avian migration phenology.

Many organisms at northern latitudes have responded to climate warming by advancing their spring phenology. Birds are known to show earlier timing of spring migration and reproduction in response to warmer springs. However, species show heterogeneous phenological responses to climate warming, with those that have not advanced or have delayed migration phenology experiencing population declines. Although some traits (such as migration distance) partly explain heterogeneity in phenological responses, the factors affecting interspecies differences in the responsiveness to climate warming have yet to be fully explored. In this comparative study, we investigate whether variation in wing aspect ratio (reflecting relative wing narrowness), an ecomorphological trait that is strongly associated with flight efficiency and migratory behaviour, affects the ability to advance timing of spring migration during 1960-2006 in a set of 80 European migratory bird species. Species with larger aspect ratio (longer and narrower wings) showed smaller advancement of timing of spring migration compared to species with smaller aspect ratio (shorter and wider wings) while controlling for phylogeny, migration distance and other life-history traits. In turn, migration distance positively predicted aspect ratio across species. Hence, species that are better adapted to migration appear to be more constrained in responding phenologically to rapid climate warming by advancing timing of spring migration. Our findings corroborate the idea that aspect ratio is a major evolutionary correlate of migration, and suggest that selection for energetically efficient flights, as reflected by high aspect ratio, may hinder phenotypically plastic/microevolutionary adjustments of migration phenology to ongoing climatic changes.

Life history, immunity, Peto's paradox and tumours in birds.

Cancer and tumours may evolve in response to life-history trade-offs between growth and duration of development on one hand, and between growth and maintenance of immune function on the other. Here, we tested whether (i) bird species with slow developmental rates for their body size experience low incidence of tumours because slow development allows for detection of rapid proliferation of cell lineages. We also test whether (ii) species with stronger immune response during development are more efficient at detecting tumour cells and hence suffer lower incidence of tumours. Finally, we tested Peto's paradox, that there is a positive relationship between tumour incidence and body mass. We used information on developmental rates and body mass from the literature and of tumour incidence (8468 birds) and size of the bursa of Fabricius for 7659 birds brought to a taxidermist in Denmark. We found evidence of the expected negative relationship between incidence of tumours and developmental rates and immunity after controlling for the positive association between tumour incidence and body size. These results suggest that evolution has modified the incidence of tumours in response to life history and that Peto's paradox may be explained by covariation between body mass, developmental rates and immunity.

Resuspension and atmospheric transport of radionuclides due to wildfires near the Chernobyl Nuclear Power Plant in 2015: An impact assessment.

In April and August 2015, two major fires in the Chernobyl Exclusion Zone (CEZ) caused concerns about the secondary radioactive contamination that might have spread over Europe. The present paper assessed, for the first time, the impact of these fires over Europe. About 10.9 TBq of (137)Cs, 1.5 TBq of (90)Sr, 7.8 GBq of (238)Pu, 6.3 GBq of (239)Pu, 9.4 GBq of (240)Pu and 29.7 GBq of (241)Am were released from both fire events corresponding to a serious event. The more labile elements escaped easier from the CEZ, whereas the larger refractory particles were removed more efficiently from the atmosphere mainly affecting the CEZ and its vicinity. During the spring 2015 fires, about 93% of the labile and 97% of the refractory particles ended in Eastern European countries. Similarly, during the summer 2015 fires, about 75% of the labile and 59% of the refractory radionuclides were exported from the CEZ with the majority depositing in Belarus and Russia. Effective doses were above 1 mSv y(-1) in the CEZ, but much lower in the rest of Europe contributing an additional dose to the Eastern European population, which is far below a dose from a medical X-ray.

Ionizing radiation, antioxidant response and oxidative damage: A meta-analysis.

One mechanism proposed as a link between exposure to ionizing radiation and detrimental effects on organisms is oxidative damage. To test this hypothesis, we surveyed the scientific literature on the effects of chronic low-dose ionizing radiation (LDIR) on antioxidant responses and oxidative damage. We found 40 publications and 212 effect sizes for antioxidant responses and 288 effect sizes for effects of oxidative damage. We performed a meta-analysis of signed and unsigned effect sizes. We found large unsigned effects for both categories (0.918 for oxidative damage; 0.973 for antioxidant response). Mean signed effect size weighted by sample size was 0.276 for oxidative damage and -0.350 for antioxidant defenses, with significant heterogeneity among effects for both categories, implying that ionizing radiation caused small to intermediate increases in oxidative damage and small to intermediate decreases in antioxidant defenses. Our estimates are robust, as shown by very high fail-safe numbers. Species, biological matrix (tissue, blood, sperm) and age predicted the magnitude of effects for oxidative damage as well as antioxidant response. Meta-regression models showed that effect sizes for oxidative damage varied among species and age classes, while effect sizes for antioxidant responses varied among species and biological matrices. Our results are consistent with the description of mechanisms underlying pathological effects of chronic exposure to LDIR. Our results also highlight the importance of resistance to oxidative stress as one possible mechanism associated with variation in species responses to LDIR-contaminated areas.

Environmental conditions during early life accelerate the rate of senescence in a short-lived passerine bird.

Environmental conditions experienced in early life may shape subsequent phenotypic traits including life history. We investigated how predation risk caused by domestic cats (Felis silvestris catus) and local breeding density affected patterns of reproductive and survival senescence in Barn Swallows (Hirundo rustica) breeding semicolonially in Denmark. We recorded the abundance of cats and the number of breeding pairs at 39 breeding sites during 24 years and related these to age-specific survival rate and reproductive senescence to test predictions of the life history theory of senescence. We found evidence for actuarial senescence for the first time in this species. Survival rate increased until reaching a plateau in midlife and then decreased later. We also found that survival rate was higher for males than females. Local breeding density or predation risk did not affect survival as predicted by theory. Barn Swallows with short lives did not invest more in reproduction in early life, inconsistent with expectations for trade-offs between reproduction and survival as theory suggests. However, we found that the rate of reproductive decline during senescence was steeper for individuals exposed to intense competition, and predation pressure accelerated the rate of reproductive senescence, but only in sites with many breeding pairs. These latter results are in accordance with one of the predictions suggested by the life history theory of aging. These results emphasize the importance of considering intraspecific competition and interspecific interactions such as predation when analyzing reproductive and actuarial senescence.

Abundance and genetic damage of barn swallows from Fukushima.

A number of studies have assessed or modeled the distribution of the radionuclides released by the accident at the Fukushima-Daiichi Nuclear Power Plant (FDNPP). Few studies however have investigated its consequences for the local biota. We tested whether exposure of barn swallow (Hirundo rustica) nestlings to low dose ionizing radiation increased genetic damage to their peripheral erythrocytes. We estimated external radiation exposure by using thermoluminescent dosimeters, and by measuring radioactivity of the nest material. We then assessed DNA damage by means of the neutral comet assay. In addition, we conducted standard point-count censuses of barn swallows across environmental radiation levels, and estimated their abundance and local age ratio. Radioactivity of nest samples was in the range 479-143,349 Bq kg(-1), while external exposure varied between 0.15 and 4.9 mGy. Exposure to radioactive contamination did not correlate with higher genetic damage in nestlings. However, at higher levels of radioactive contamination the number of barn swallows declined and the fraction of juveniles decreased, indicating lower survival and lower reproduction and/or fledging rate. Thus, genetic damage to nestlings does not explain the decline of barn swallows in contaminated areas, and a proximate mechanism for the demographic effects documented here remains to be clarified.

Life history, predation and flight initiation distance in a migratory bird.

Life-history trade-offs occur as a consequence of the compromise between maximization of different components such as the size and the number of clutches. Flight initiation distance (FID) potentially constitutes a general proximate factor influencing such trade-offs reflecting the risks that individuals take. Therefore, greater investment in reproduction occurs at a higher risk of death, resulting in selection for efficient flight morphology. I analysed long-term data on FID in a population of barn swallows Hirundo rustica during 1984-2013 with 2196 records of FID for 1789 individuals. FID had a repeatability of 0.62 (SE = 0.04) and a heritability of 0.48 (SE = 0.07). FID varied between individuals and sites, and it increased over time as climate ameliorated. FID showed a U-shaped relationship with age, with young and very old individuals having the longest FIDs. Barn swallows that arrived early from spring migration, started to breed early and produced many fledglings had the longest FID. Individuals with the longest tails had the longest FID, and individuals with the shortest aspect ratios and wing loadings had the longest FID. Individuals that died from predation had shorter FID than survivors. These findings are consistent with the hypothesis that FID relates directly to life history, with longer FIDs being associated with smaller levels of risk-taking.

Recognizing odd smells and ejection of brood parasitic eggs. An experimental test in magpies of a novel defensive trait against brood parasitism.

One of the most important defensive host traits against brood parasitism is the detection and ejection of parasitic eggs from their nests. Here, we explore the possible role of olfaction in this defensive behaviour. We performed egg-recognition tests in magpie Pica pica nests with model eggs resembling those of parasitic great spotted cuckoos Clamator glandarius. In one of the experiment, experimental model eggs were exposed to strong or moderate smell of tobacco smoke, whereas those of a third group (control) were cleaned with disinfecting wipes and kept in boxes containing odourless cotton. Results showed that model eggs with strong tobacco scent were more frequently ejected compared with control ones. In another experiment, models were smeared with scents from cloacal wash from magpies (control), cloacal wash or uropygial secretions from cuckoos, or human scents. This experiment resulted in a statistically significant effect of treatment in unparasitized magpie nests in which control model eggs handled by humans were more often rejected. These results provide the first evidence that hosts of brood parasites use their olfactory ability to detect and eject foreign eggs from their nests. These findings may have important consequences for handling procedures of experimental eggs used in egg-recognition tests, in addition to our understanding of interactions between brood parasites and their hosts.

Predator-prey interactions, flight initiation distance and brain size.

Prey avoid being eaten by assessing the risk posed by approaching predators and responding accordingly. Such an assessment may result in prey-predator communication and signalling, which entail further monitoring of the predator by prey. An early antipredator response may provide potential prey with a selective advantage, although this benefit comes at the cost of disturbance in terms of lost foraging opportunities and increased energy expenditure. Therefore, it may pay prey to assess approaching predators and determine the likelihood of attack before fleeing. Given that many approaching potential predators are detected visually, we hypothesized that species with relatively large eyes would be able to detect an approaching predator from afar. Furthermore, we hypothesized that monitoring of predators by potential prey relies on evaluation through information processing by the brain. Therefore, species with relatively larger brains for their body size should be better able to monitor the intentions of a predator, delay flight for longer and hence have shorter flight initiation distances than species with smaller brains. Indeed, flight initiation distances increased with relative eye size and decreased with relative brain size in a comparative study of 107 species of birds. In addition, flight initiation distance increased independently with size of the cerebellum, which plays a key role in motor control. These results are consistent with cognitive monitoring as an antipredator behaviour that does not result in the fastest possible, but rather the least expensive escape flights. Therefore, antipredator behaviour may have coevolved with the size of sense organs, brains and compartments of the brain involved in responses to risk of predation.

High frequency of albinism and tumours in free-living birds around Chernobyl.

The effects of radioactive contamination on the phenotype of free-living organisms are poorly understood, mainly because of the difficulty of capturing the large numbers of individual specimens that are required to quantify rare events such as albinism and tumour formation. We hypothesized that the frequency of abnormalities like albinism and the frequency of radiation-induced diseases like cancer would increase with the level of background radiation, that the two markers of radiation would be positively correlated, and that the reduction in abundance of animals would be greater in species with a higher frequency of albinism and tumour formation, if these markers reliably reflected poor viability. Here we analyzed the frequency of albinistic feathers and tumours in a sample of 1669 birds captured during 2010-2012 at eight sites around Chernobyl that varied in level of background radiation from 0.02 to more than 200µSv/h. We recorded 111 cases of partial albinism and 25 cases of tumour formation. Nominal logistic models were used to partition the variance into components due to species and background radiation. Radiation was a strong predictor of the two markers in birds, with a small, but significant effect of species for albinism. The slope of the relationship between abundance and radiation in different bird species was significantly inversely correlated with the frequency of albinism and tumours, as was to be expected if a common underlying cause (i.e. radiation) affects both variables. These findings are consistent with the hypothesis that background radiation is a cause of albinism and tumours, that albinism and tumours are biomarkers of radiation exposure, and that high frequencies of albinism and tumours were present despite the low viability of birds with these conditions.

Risk-taking and the evolution of mechanisms for rapid escape from predators.

Flight initiation distance (FID) is the distance at which an individual animal takes flight when approached by a human. This behavioural measure of risk-taking reflects the risk of being captured by real predators, and it correlates with a range of life history traits, as expected if flight distance optimizes risk of predation. Given that FID provides information on risk of predation, we should expect that physiological and morphological mechanisms that facilitate flight and escape predict interspecific variation in flight distance. Haematocrit is a measure of packed red blood cell volume and as such indicates the oxygen transport ability and hence the flight muscle contracting reaction of an individual. Therefore, we predicted that species with short flight distances, that allow close proximity between a potential prey individual and a predator, would have high haematocrit. Furthermore, we predicted that species with large wing areas and hence relatively low costs of flight and species with large aspect ratios and hence high manoeuvrability would have evolved long flight speed. Consistent with these predictions, we found in a sample of 63 species of birds that species with long flight distances for their body size had low levels of haematocrit and large wing areas and aspect ratios. These findings provide evidence consistent with the evolution of risk-taking behaviour being underpinned by physiological and morphological mechanisms that facilitate escape from predators and add to our understanding of predator-prey coevolution.

Geographical variation in reproductive ageing patterns and life-history strategy of a short-lived passerine bird.

We investigated differences in ageing patterns in three measures of breeding performance in populations of barn swallows Hirundo rustica L. from Spain and Denmark differing in breeding latitude and hence migration distance and duration of the breeding season. We found differences in ageing patterns between populations. Generally, young (i.e. yearling) and old females (i.e. ≥ 5 years of age) laid their first eggs later and produced smaller clutches than middle-aged females (i.e. 2-4 years of age) in both populations. The southernmost population (i.e. Spanish) showing the shorter migratory distance experienced a greater within-individual increase in timing of breeding and clutch size in early life and a greater within-individual decrease in laying date but not in clutch size during senescence compared with the northernmost population (i.e. Danish). We also found that the number of fledglings produced annually was related to the age of the two members of the breeding pairs with pairs composed of young and old females performing less well than breeding pairs composed of middle-aged females. We did not find reproductive senescence for the age of the male while controlling for the age of the female on the number of fledglings produced annually by the breeding pair. Differential survival between individuals did not explain age effects on laying date or annual clutch size in neither population. However, the increase in the number of fledglings produced annually with age was partly explained by the disappearance of poor-quality members of the pairs, mainly poor-quality males. Age-related breeding success (i.e. number of fledglings) was similar for barn swallows from Spain and Denmark. Therefore, the study of ageing patterns and life-history strategies in free-ranging animals from more than a single population can throw new light on life-history theory, population dynamics and evolutionary studies of senescence.

The evolution of size of the uropygial gland: mutualistic feather mites and uropygial secretion reduce bacterial loads of eggshells and hatching failures of European birds.

Potentially, pathogenic bacteria are one of the main infective agents against which a battery of chemical and physical barriers has evolved in animals. Among these are the secretions by the exocrine uropygial gland in birds. The antimicrobial properties of uropygial secretions may prevent colonization and growth of microorganisms on feathers, skin and eggshells. However, uropygial gland secretions also favour the proliferation of feather mites that feed on secretions and microorganisms living on feathers that would otherwise reach eggshells during incubation if not consumed by feather mites. Therefore, at the interspecific level, uropygial gland size (as an index of volume of uropygial secretion) should be positively related to eggshell bacterial load (i.e. the risk of egg infection), whereas eggshell bacterial loads may be negatively related to abundance of feather mites eating bacteria. Here, we explore these previously untested predictions in a comparative framework using information on eggshell bacterial loads, uropygial gland size, diversity and abundance of feather mites and hatching success of 22 species of birds. The size of the uropygial gland was positively related to eggshell bacterial loads (mesophilic bacteria and Enterobacteriaceae), and bird species with higher diversity and abundance of feather mites harboured lower bacterial density on their eggshells (Enterococcus and Staphylococcus), in accordance with the hypothesis. Importantly, eggshell bacterial loads of mesophilic bacteria, Enterococcus and Enterobacteriaceae were negatively associated with hatching success, allowing us to interpret these interspecific relationships in a functional scenario, where both uropygial glands and mutualistic feather mites independently reduce the negative effects of pathogenic bacteria on avian fitness.

Effects of parental radiation exposure on developmental instability in grasshoppers.

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.