The "parasite detoxification hypothesis": lead exposure potentially changes the ecological interaction from parasitism to mutualism.

In urban areas, organisms are exposed to high pollutant levels, especially element trace metals that may impact host-parasite interactions. Indeed, parasites have been reported to reduce the negative effects of pollutants on their hosts. The fitness of parasitized organisms in polluted environments may therefore be greater than that of unparasitized organisms. In our study, we used an experimental approach to test this hypothesis on feral pigeons (Columba livia), which are endemically parasitized by nematodes and exposed to high levels of lead in urban areas. We tested the combined effects of lead exposure and helminth parasitism on different pigeon fitness components: preening, immunocompetence, abundance of lice (Columbicola columbae) and haemosporidian parasites (Heamoproteus spp., Plasmodium spp.), reproduction investment, and oxidative stress. Our results show that among pigeons exposed to lead treatment, individuals harboring nematode parasites exhibit more preening activity and have fewer ectoparasites lice than nematode-free individuals. Benefits for nematode-parasitized individuals exposed to lead were not detected for other fitness parameters. Further studies are required to confirm the "parasite detoxification hypothesis" in pigeons and to identify the mechanisms by which this detoxification occurs.

Pigeon odor varies with experimental exposure to trace metal pollution.

Trace metals are chemical pollutants that have well-known noxious effects on wildlife and that are current major environmental issues in urban habitats. Previous studies have demonstrated their negative (e.g. lead) or positive (e.g. zinc) effects on body condition, immunity and reproductive success. Because of their effects on condition, trace metals are likely to influence the production of condition-dependent ornaments. The last decade has revealed that bird odors, like mammal odors, can convey information on individual quality and might be used as secondary sexual ornaments. Here, we used solid-phase microextraction headspace sampling with gas chromatography-mass spectrometry to investigate whether plumage scent varied with experimental supplementation in lead and/or zinc in feral pigeons. Zinc supplementation (alone or in combination with lead) changed the proportion of several volatiles, including an increase in the proportion of hydroxy-esters. The production of these esters, that most likely originate from preen gland secretions, may be costly and might thus be reduced by stress induced by zinc deficiency. Although lead is known to negatively impact pigeon condition, it did not statistically affect feather scent, despite most of the volatiles that increased with zinc exposure tended to be decreased in lead-supplemented pigeons. Further studies should evaluate the functions of plumage volatiles to predict how trace metals can impact bird fitness.

Do trace metals select for darker birds in urban areas? An experimental exposure to lead and zinc.

Trace metals from anthropogenic activities are involved in numerous health impairments and may therefore select for detoxification mechanisms or a higher tolerance. Melanin, responsible for the black and red colourations of teguments, plays a role in metal ion chelation and its synthesis is positively linked to immunity, antioxidant capacity and stress resistance due to pleiotropic effects. Therefore, we expected darker birds to (1) store higher amounts of metals in their feathers, (2) maintain lower metal concentrations in blood and (3) suffer less from metal exposure. We exposed feral pigeons (Columba livia) exhibiting various plumage darkness levels to low, but chronic, concentrations of zinc and/or lead, two of the most abundant metals in urban areas. First, we found negative and positive effects of lead and zinc, respectively, on birds' condition and reproductive parameters. Then, we observed positive relationships between plumage darkness and both zinc and lead concentrations in feathers. Interestingly, though darker adults did not maintain lower metal concentrations in blood and did not have higher fitness parameters, darker juveniles exhibited a higher survival rate than paler ones when exposed to lead. Our results show that melanin-based plumage colouration does modulate lead effects on birds' fitness parameters but that the relationship between metals, melanin, and fitness is more complex than expected and thus stress the need for more studies.

Sex-associated differences in trace metals concentrations in and on the plumage of a common urban bird species.

Urban areas encompass both favorable and stressful conditions linked with human activities and pollution. Pollutants remain of major ecological importance for synanthropic organisms living in the city. Plumage of urban birds harbour trace metals, which can result from external deposition or from internal accumulation. External and internal plumage concentrations likely differ between specific trace metals, and may further differ between males and females because of potential sex-linked differential urban use, physiology or behaviour. Here, we measured the concentrations in four trace metals (cadmium, copper, lead and zinc) in both unwashed and washed feathers of 49 male and 38 female feral pigeons (Columba livia) from Parisian agglomeration. We found that these concentrations indeed differed between unwashed and washed feathers, between males and females, and for some metals depended on the interaction between these factors. We discuss these results in the light of physiological and behavioural differences between males and females and of spatial repartition of the four trace metals in the city.

Feather bacterial load shapes the trade-off between preening and immunity in pigeons.

BACKGROUND: Complex communities of bacteria inhabit the feathers of all birds. Under normal conditions, individuals maintain a healthy state by defending themselves against these potential invaders by preening. The immune system is only triggered when bacteria gain access into the body. Preening is, however, costly and may trade-off with investment in the immune system. To shed light on how birds balance the trade-off between immunity and preen secretions when facing high or low feather bacterial load, we experimentally manipulated feather bacteria load of feral pigeons (Columba livia), and investigated the effects on immune defenses. RESULTS: Birds facing high feather bacterial load had lower immune response to PHA skin-swelling test (a measure of induced pro-inflammatory capacity) than controls, while birds facing low feather bacterial load had higher blood bacterial killing ability (a measure of the capacity to eliminate bacterial pathogens) than controls. No other components of the immune system (i.e., hemagglutination and hemolysis capacity of plasma, primary and secondary responses to KLH and quantity of blood parasites) were found to be affected by feather bacterial load. CONCLUSION: Pigeons had previously been shown to adjust preening to feather bacterial load. The decrease in the energetically costly inflammatory response of birds experiencing high bacterial load suggests a trade-off between investment in preen secretion and immunity and reinforces the idea that feather microbiota may have a strong impact on the ecology and evolution of the avian host.

Melanin-specific life-history strategies.

The maintenance of genetic variation is a long-standing issue because the adaptive value of life-history strategies associated with each genetic variant is usually unknown. However, evidence for the coexistence of alternative evolutionary fixed strategies at the population level remains scarce. Because in the tawny owl (Strix aluco) heritable melanin-based coloration shows different physiological and behavioral norms of reaction, we investigated whether coloration is associated with investment in maintenance and reproduction. Light melanic owls had lower adult survival compared to dark melanic conspecifics, and color variation was related to the trade-off between offspring number and quality. When we experimentally enlarged brood size, light melanic males produced more fledglings but in poorer condition, and they were less often recruited in the local breeding population than those of darker melanic conspecifics. Our results also suggest that dark melanic males allocate a constant effort to raise their brood independently of environmental conditions, whereas lighter melanic males finely adjust reproductive effort in relation to changes in environmental conditions. Color traits can therefore be associated with life-history strategies, and stochastic environmental perturbation can temporarily favor one phenotype over others. The existence of fixed strategies implies that some phenotypes can sometimes display a "maladapted" strategy. Long-term population monitoring is therefore vital for a full understanding of how different genotypes deal with trade-offs.

Effect of urbanization on the trace element concentrations in the kidney, liver and spines of the European hedgehog (Erinaceus europaeus).

Urbanized environments may be suitable for some wild species, like the European hedgehog (Erinaceus europaeus). However, the (sub)urban areas are source of several pollutants, such as trace elements (TEs). The main objective of our study is to investigate the role of the European hedgehog as a potential bioindicator species for seven TEs (As, Cd, Cr, Cu, Ni, Pb, Zn) in a big urban agglomeration. We analyzed the kidney, liver and spines of 50 European hedgehogs. Moreover, we carried out geographic information system (GIS) with 31 individuals to examine the effects of human pressure (human density and urbanization) on TE concentrations in tissues. We detected the 7 TEs in all tissues. Trace elements, especially Pb and Zn, in the liver, kidney and spines seem to be influenced by human density and urbanization.

Pale and dark reddish melanic tawny owls differentially regulate the level of blood circulating POMC prohormone in relation to environmental conditions.

Knowledge of the hormonal pathway controlling genotype-specific norms of reaction would shed light on the ecological factors to which each genotype is adapted. Environmentally mediated changes in the sign and magnitude of covariations between heritable melanin-based colouration and fitness components are frequent, revealing that extreme melanin-based phenotypes can display different physiological states depending on the environment. Yet, the hormonal mechanism underlying this phenomenon is poorly understood. One novel hypothesis proposes that these covariations stem from pleiotropic effects of the melanocortin system. Melanocortins are post-translationally modified bioactive peptides derived from the POMC prohormone that are involved in melanogenesis, anti-inflammation, energy homeostasis and stress responses. Thus, differential regulation of fitness components in relation to environmental factors by pale and dark melanic individuals may be due to colour-specific regulation of the POMC prohormone. Accordingly, we found that the degree of reddish melanic colouration was negatively correlated with blood circulating levels of the POMC prohormone in female tawny owls (Strix aluco) rearing a brood for which the size was experimentally reduced, but not when enlarged, and in females located in rich but not in poor territories. Our findings support the hypothesis that the widespread links between melanin-based colouration and fitness components may be mediated, at least in part, by the melanocortin system.

Sudden weather deterioration but not brood size affects baseline corticosterone levels in nestling Alpine swifts.

While evidence is accumulating that stress-induced glucocorticoid responses help organisms to quickly adjust their physiology and behaviour to life-threatening environmental perturbations, the function and the ecological factors inducing variation in baseline glucocorticoid levels remain poorly understood. In this study we investigated the effects of brood size by experimentally manipulating the number of nestlings per brood and the effect of weather condition on baseline corticosterone levels of nestling Alpine swifts (Apus melba). We also examined the potential negative consequences of an elevation of baseline corticosterone on nestling immunity by correlating corticosterone levels with ectoparasite intensity and the antibody production towards a vaccine. Although nestlings reared in enlarged broods were in poorer condition than nestlings reared in reduced broods, they showed similar baseline corticosterone levels. In contrast, nestling baseline corticosterone levels were higher immediately after cold and rainy episodes with strong winds. Neither nestling infestation rate by ectoparastic flies nor nestling antibody production against a vaccine was correlated with baseline corticosterone levels. Thus, our results suggest that altricial Alpine swift nestlings can quickly modulate baseline corticosterone levels in response to unpredictable variations in meteorological perturbation but not to brood size which may be associated with the degree of sibling competition. Apparently, short-term elevations of baseline corticosterone have no negative effects on nestling immunocompetence.

Maternal effects and urbanization: Variation of yolk androgens and immunoglobulin in city and forest blackbirds.

Wildlife inhabiting urban environments exhibit drastic changes in morphology, physiology, and behavior. It has often been argued that these phenotypic responses could be the result of micro-evolutionary changes following the urbanization process. However, other mechanisms such as phenotypic plasticity, maternal effects, and developmental plasticity could be involved as well. To address maternal effects as potential mechanisms, we compared maternal hormone and antibody concentrations in eggs between city and forest populations of European blackbirds (Turdus merula), a widely distributed species for which previous research demonstrated differences in behavioral and physiological traits. We measured egg and yolk mass, yolk concentrations of androgens (androstenedione [A4], testosterone [T], 5α-dihydrotestosterone [5α-DHT], and immunoglobulins [IgY]) and related them to population, clutch size, laying order, embryo sex, and progress of breeding season. We show (a) earlier onset of laying in the city than forest population, but similar egg and clutch size; (b) higher overall yolk androgen concentrations in the forest than the city population (sex-dependent for T); (c) greater among-female variation of yolk T and 5α-DHT concentrations in the forest than city population, but similar within-clutch variation; (d) similar IgY concentrations with a seasonal decline in both populations; and (e) population-specific positive (city) or negative (forest) association of yolk A4 and T with IgY concentrations. Our results are consistent with the hypotheses that hormone-mediated maternal effects contribute to differences in behavioral and physiological traits between city and forest individuals and that yolk androgen and immunoglobulin levels can exhibit population-specific relationships rather than trade-off against each other.

Artificial selection reveals the role of transcriptional constraints in the maintenance of life history variation.

The trade-off between reproduction and self-maintenance is a cornerstone of life history theory, yet its proximate underpinnings are elusive. Here, we used an artificial selection approach to create replicated lines of Japanese quail (Coturnix japonica) that differ genetically in their reproductive investment. Whole transcriptome sequencing revealed that females from lines selected for high reproductive output show a consistent upregulation of genes associated with reproduction but a simultaneous downregulation of immune genes. Concordant phenotypic differences in immune function (i.e., specific antibody response against keyhole limpet hemocyanin) were observed between the selection lines, even in males who do not provide parental care. Our findings demonstrate the key role of obligate transcriptional constraints in the maintenance of life history variation. These constraints set fundamental limits to productivity and health in natural and domestic animal populations.

Pheomelanin-based coloration and the ability to cope with variation in food supply and parasitism.

Although gene by environment interactions may play a key role in the maintenance of genetic polymorphisms, little is known about the ecological factors involved in these interactions. We investigated whether food supply and parasites can mediate covariation between the degree of adult pheomelanin-based coloration, a heritable trait, and offspring body mass in the tawny owl (Strix aluco). We swapped clutches between nests to allocate genotypes randomly among environments. Three weeks after hatching, we challenged the immune system of 80 unrelated nestlings with either a phytohemagglutinin (PHA) or a lipopolysaccharide, surrogates of alternative parasites, and then fed them ad lib. or food-restricted them during the following 6 days in the laboratory. Whatever the immune challenge, nestlings fed ad lib. converted food more efficiently into body mass when their biological mother was dark pheomelanic. In contrast, food-restricted nestlings challenged with PHA lost less body mass when their biological mother was pale pheomelanic. Nestling tawny owls born from differently melanic mothers thus show differing reaction norms relative to food availability and parasitism. This suggests that dark and pale pheomelanic owls reflect alternative adaptations to food availability and parasites, factors known to vary in space and time.

Strength and cost of an induced immune response are associated with a heritable melanin-based colour trait in female tawny owls.

1. Melanin pigments provide the most widespread source of coloration in vertebrates, but the adaptive function of such traits remains poorly known. 2. In a wild population of tawny owls (Strix aluco), we investigated the relationships between plumage coloration, which varies continuously from dark to pale reddish, and the strength and cost of an induced immune response. 3. The degree of reddishness in tawny owl feather colour was positively correlated with the concentration of phaeomelanin and eumelanin pigments, and plumage coloration was highly heritable (h(2) = 0.93). No carotenoids were detected in the feathers. 4. In mothers, the degree of melanin-based coloration was associated with antibody production against a vaccine, with dark reddish females maintaining a stronger level of antibody for a longer period of time compared to pale reddish females, but at a cost in terms of greater loss of body mass. 5. A cross-fostering experiment showed that, independent of maternal coloration, foster chicks reared by vaccinated mothers were lighter than those reared by nonvaccinated mothers. Hence, even though dark reddish mothers suffered a stronger immune cost than pale reddish mothers, this asymmetric cost was not translated to offspring growth. 6. Our study suggests that different heritable melanin-based colorations are associated with alternative strategies to resist parasite attacks, with dark reddish individuals investing more resources towards the humoral immune response than lightly reddish conspecifics.

Carotenoid-based plumage colors and immune function: is there a trade-off for rare carotenoids?

Theory suggests that carotenoid-based signals are used in animal communication because they contain specific information about parasite resistance or immunocompetence. This implies that honesty of carotenoid-based signals is maintained by a trade-off between pigmentation and immune function for carotenoids, assuming that the carotenoids used for coloration are also immunoenhancing. We tested this hypothesis by altering the diets of nestling great tits (Parus major) with supplementary beadlets containing the carotenoids that are naturally ingested with food or beadlets containing the carotenoids that are incorporated into the feathers; a control group received beadlets containing no carotenoids. We simultaneously immune challenged half of the nestlings of each supplementation group, using a two-factorial design. Activation of the immune system led to reduced color expression. However, only nestlings fed with the naturally ingested carotenoids and not with the carotenoids deposited in the feathers showed an increased cellular immune response. This shows that the carotenoids used for ornamentation do not promote the immune function, which conflicts with the trade-off hypothesis. Our results indicate that honesty of carotenoid-based signals is maintained by an individual's physiological limitation to absorb and/or transport carotenoids and by access to carotenoids, indicating that preferences for carotenoid-based traits in sexual selection or parent-offspring interactions select for competitive individuals, rather than specifically for immune function.

Impact of greenspaces in city on avian species richness and abundance in Northern Africa.

Increasing urbanization is a major challenge in the context of global changes, because this environment is known to negatively impact biodiversity. It is therefore important to identify factors maintaining biodiversity in such areas. Here, we tested in 650 sites whether the greenspaces in urbanized area of Annaba (Algeria) has positive effects on avian species richness and abundances. Our results show that species detection (n=26) is more important during the breeding season as compared to the winter season, and that avian species richness is positively affected by the greenspaces. For most species, greenspaces impact positively their presence and abundances. Only the feral pigeon was less detected in greenspaces as compared to built-up areas. Our study therefore confirmed, for the first time in a Northern African city, that greenspaces significantly increase the species richness and abundances of birds, and shows that the season can profoundly affect such indicators.

Telomere erosion varies with sex and age at immune challenge but not with maternal antibodies in pigeons.

Conditions experienced early in life have profound impact on adult fitness, and telomere erosion could be a key mechanism in this process. In particular, early exposure to parasites is a frequent phenomenon in young vertebrates, which is associated with several short- and long-term costs such as telomere erosion. However, the timing of exposure to parasites during ontogeny and maternal antibodies can strongly modulate the costs of immunity, and could differentially affect telomere erosion. Here, we compared the effects of an early or late immune challenge on telomere erosion rate in male and female young feral pigeons (Columba livia) having received or not maternal antibodies. More specifically, we tested whether (i) early or late injections of antigens had different effects on nestling telomere erosion rate, (ii) whether this effect was different between male and female nestlings, and (iii) whether maternal antibodies could modulate telomere erosion rate. Our results show an interaction between sex and age at injection. Late-injected nestlings (injected at 14 days of age) had an accelerated erosion rate compared with the early-injected nestlings (injected at 3 days of age), and this effect was higher in females compared with the males. However, we did not find any effect of maternal antibodies on telomere erosion rate. These results suggest that the age at which an immune challenge occurs is important for telomere erosion and that sex-specific approaches are needed to better understand the short-term and long-term costs of parasite exposure in young vertebrates.

Melanin-based coloration is a nondirectionally selected sex-specific signal of offspring development in the alpine swift.

Two mutually exclusive hypotheses have been put forward to explain the evolution and adaptive function of melanin-based color traits. According to sexual selection theory melanism is a directionally selected signal of individual quality, whereas theory on the maintenance of genetic polymorphism proposes that alternative melanin-based variants achieve equal fitness. Alpine swift (Apus melba) males and females have a conspicuous patch of white feathers on the breast with their rachis varying continuously from white to black, and hence the breast varies from white to striated. If this trait is a sexually selected signal of quality, its expression should be condition dependent and the degree of melanism directionally selected. If variation in melanism is a polymorphism, its expression should be genetically determined and fitness of melanin-based variants equal. We experimentally tested these predictions by exchanging eggs or hatchlings between randomly chosen nests and by estimating survival and reproduction in relation to melanism. We found that breast melanism is heritable and that the environment and body condition do not significantly influence its expression. Between 5 and 50 days of age nestlings were heavier and their wings longer when breast feathers of their biological father were blacker, and they also fledged at a younger age. This shows that aspects of offspring quality covary positively with the degree of melanism. However, this did not result in directional selection because nestling survival and recruitment in the local breeding population were not associated with father breast melanism. Furthermore, adult survival, age at first reproduction and probability of skipping reproduction did not covary with the degree of melanism. Genetic variation in breast melanism is therefore maintained either because nonmelanic males achieve fitness similar to melanic males via a different route than producing fast-growing offspring, or because the advantage of producing fast-growing offspring is not sufficiently pronounced to result in directional selection.

Kittiwakes strategically reduce investment in replacement clutches.

Many life-history traits are expressed interactively in life, but to a varying extent on different occasions. Changes in trait expression can be accounted for by differences in the quality of the environment ('environmental constraint' hypothesis) or by strategic adjustments, if the relative contribution of the trait to fitness varies with time ('strategic allocation' hypothesis). In birds, egg production is lower in replacement clutches than in first clutches, but it is unknown whether this reduction results from an environmental constraint (e.g. food being less available at the time when the replacement clutch is produced) or from a strategic allocation of resources between the two breeding attempts. To distinguish between these two hypotheses, we performed an experiment with black-legged kittiwakes (Rissa tridactyla). Pairs were either food-supplemented or not before the first clutch was laid onwards and we induced them to produce a replacement clutch by removing eggs once when the first clutch was complete. As predicted by the 'strategic allocation' hypothesis, egg production of food-supplemented and non-food-supplemented birds decreased between first and replacement clutches. This suggests that kittiwakes strategically reduce investment in egg production for their replacement clutches compared to first clutches.

Food availability and maternal immunization affect transfer and persistence of maternal antibodies in nestling pigeons.

The ability of mothers to transfer antibodies (Abs) to their young and the temporal persistence of maternal Abs in offspring constitute important life-history traits that can impact the evolution of host-parasite interactions. Here, we examined the effects of food availability and parental immunization on the transfer and persistence of maternal antibodies in nestling pigeons (Columba livia). This species can transmit maternal Abs to offspring before hatching through the egg yolk and potentially after hatching through crop milk. However, the role of this postnatal substance in immunity remains elusive. We used a full cross-fostering design to disentangle the effects of food limitation and parental immunization both before and after hatching on the levels and persistence of maternal Abs in chicks. Parents were immunized via injection with keyhole limpet hemocyanin antigens. Using an immunoassay that specifically detected the IgY antibodies that are known to be transmitted via the yolk, we found that the levels of anti-KLH Abs in newly hatched chicks were positively correlated with the levels of anti-KLH Abs in the blood of their biological mothers. However, this correlation was not present between chicks and their foster parents, suggesting limited IgY transfer via crop milk to the chick's bloodstream. Interestingly, biological mothers subjected to food limitation during egg laying transferred significantly fewer specific maternal Abs, which suggests that the transfer of antibodies might be costly for them. In addition, the persistence of maternal Abs in a chick's bloodstream was not affected by food limitation or the foster parents' anti-KLH Ab levels; it was only affected by the initial level of maternal anti-KLH Abs that were present in newly hatched chicks. These results suggest that the maternal transfer of Abs could be costly but that their persistence in an offspring's bloodstream may not necessarily be affected by environmental conditions.

Color differences among feral pigeons (Columba livia) are not attributable to sequence variation in the coding region of the melanocortin-1 receptor gene (MC1R).

BACKGROUND: Genetic variation at the melanocortin-1 receptor (MC1R) gene is correlated with melanin color variation in many birds. Feral pigeons (Columba livia) show two major melanin-based colorations: a red coloration due to pheomelanic pigment and a black coloration due to eumelanic pigment. Furthermore, within each color type, feral pigeons display continuous variation in the amount of melanin pigment present in the feathers, with individuals varying from pure white to a full dark melanic color. Coloration is highly heritable and it has been suggested that it is under natural or sexual selection, or both. Our objective was to investigate whether MC1R allelic variants are associated with plumage color in feral pigeons. FINDINGS: We sequenced 888 bp of the coding sequence of MC1R among pigeons varying both in the type, eumelanin or pheomelanin, and the amount of melanin in their feathers. We detected 10 non-synonymous substitutions and 2 synonymous substitution but none of them were associated with a plumage type. It remains possible that non-synonymous substitutions that influence coloration are present in the short MC1R fragment that we did not sequence but this seems unlikely because we analyzed the entire functionally important region of the gene. CONCLUSIONS: Our results show that color differences among feral pigeons are probably not attributable to amino acid variation at the MC1R locus. Therefore, variation in regulatory regions of MC1R or variation in other genes may be responsible for the color polymorphism of feral pigeons.