Effects of chronic exposure to toxic metals on haematological parameters in free-ranging small mammals.

Blood circulates through the vascular system to carry oxygen, nutrients and metabolites to and away from tissues, and as such is a key-component of animal physiology. The impacts of metal pollution on blood, however, are poorly documented in free-ranging vertebrates. While the counteracting effect of selenium on mercury toxicity is well known in marine mammals, its potential role against the toxicity of other metals is less studied, especially on terrestrial wildlife. We explored the consequences of chronic exposure to two non-essential metals (cadmium and lead) along a pollution gradient in Northern France, on eleven haematological parameters in two free ranging small mammals, the wood mouse Apodemus sylvaticus and the bank vole Myodes glareolus. We hypothesized that haematology was related to metal concentrations in tissues, and that selenium might exert modulating effects. Concentrations of cadmium and lead in the tissues indicated an increased chronic exposure to and accumulation of metals along the gradient. Some haematological parameters were not explained by any measured variables while some others varied only with gender or age. Red blood cells, red blood cells distribution width, and blood iron concentration, however, decreased with increasing cadmium in the tissues in wood mice. Red blood cells and haemoglobin decreased with increasing renal lead and hepatic cadmium, respectively, in bank voles. Red blood cells distribution width in wood mice increased with cadmium concentrations in the liver but this was counteracted by high selenium levels in the same organ. An interaction of selenium and lead on red blood cells was also observed in bank voles. Further, selenium concentrations were associated with an increase of monocytes in wood mice. The present results show that toxic metals were related to haematology changes, particularly erythrocyte indicators, and that some essential elements like selenium should be measured as well since they may counteract toxic effects.

Pervasive exposure of wild small mammals to legacy and currently used pesticide mixtures in arable landscapes.

Knowledge gaps regarding the potential role of pesticides in the loss of agricultural biodiversity worldwide and mixture-related issues hamper proper risk assessment of unintentional impacts of pesticides, rendering essential the monitoring of wildlife exposure to these compounds. Free-ranging mammal exposure to legacy (Banned and Restricted: BRPs) and currently used (CUPs) pesticides was investigated, testing the hypotheses of: (1) a background bioaccumulation for BRPs whereas a "hot-spot" pattern for CUPs, (2) different contamination profiles between carnivores and granivores/omnivores, and (3) the role of non-treated areas as refuges towards exposure to CUPs. Apodemus mice (omnivore) and Crocidura shrews (insectivore) were sampled over two French agricultural landscapes (n = 93). The concentrations of 140 parent chemicals and metabolites were screened in hair samples. A total of 112 compounds were detected, showing small mammal exposure to fungicides, herbicides and insecticides with 32 to 65 residues detected per individual (13-26 BRPs and 18-41 CUPs). Detection frequencies exceeded 75% of individuals for 13 BRPs and 25 CUPs. Concentrations above 10 ng/g were quantified for 7 BRPs and 29 CUPs (in 46% and 72% of individuals, respectively), and above 100 ng/g for 10 CUPs (in 22% of individuals). Contamination (number of compounds or concentrations) was overall higher in shrews than rodents and higher in animals captured in hedgerows and cereal crops than in grasslands, but did not differ significantly between conventional and organic farming. A general, ubiquitous contamination by legacy and current pesticides was shown, raising issues about exposure pathways and impacts on ecosystems. We propose a concept referred to as "biowidening", depicting an increase of compound diversity at higher trophic levels. This work suggests that wildlife exposure to pesticide mixtures is a rule rather than an exception, highlighting the need for consideration of the exposome concept and questioning appropriateness of current risk assessment and mitigation processes.

Is blood a reliable indicator of trace metal concentrations in organs of small mammals?

In wildlife ecotoxicology, the rationale for using blood rather than other body fluids or tissues is that sampling blood is a minimally invasive technique without animal mortality, providing both ethical and scientific benefits. To date, few studies are available on the relationships between blood and organ metal concentrations of small mammals living in contaminated sites. The present work aimed to study the relationships between the concentrations of 18 essential and nonessential metals in blood and their concentrations in the liver and kidneys, two accumulation and target organs, in wood mice from a former lead and zinc smelter, Metaleurop Nord, in northern France. The results from Se, Pb and Tl indicate that blood levels may be used to predict concentrations in organs of small mammals. Conversely, for Cd, Cu, Fe, Mo, Ti and Zn, blood concentrations were poorly or not related to liver and kidney concentrations. In addition to accurately predicting the concentrations of some metals in target organs, blood can provide important information about the physiological and biochemical status of organisms, but further toxicokinetic research is required to develop the use of blood sampling as a minimally invasive biomonitoring and ecotoxicological method in wildlife.

Cold Tolerance and Sex-Dependent Hypothermia May Explain Winter Sexual Segregation in a Farmland Bird.

Migration is an important event in the life cycle of many organisms, but considerable intraspecific variation may occur in its timing and/or destination, resulting in sexual segregation during wintering periods. In this study, we tested the body size hypothesis, or cold tolerance hypothesis, which predicts that body size dimorphism modulates metabolic costs associated with cold climate. Using the Eurasian skylark, we first investigated whether this species showed sexual differential migration. Then we explored the body size hypothesis by experimentally testing the effect of low ambient temperature (Ta) on both metabolic rate (MR) and body temperature (Tb). We tested for sex-related differences in metabolism and in energy-saving mechanism (hypothermia). We found clear differential migration by sex in skylark wintering populations, with a male-biased sex ratio decreasing toward southern latitudes. Measurements on captive birds at 20°, 6°, and -5°C demonstrated a significant increase in MR when Ta decreased, but there is no difference between sexes. While both males and females reduced their Tb overnight, Tb reduction was more pronounced in females exposed to the coldest temperature treatment. In addition, we found that individuals with the most reduced Tb lost less body weight during the night, suggesting that Tb reduction may help minimize energy expenditure when conditions become constraining. Our study suggests that functional mechanisms may be involved in latitudinal segregation between sexes and supports the hypothesis that sex-specific physiological strategies and thermal tolerance may explain segregation between sexes.

Skylarks trade size and energy content in weed seeds to maximize total ingested lipid biomass.

The trade-off between forage quality and quantity has been particularly studied in herbivore organisms, but much less for seed eating animals, in particular seed-eating birds which constitute the bulk of wintering passerines in European farmlands. The skylark is one of the commonest farmland birds in winter, mainly feeding on seeds. We focus on weed seeds for conservation and management purposes. Weed seeds form the bulk of the diet of skylarks during winter period, and although this is still a matter for discussion, weed seed predation by granivorous has been suggested as an alternative to herbicides used to regulate weed populations in arable crops. Our objectives were to identify whether weed seed traits govern foraging decisions of skylarks, and to characterize key seed traits with respect to size, which is related to searching and handling time, and lipid content, which is essential for migratory birds. We combined a single-offer experiment and a multiple-offer one to test for feeding preferences of the birds by estimating seed intake on weed seed species differing in their seed size and seed lipid content. Our results showed (1) a selective preference for smaller seeds above a threshold of seed size or seed size difference in the pair and, (2) a significant effect of seed lipid biomass suggesting a trade-off between foraging for smaller seeds and selecting seeds rich in lipids. Skylarks foraging decision thus seems to be mainly based on seed size, that is presumably a 'proxy' for weed seed energy content. However, there are clearly many possible combinations of morphological and physiological traits that must play crucial role in the plant-bird interaction such as toxic compound or seed coat.

Sex-related differences in the trade-off between foraging and vigilance in a granivorous forager.

The relationship between intake rate and food density can provide the foundation for models that predict the spatiotemporal distribution of organisms across a range of resource densities. The functional response, describing the relationship between resource density and intake rate is often interpreted mechanistically as the relationships between times spend searching and handling. While several functional response models incorporate anti-predator vigilance (defined here as an interruption of feeding or some other activity to visually scan the environment, directed mainly towards detecting potential predators), the impacts of environmental factors influencing directly anti-predator vigilance remains unclear. We examined the combined effects of different scenarios of predation risk and food density on time allocation between foraging and anti-predator vigilance in a granivorous species. We experimentally exposed Skylarks to various cover heights and seed densities, and measured individual time budget and pecking and intake rates. Our results indicated that time devoted to different activities varied as a function of both seed density and cover height. Foraging time increased with seed density for all cover heights. Conversely, an increased cover height resulted in a decreased foraging time. Contrary to males, the decreased proportion of time spent foraging did not translate into a foraging disadvantage for females. When vegetation height was higher, females maintained similar pecking and intake rates compared to intermediate levels, while males consistently decreased their energy gain. This difference in anti-predator responses suggests a sexually mediated strategy in the food-safety trade-off: when resource density is high a females would adopt a camouflage strategy while an escape strategy would be adopted by males. In other words, males would leave risky-areas, whereas females would stay when resource density is high. Our results suggest that increased predation risk might generate sexually mediated behavioural responses that functional response models should perhaps better consider in the future.