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Influence of persistent organic pollutants on the endocrine stress response in free-living and captive red kites (Milvus milvus)
Abstract
Persistent organic pollutants (POPs) have the potential to impair the endocrine regulation of organisms and alter their ability to respond to environmental changes. We studied whether polychlorinated biphenyls
(PCBs) and organochlorine pesticides (OCPs) affected the endocrine regulation of free-living and captive red kites (Milvus milvus) through studying the dynamics of corticosterone (CORT) and dehydroepiandrosterone (DHEA). We sampled migratory free-living kites coming from northern Europe and captive kites born in a rehabilitation center in Spain. We used body feathers from the interscapular region as a minimally-invasive and integrative matrix. The most abundant compound detected in freeliving kites was 4,40-dichlorodiphenyldichloroethylene (4,40-DDE; 6.10 ± 1.56 ng g-1 dw feather) followed by CB-153 (3.10 ± 0.63 ng g-1 dw feather) and CB-180 (2.43 ± 1.08 ng g-1 dw feather). In captive kites, the most abundant compounds were 4,40-dichlorodyphenyltrichloroethane (4,40-DDT; 2.38 ± 1.30 ng g-1 dw feather), CB-153 (2.15 ± 0.47 ng g-1 dw feather) and hexachlorobenzene (HCB; 2.03 ± 0.45 ng g-1 dw feather) at similar concentrations. Free-living kites showed higher levels of 4,40-DDE and CB-180 in comparison to captive kites. Age influenced HCB and CB-101 levels, whereas body mass was inversely related to CB-180 and 4,40-DDT. Interestingly, captive kites showed a ratio DDT/DDE higher than 1 suggesting a relatively recent exposure of DDT, in contrast to free-living kites. Regarding hormonal levels, free-living kites showed higher levels of CORT (3.30 ± 0.22 pg mm-1 feather) than captive (2.40 ± 0.16 pg mm-1 feather), reflecting higher allostatic load. In addition, a positive association between PCBs and DDTs and adrenal hormones was found in free-living kites, suggesting an increase of CORT as a response of the endocrine system to cope with stressors and a subsequent elevation of DHEA to ameliorate the potential negative effects that high CORT levels could cause to the organism.
... An advantage of CORTf measurement is the storage of feathers. Because feathers are a stable matrix, except of storing them dry and clean, there they require no further treatment [3,[16][17][18][19]. This enables longer storage, and thus, e.g., samples of rare species or wild birds can be collected when the opportunity arises and analyzed at a later time if needed. ...
... The localization was perfect for fast and safe sampling and had no impact on the bird's flight ability. This sampling region has already been used in other research projects [19,27,28]. An additional point in favor of the alternative cutting technique is that in the process of CORTf determination, the calamus of the feather is first cut off before the feather is analyzed in more detail (e.g., measurement of length and weight) [11,16,28,29]. ...
... Therefore, we think that feathers from the region between the shoulders are better suited, even if the standardization may be slightly impaired. This region has already been selected for CORTf measurements in Greater Flamingos [27], Broilers (Gallus gallus domesticus) [28], Red Kites (Milvus milvus) [19], Domestic Geese and Mulard Ducks [20]. ...
This research project had the aim to validate the possible alternative and less-painful sampling method of cutting feathers close to the skin instead of plucking them for subsequent feather corticosterone analysis, confirming recently-published results for other species in captivity. Analyzing CORTf is often used in animal welfare studies in combination with behavioral monitoring. The background of this idea was to act in the sense of animal welfare and reduce the burden of animal studies according to the 3-R-Principle (Replacement, Reduction, and Refinement) by refining procedures. To confirm the hypothesis that the sampling method itself has no influence on CORTf levels measured, plucked and cut samples of the respective bird were collected. Birds of two wild species were used: the Mallard (Anas platyrhynchos) and the Greater Flamingo (Phoenicopterus roseus). The CORTf was measured by using an enzyme-linked immunosorbent assay (ELISA). The determined values were inspected for their mean values, standard deviation (SD), and average differences. Afterwards, the CORTf levels of both species were compared, according to the sampling method, with the concordance correlation coefficient (CCC). In the Bland-Altman (BA) plot the differences of the methods were displayed against the mean values. Additionally, sex, as a possible factor influencing CORTf, was analyzed using the Mann-Whitney U test. The values of CCC showed poor agreement in the comparability of the two methods, whereas the concordance of the BA plot was decent. The average differences between the methods were marginal for both species (Mallards: −0.16 pg/mm, Flamingos −0.13 pg/mm). In summary, all anomalies or differences between the methods were negligible. Therefore, the alternative sampling method seems to be as suitable as the common standard method. No significant difference was found between females and males. Nevertheless, our results suggest that CORTf should not be interpreted in just considering the values themselves, but the results they should be analyzed in the context of a wider set of parameters. Hence, further studies are encouraged to create a larger data pool.
... Highly contaminated individuals show, for example, decreased breeding capacities, which could be abnormal breeding behaviour, reduced fertility, or low breeding success (Bustnes et al. 2007;Tartu et al. 2014). Besides, POPs have been proven to influence the stress-response (corticosterone level) in free-living Red kites (Milvus milvus; Monclús et al. 2018a), suggesting that these compounds have the potential to impair the endocrine regulation of organisms and alter their ability to respond to environmental changes. Several studies have shown that POPs may be responsible for the decline of some wildlife populations (Fyfe et al. 1988;Naso et al. 2003;Gómara et al. 2008;Sonne et al. 2020). ...
... Particularly, in zoo and cattle rearing populations p,p′-DDE accounted for 100% of the total DDT average concentrations. The high dominance of this metabolite has already been observed in feathers of other species such as passerines from Belgium (Dauwe et al. 2005), seabirds from Argentina (Adrogué et al. 2019), and raptors from Spain and Brazil (Gómara et al. 2008;Monclús et al. 2018a;Aver et al. 2020). On the other hand, p,p′-DDD was the more abundant metabolite (more than 75%) in farm and agriculture populations. ...
... One experimental study has reported that concentrations of 4.80 μg g −1 of ΣDDTs (DDT, DDD, and DDE) in feathers of white pelican (Pelecanus erythrorhynchos) nestlings showed sublethal effects on the levels of vitamin A in the liver and levels of potassium, calcium, and protein in serum (Greichus et al. 1975). Monclús et al. (2018a) studied the influence of POPs on the endocrine stress response in Red kites (Milvus milvus) and showed that higher POP concentrations could act as endocrine disruptors and affect the functioning of the hypothalamic pituitary adrenal axis. The authors found a positive correlation between PCBs and DDTs and adrenal hormones. ...
Persistent organic pollutants (POPs) are still globally distributed and can exert different effects on ecosystems. Little is known about the occurrence of these contaminants in terrestrial birds from South America. In this study, POPs were assessed for the first time in a flightless herbivorous species from the Pampas grasslands, the Greater rhea (Rhea americana). Concentrations of polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), and organochlorine pesticides (OCPs) were determined in 18 samples of feathers from free-ranging and captive individuals inhabiting four sites with different land uses in central Argentina. Among the 16 POPs tested in those feathers, 6 PCBs (28, 52, 101, 138, 153, and 180) and 8 OCPs (α-HCH, β-HCH, γ-HCH, p,p′-DDE, p,p′-DDD, o,p′-DDT, p,p′-DDT, and HCB) were quantified. No PBDEs were detected. The total concentration of POPs was higher in populations living in an intensive crop production area (agriculture 159 ng g ⁻¹ and farm: 97.53 ng g⁻¹) compared with the population in an urban area (zoo 45.86 ng g⁻¹) and an agroecosystem with extensive rearing of livestock (cattle rearing 36.77 ng g⁻¹). PCBs were the most abundant pollutants in all the populations studied. Lower chlorinated CB 52 and CB 101 were the principal PCB congeners detected, representing at least 70% of the total quantified. All populations studied showed a DDE + DDD/DDT ratio > 1, indicating a historical application of this insecticide. This study provides a new contribution to the scarce data on POP concentrations in South American bird species. Further investigations are needed to evaluate their potential effects on the health of individuals and populations.
... HCB is less persistent and more volatile than other OCPs in the environment (Wania et al., 1996). Therefore, the presence in feathers could reflect a recent exposure to the pollutant or exogenous contamination from atmospheric sources or uropigial gland secretions (Dauwe et al., 2005;Monclús et al., 2018a). Ramos et al. (2017) suggested that the NW region of Spain was one of the most HCB polluted area possibly due to industrial source emissions. ...
... Ramos et al. (2017) suggested that the NW region of Spain was one of the most HCB polluted area possibly due to industrial source emissions. HCB was also one of the main OCP contributors in feathers of captive red kites (Milvus milvus) in NE Spain (Monclús et al., 2018a) showing similar concentration than ours. Briels et al. (2019) showed that OCP concentrations were the dominant POPs in feathers of Northern goshawk (Accipiter gentilis) nestlings from two sites of Norway (range 5.7e183 ng/g). ...
... Behrooz et al. (2009) showed in collared dove from Iran, levels of 8.0 ng/g for PCB markers from tail feathers with PCB 138 and 180 as the major contributors. Monclús et al. (2019Monclús et al. ( , 2018a showed PCB concentrations in cinereous vulture (Aegypius monachus) of 3.0 ± 0.20 ng/g in down feathers and in free-living red kite concentrations of 9.1 ± 2.6 ng/g in interscapular feathers. In contrast, Acampora et al. (2018) and Arikan et al. (2018) found high PCB level concentrations in common tern breast feathers from Ireland and in spur-winged lapwing (Vanellus spinosus) tail feathers from Turkey (27 ng/g ww and 54 ng/g, repectively). ...
A large portion of organic pollutants (OPs) represent a potential hazard to humans and living beings due to their toxic properties. For several years, birds have been used as biomonitor species of environmental pollution. Polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs), polybrominated biphenyl ethers (PBDEs), organophosphate pesticides (OPPs), polycyclic aromatic hydrocarbons (PAHs) and py-rethroids (PYRs) were assessed in body feather samples of 71 feral pigeons (Columba livia domestica) collected from Asturias and Galicia (NW Spain). The percentage of detection for all chemical groups were above 90% in studied birds. The general pattern was dominated by PAHs (mean value ± standard deviation (SD) 32 ± 15 ng/g) followed by OCPs (3.8 ± 1.1 ng/g), PYRs (3.4 ± 3.8 ng/g), PCBs (1.6 ± 1.0 ng/g), OPPs (1.3 ± 0.70 ng/g) and PBDEs (0.80 ± 0.30 ng/g). Significant differences were observed between age, location and gender suggesting different sources of exposure and accumulation pathways.
... We hypothesised negative relationships between OHCs and thyroid hormones, indicating possible thyroid disruption (McNabb, 2007), and positive relationships between OHCs and CORT f , as individuals with high OHC burdens may experience more stress (Monclús et al., 2019(Monclús et al., , 2018. Positive relationships were also hypothesised between OHCs and selected BCCPs, implying potential OHC-induced perturbations in hepatic and renal function (Sonne et al., 2012(Sonne et al., , 2010. ...
... The corticosterone concentrations in the feathers (Table 1) were in the same range as those found in feathers of common buzzard (Buteo buteo, Martínez-Padilla et al., 2013) and red kite (Milvus milvus) nestlings (Monclús et al., 2018). These concentrations may indicate that the nestlings did not experience chronic stress during their time in the nests, as they are not particularly high compared to concentrations previously reported in feathers of birds of prey (López-Jiménez et al., 2017). ...
... However, corticosterone measured in feathers and plasma should not be directly compared as they present different time points (Bortolotti, 2008), even though studies have found significant correlations between the two matrices (Fairhurst et al., 2013). Previous studies have reported positive correlations between legacy OHCs and corticosterone concentrations measured in feathers (Monclús et al., 2019(Monclús et al., , 2018 and plasma of birds (Bowerman et al., 2002;Nordstad et al., 2012;Verboven et al., 2010). However, a lack of correlations has also been reported between legacy OHCs and corticosterone in both feathers and plasma (Bourgeon et al., 2012;Tartu et al., 2014a). ...
Environmental exposure to organohalogenated contaminants (OHCs), even at low concentrations, may cause detrimental effects on the development and health of wild birds. The present study investigated if environmental exposure to OHCs may influence the variation of multiple physiological parameters in Norwegian white-tailed eagle (Haliaeetus albicilla) nestlings. Plasma and feather samples were obtained from 70 nestlings at two archipelagos in Norway in 2015 and 2016. The selected physiological parameters were plasma concentrations of thyroid hormones (thyroxine, T4 and triiodothyronine, T3), plasma proteins (prealbumin, albumin, α1-, α2-, β- and γ-globulins) and selected blood clinical chemical parameters (BCCPs) associated with liver and kidney functioning. Feather concentrations of corticosterone (CORTf) were also included to investigate the overall stress level of the nestlings. Concentrations of all studied physiological parameters were within the ranges of those found in other species of free-living birds of prey nestlings and indicated that the white-tailed eagle nestlings were of good health. Our statistical models indicated that perfluoroalkyl substances (PFASs) and legacy OHCs, such as polychlorinated biphenyls, organochlorinated pesticides and polybrominated diphenyl ethers, influenced only a minor fraction of the variation of plasma thyroid hormones, prealbumin and CORTf (5–15%), and partly explained the selected BCCPs (<26%). Most of the variation in each studied physiological parameter was explained by variation between nests, which is most likely due to natural physiological variation of nestlings in these nests. This indicates the importance of accounting for between nest variation in future studies. In the present nestlings, OHC concentrations were relatively low and seem to have played a secondary role compared to natural variation concerning the variation of physiological parameters. However, our study also indicates a potential for OHC-induced effects on thyroid hormones, CORTf, prealbumin and BCCPs, which could be of concern in birds exposed to higher OHC concentrations than the present white-tailed eagle nestlings.
... 4 Several studies have illustrated that specific POPs can interact with the endocrine system of birds, i.e. the thyroid system (Cesh et al., 2010;Fernie and Marteinson, 2016;Nøst et al., 2012;Rogstad et al., 2017;Van den Steen et al., 2010) and the sex steroids (Nossen et al., 2016;Rogstad et al., 2017;Van den Steen et al., 2010;Verboven et al., 2008). Less research has been done regarding the effects of POPs on the hypothalamic-pituitary-adrenal (HPA) axis and mixed results have been published [e.g., Tartu et al., 2014Tartu et al., , 2015Monclús et al., 2018b; but also Love et al., 2003 (summarized in Table A1 in Appendices)]; probably because of the different matrixes used and the different species and field/lab conditions tested. The HPA axis is one of the most important regulatory pathways to deal with stressors by releasing corticosterone (CORT) into bloodstream (Romero, 2004;Sapolsky, 2000). ...
... 17 more recent study (Monclús et al., 2018b) has observed that high POP levels may not solely be positively correlated to high CORT levels but also to increasing levels of dehydroepiandrostendione (DHEA), a protective adrenal hormone with "anti-CORT" ...
... Surprisingly, the effect was not negative and males with high concentrations of PC1-POPs showed a shorter period of chick development and not longer, as it would be expected if the concentrations of POPs were high enough to cause negative consequences on the growth of the chicks. Overall, these findings may indicate a compensatory response of the chicks rather than a means of chronic stress (see Dickens and Romero, 2013), in agreement with the previous findings of Monclús et al. (2018b). ...
Persistent organic pollutants (POPs) are still globally distributed and some have been shown to interact with the endocrine system of birds. However, the relationship between POPs and the stress response mediated by the hypothalamic-pituitary-adrenal (HPA) axis is still poorly understood. Raising concerns are now focused on the toxic properties of emergent organophosphate ester flame retardants (OPEs), but whether OPEs interact with the HPA axis response has not yet been investigated. We measured corticosterone concentrations in feathers (CORTf) as a long-term biomarker of the bird HPA axis response and we investigated their relationship with POP and OPE concentrations in down feathers of nestling cinereous vultures (Aegypius monachus). We also examined whether high contaminant burden and high CORTf concentrations impacted the duration of chick development. The most predominant compounds were the following: p,p'-DDE (3.28 ± 0.26 ng g-1 dw) > γ-HCH (0.78 ± 0.09 ng g-1 dw) > BDE-99 (0.73 ± 0.09 ng g-1 dw) > CB-153 (0.67 ± 0.04 ng g-1 dw). The most persistent POP compounds (CB-170, -177, -180, -183, -187, -194 and p,p'-DDE) were associated (P = 0.02) with high concentrations of CORTf (range: 0.55-6.09 pg mm-1), while no relationship was found when OPEs were tested (P > 0.05). Later egg-laying was positively associated to high levels of CORTf (P = 0.02) and reduced duration of chick development (P < 0.001), suggesting a beneficial effect of the HPA axis response on the growth of the chicks. In addition, males with high concentrations of the most persistent POP compounds tended to show a reduced duration of the nestling period (P = 0.05) and an equal fledging success than chicks with lower levels. These findings suggest that POPs, but not OPEs, may interact with the HPA axis response of chicks, although levels were not high enough to cause detrimental consequences.
... The plethora of sampling procedures (mainly determined by the accessibility and biology of the investigated species) and methodological approaches available to researchers may contribute to discrepancies among studies. Similar to our study, Randulff et al. (2022) found no associations between fCORT and POP levels in Norwegian goshawk (Accipiter gentilis) nestlings, while two studies on red kites and cinereous vultures (Aegypius monachus) both reported positive relationships between fCORT and POP concentrations (Monclus et al. (2018) and Monclus et al. (2019), respectively). In contrast, Loseth et al. (2019) reported that fCORT decreased with increasing levels of perfluoralkyl substances (PFAS) in the Norwegian WTE nestlings although ranges in PFAS and fCORT levels encompassed different study locations. ...
... As such, spatial variations in fCORT are more likely to be driven by heterogenous environmental conditions among locations/populations rather than pollutant exposure per se. Although anthropogenic pollutants have been proposed as a chronic stressor in wildlife (Ganz et al., 2018), findings in the current and above-mentioned studies by Loseth et al. (2019), Monclus et al. (2018Monclus et al. ( , 2019, and Randulff et al. (2022) do not support that POPs influence CORT physiology. In addition, studies investigating other pollutants such as toxic metals (Strong et al., 2015) and other matrices (blood: e.g., Tartu et al. (2015a)) also reported contradicting findings on the CORT-contaminant relationship, further emphasizing the complexity behind establishing CORT as a proximal mechanism underlying the effects of contaminant exposure in avian wildlife. ...
Exposure to persistent organic pollutants (POPs), such as organochlorines (OCs) and polybrominated diphenyl ethers (PBDEs), is associated with adverse health effects in wildlife. Many POPs have been banned and consequently their environmental concentrations have declined. To assess both temporal trends of POPs and their detrimental impacts, raptors are extensively used as biomonitors due to their high food web position and high contaminant levels. White-tailed eagles (WTEs; Haliaeetus albicilla) in the Baltic ecosystem represent a sentinel species of environmental pollution, as they have suffered population declines due to reproductive failure caused by severe exposure to dichlorodiphenyltrichloroethane (DDT) and polychlorinated biphenyls (PCB) during the 1960s through 1980s. However, there is a lack of long-term studies that cover a wide range of environmental contaminants and their effects at the individual level. In this study, we used 135 pooled samples of shed body feathers collected in 1968-2012 from breeding WTE pairs in Sweden. Feathers constitute a temporal archive for substances incorporated into the feather during growth, including corticosterone, which is the primary avian glucocorticoid and a stress-associated hormone. Here, we analysed the WTE feather pools to investigate annual variations in feather corticosterone (fCORT), POPs (OCs and PBDEs), and stable carbon and nitrogen isotopes (SIs; dietary proxies). We examined whether the expected fluctuations in POPs affected fCORT (8-94 pg. mm-1) in the WTE pairs. Despite clear temporal declining trends in POP concentrations (p < 0.01), we found no significant associations between fCORT and POPs or SIs (p > 0.05 in all cases). Our results do not support fCORT as a relevant biomarker of contaminant-mediated effects in WTEs despite studying a highly contaminated population. However, although not detecting a relationship between fCORT, POP contamination and diet, fCORT represents a non-destructive and retrospective assessment of long-term stress physiology in wild raptors otherwise not readily available.
... Corticosterone DHEA • Free-living kites had higher levels of corticosterone than captive birds, indicating a higher AL [74] No ...
... There were common themes amongst the 63 publications, including a focus on environmental challenges, social structure, and animals under managed care. Evaluating AL in the context of environmental challenges was a focus of several publications and encompassed different focus areas including the impacts of human activities (i.e., agriculture [51], urbanization [102], snow sports [14], and pollution [74]), and characterization of the effects of environmental parameters on AL (i.e., weather [70], fire [79], and salinity [47]). Several publications investigated the effects of social structure on AL in several species including hyena [100], Assamese macaques [75], bearded capuchins [81], cichlids [60], and rainbow trout [52]. ...
Principles of allostasis and allostatic load have been widely applied in human research to assess the impacts of chronic stress on physiological dysregulation. Over the last few decades, researchers have also applied these concepts to non-human animals. However, there is a lack of uniformity in how the concept of allostasis is described and assessed in animals. The objectives of this review were to: 1) describe the extent to which the concepts of allostasis and allostatic load are applied theoretically to animals, with a focus on which taxa and species are represented; 2) identify when direct assessments of allostasis or allostatic load are made, which species and contexts are represented, what biomarkers are used, and if an allostatic load index was constructed; and 3) detect gaps in the literature and identify areas for future research. A search was conducted using CABI, PubMed, Agricola, and BIOSIS databases, in addition to a complementary hand-search of 14 peer-reviewed journals. Search results were screened, and articles that included non-human animals, as well as the terms “allostasis” or “allostatic” in the full text, were included. A total of 572 articles met the inclusion criteria (108 reviews and 464 peer-reviewed original research). Species were represented across all taxa. A subset of 63 publications made direct assessments of allostatic load. Glucocorticoids were the most commonly used biomarker, and were the only biomarker measured in 25 publications. Only six of 63 publications (9.5%) constructed an allostatic load index, which is the preferred methodology in human research. Although concepts of allostasis and allostatic load are being applied broadly across animal species, most publications use single biomarkers that are more likely indicative of short-term rather than chronic stress. Researchers are encouraged to adopt methodologies used in human research, including the construction of species-specific allostatic load indexes.
... Frecuentan basureros, mataderos o zonas donde puedan encontrar carroña y otros restos orgánicos (Seoane et al., 2003;Madroño et al., 2004;De Pablo, 2015). Estos hábitos carroñeros, junto con su comportamiento semicolonial, son un grave problema para la conservación de la especie, como consecuencia de los venenos que se pueden encontrar en estas fuentes de alimentación (Monclús et al., 2018). ...
... las diferentes especies. La variabilidad intraespecífica que se aprecia en la invernada del milano real puede responder a los mismos motivos (variación geográfica y distinta disponibilidad de recursos), a los que se podría añadir otros, como las reservas grasas del individuo, la eficiencia en la caza, la cercanía a núcleos de alimentación como vertederos o el estado fisiológico del individuo, especialmente cuando están infectados por parásitos (Marucci et al.,2021) o afectados por contaminantes (Monclús et al.,2018). ...
138 red kites (Milvus milvus) were tagged with GPS/satellite transmitters between
2009 and 2020 in different locations within the distribution area of the species in
Spain. This work was the result of a high tagging effort over more than a decade.
Hundreds of thousands of locations have been recorded, which allowed to understand
the spatial and migratory behavior of this population. The individuals have
been analyzed at different stages of their life (reproduction, post-reproduction,
wintering, migration and juvenile dispersal), both of the breeding and wintering
population, highlighting their high behavioural variability and the many factors on
which it depends.
... They frequent garbage dumps, slaughterhouses or areas where they can find carrion and other organic remains [19,20]. These scavenging habits, together with their semi-colonial behaviour, are a serious problem for the conservation of the species as a consequence of the poisons that can be found in these food sources [21]. ...
... This intraspecific variability may be explained by the possibility of expanding or restricting the range area depending on the availability of food and resources, as well as by the geographical and biological characteristics of the territory selected by the individual. Furthermore, the changes could also be due to the physiological state of the individual, especially when they are infected by parasites [43] or affected by pollutants [21]. Interspecific differences, on the other hand, may also be due to the particularities of the territory selected by the species during wintering and, above all, its biological capabilities and ecological requirements (amount of food required, fat storage capacity, feeding efficiency, etc.) [2]. ...
To develop effective conservation strategies for migratory birds, it is essential to understand the ecology of a species at each biological phase, including its wintering (or non-breeding) season. For the red kite (Milvus milvus), an endangered raptor from the Western Palearctic, its wintering ecology is little known. We tagged 44 red kites using GPS/satellite transmitters to study their non-breeding seasons in Spain. Two spatial strategies were recorded: 34 individuals (77%) spent all their wintering periods in only one area, whilst the remaining individuals (23%) moved between two main areas at least once. This strategy, however, was not consistent over the years. In the latter case, the distance between wintering areas was 311.6 ± 134.7 km, and individuals usually spent equally long periods in each area (96 ± 35 days). No effects of age or sex were found on these area shifts, so they may have been driven by food or habitat resource availability. We also found high interindividual variability in home range sizes. The home ranges of adults were two-to three-times smaller than those of immatures, probably due to a better knowledge of the territory.
... Lead and organochlorine exposures have been associated with both transient and permanent alterations to the hypothalamic-pituitary-adrenal (HPA) axis, responsible for regulating the release of GCs in response to stress (Cory-Slechta et al., 2008;Tartu et al., 2014;White et al., 2007). Lead or organochlorine-induced HPA axis alterations can result in increased or suppressed baseline circulating GC concentrations (Monclús et al., 2018;Rossi-George et al., 2009) or inappropriately high responses to stressors (Baos et al., 2006;Tartu et al., 2015). Decreased survival and fitness have been documented in several avian species when circulating levels of GCs are present at inappropriate concentrations (Ellenberg et al., 2007;Owen et al., 2012;Schoenle et al., 2017). ...
... Contaminants found in condors and their marine mammal food sources, such as DDE (a major metabolite of the chlorinated pesticide DDT), PCBs, polybrominated diphenyl ethers, and mercury have been documented to have endocrine-disrupting effects in vertebrates (Chen et al., 2017;Herring et al., 2018Herring et al., , 2012Hoffmann and Kloas, 2016;Monclús et al., 2018;von Hippel et al., 2018). PCBs were frequently associated with altered GC release in seabirds but there is a significant degree of variation in effect observed by species and by sex, with some species even experiencing attenuated GC release in response to stress (Tartu et al., 2015). ...
Wild California condors (Gymnogyps californianus) are frequently exposed to lead via lead-based ammunition ingestion, and recent studies indicate significant exposure to organochlorines (e.g. dichlorodiphenyldichloroethylene (DDE) and polychlorinated biphenyls (PCBs)) for condors feeding on beach-cast marine mammals. We investigated the influence of contaminant exposure on condor glucocorticoid response through comparisons between wild and captive populations and identified modifiers of glucocorticoid release. We assessed the glucocorticoid response to routine trapping and handling events through measurement of plasma corticosterone and urate glucocorticoid metabolites (GCM). Comparison of peak urate GCM levels showed wild condors exhibited higher responses to handling-associated stressors (2250 ± 1440 ng/g dry wt, average +/- SD, n=27) than captive condors (907 ± 489 ng/g dry wt., n=6, U = 28, p = 0.003). Multiple linear regression models and an information theoretic approach (AICc) identified several extrinsic variables (e.g., time captive in flight pen before sample collection) that were negatively associated with plasma corticosterone and urate GCM levels in wild condors, which explained ∼25% of glucocorticoid variation. When accounting for these extrinsic variables we found that behavioral variables associated with increased lead and organochlorine exposure risk were positively associated with GCM levels, explaining an additional 15% of glucocorticoid variation among wild condors. Days absent from management area, a variable associated reduced survival attributed to increased lead exposure risk, had a positive influence on plasma corticosterone levels (β = 53 ± 20 SE) and peak urate GCM levels (β = 1090 ± 586 SE). Years observed feeding on marine mammals, a variable positively associated with DDE and PCB exposure, positively influenced peak urate GCM (β = 1100 ± 520 SE) and the magnitude of GCM response (peak GCM – 1st urate GCM) (β = 1050 ± 500 SE). Our findings suggest that individual propensities for these higher risk foraging behaviors predict higher stress-induced glucocorticoid levels in wild condors, and that accounting for variables associated with trapping and handling is essential for assessing the impact of environmental stressors such as contaminants on the condor stress response. As an abnormal glucocorticoid response to stress is associated with reduced reproduction and survival in vertebrates, this work indicates the critical need for further investigations into the physiological impacts of sub-lethal contaminant exposures in scavenging species worldwide.
... Measuring CORT concentrations in feathers (CORTf) is a rather new but increasingly used method in the field of stress research in birds [31]. Compared to the conventional measurement of plasma CORT, the assessment of CORTf has some advantages: (1) it is minimally or even noninvasive-feathers can be plucked both from live [32][33][34] or dead birds [35] or even collected from molting individuals without capturing them [31]; (2) it enables a retrospective, integrated measure of HPA-axis activity for the time period of feather growth and cannot be distorted by capture as long as feather growth is finished at the time of collection [35]; and (3) feathers are a stable matrix that apart from being stored dry and clean do not require additional storage conditions or processing [31,[36][37][38][39]. These advantages are especially useful in wild animals and in field work when (repeated) access to birds is difficult and equipment is limited. ...
... Greater Flamingos under one year of age were excluded. Feathers were plucked from the interscapular region of each individual [39,58] and stored dry and in the dark in labeled paper envelopes. ...
Deflighting zoo birds is a practice that receives increasing criticism due to its presumed incompatibility with animal welfare. To our knowledge, this is the first approach to address this problem in a scientific way. To do this, we compared feather corticosterone (CORTf) from Greater Flamingos (Phoenicopterus roseus, n = 151) of different flight status (i.e., pinioned, feather clipped, airworthy) from twelve different zoological institutions. To complement the hormone measurements, behavioral observations (scan samplings) were conducted prior to feather sampling within the presumed time frame of feather growth. We hypothesized that CORTf of the deflighted flamingos would differ from CORTf of their airworthy conspecifics. No significant difference in CORTf was found between the three groups, and our hypothesis was rejected. However, the impact of the institution itself (i.e., the housing conditions) proved to be the most dominant variable (variance between the institutions = 53.82%). Due to high variability, the behavioral observations were evaluated descriptively but did not give rise to doubt the findings in CORTf. Therefore, we assume that the method of flight restraint of Greater Flamingos does not have a measurable effect on CORTf. We consider this model for evaluating animal welfare of zoo birds a useful tool and provide ideas for further adjustments for consecutive studies.
... Poisoning by pollutants in the red kite has been widely studied, is considered one of the biggest threats to the conservation of this species (Viñuela et al. 2021). Many studies demonstrated intoxication after feeding on middens (Viñuela 1999;Monclús et al. 2018). However, there are not many reports of poisoning near landfills, except for one individual found in Spain (Herrero-Villar et al. 2021). ...
... Third, pesticides may alter endocrine glands and, thus, hormonal secretions. For instance, corticosterone (stress hormone) levels are linked to DDT exposure in red kites (Monclús et al., 2018). Thyroid gland secretions (measured as triiodothyronine/ T3 and/or thyroxin/T4) are perturbed (increased or decreased, depending on the species), as are the thyroid itself and androgen hormones following exposure to DDT, imidacloprid and/or mancozeb. ...
For decades, we have observed a major biodiversity crisis impacting all taxa. Avian spe- cies have been particularly well monitored over the long term, documenting their declines. In particular, farmland birds are decreasing worldwide, but the contribution of pesticides to their decline remains controversial. Most studies addressing the effects of agrochemicals are limited to their assessment under controlled laboratory conditions, the determination of lethal dose 50 (LD50) values and testing in a few species, most belonging to Galliformes. They often ignore the high interspecies variability in sensitivity, delayed sublethal effects on the physiology, behaviour and life-history traits of individuals and their con- sequences at the population and community levels. Most importantly, they have entirely neglected to test for the multiple exposure pathways to which individu- als are subjected in the field (cocktail effects). The present review aims to provide a comprehensive over- view for ecologists, evolutionary ecologists and con- servationists. We aimed to compile the literature on the effects of pesticides on bird physiology, behaviour and life-history traits, collecting evidence from model and wild species and from field and lab experiments to highlight the gaps that remain to be filled. We show how subtle nonlethal exposure might be pernicious, with major consequences for bird populations and communities. We finally propose several prospec- tive guidelines for future studies that may be consid- ered to meet urgent needs.
... Besides poisoned baits and rodenticides (Berny and Gaillet, 2008;Mateo-Tomás et al., 2020), red kites may also be frequently exposed to diverse contaminants: herbicides used as plant protection products in agriculture (Badry et al. In press); barbiturates used as euthanasia agents for domestic animals and livestock (Herrero-Villar et al., 2021); lead from hunting ammunition (Berny et al., 2015;Descalzo et al., 2021); along with other widespread contaminants such as polychlorinated biphenyls, organochlorine pesticides (Gomara and Gonzalez, 2006;Gomara et al., 2008;Monclus et al., 2018), and polycyclic aromatic hydrocarbons (Morin-Crini et al., 2022). These findings support the postulation that red kites are good sentinels of contamination risk for raptors (Badry et al. ...
Calls for urgent action to conserve biodiversity under global change are increasing, and conservation of migratory species in this context poses special challenges. In the last two decades the Convention on the Conservation of Migratory Species of Wild Animals (CMS) has provided a framework for several subsidiary instruments including action plans for migratory bird species, but the effectiveness and transferability of these plans remain unclear. Such laws and policies have been credited with positive outcomes for the conservation of migratory species, but the lack of international coordination and on-ground implementation pose major challenges. While research on migratory populations has received growing attention, considerably less emphasis has been given to integrating ecological information throughout the annual cycle for examining strategies to conserve migratory species at multiple scales in the face of global change. We fill this gap through a case study examining the ecological status and conservation of a migratory raptor and facultative scavenger, the red kite (Milvus milvus), whose current breeding range is limited to Europe and is associated with agricultural landscapes and restricted to the temperate zone. Based on our review, conservation actions have been successful at recovering red kite populations within certain regions. Populations however remain depleted along the southern-most edge of the geographic range where many migratory red kites from northern strongholds overwinter. This led us to a forward-looking and integrated strategy that emphasizes international coordination involving researchers and conservation practitioners to enhance the science-policy-action interface. We identify and explore key issues for conserving the red kite under global change, including enhancing conservation actions within and outside protected areas, recovering depleted populations, accounting for climate change, and transboundary coordination in adaptive conservation and management actions. The integrated conservation strategy is sufficiently general such that it can be adapted to inform conservation of other highly mobile species subject to global change.
... Poisoning by pollutants in the red kite has been widely studied, is considered one of the biggest threats to the conservation of this species (Viñuela et al. 2021). Many studies demonstrated intoxication after feeding on middens (Viñuela 1999;Monclús et al. 2018). However, there are not many reports of poisoning near landfills, except for one individual found in Spain (Herrero-Villar et al. 2021). ...
The juvenile dispersal of raptors is a crucial stage that stretches from parental independence to the establishment of the first breeding area. Between 2012 and 2020, 44 juvenile red kites (Milvus milvus) from the Spanish breeding population were tagged using GPS telemetry to study their dispersal. Juveniles left the parental breeding area at the end of their first summer and performed wandering movements throughout the Iberian Peninsula, returning to the parental breeding area the following year, repeating the same pattern until they settled in their first breeding area. We analyzed the mean distance from the nest, the maximum reached distances, and the travelled distances (daily and hourly) during the first two years of dispersal and compared them. Despite the high individual variability, variables describing the dispersal movements of juveniles showed a decreasing trend during the second dispersal year: 80 % of individuals reached a shorter maximum distance in the second year, 70% decreased their mean distance to the nest, 65% decreased their hourly travelled distances, and 50% decreased their daily travelled distances. On the other hand, the Red Kites usually combined wandering movements with establishment of temporary settlement areas (TSA). The average duration of settlement in the TSAs was 75 ± 40 days (up to 182 days) and were located at 182 ± 168 km from the nest. In those areas, juveniles used 781.0 ± 1895.0 km2 (KDE 95%). Some of the TSAs were used by several individuals, which suggests that these areas might be good targets for conservation in future management plans.
... Although the production and use of many POPs (particularly organochlorine compounds) were banned or restricted decades ago, they remain highly present in the environment and biota (AMAP, 2016). Even low levels of POPs may induce sub-lethal health effects, such as endocrine disruption (Monclus et al., 2018;Nordstad et al., 2012;Verboven et al., 2010), immune system impairment (Bustnes et al., 2004;Hansen et al., 2020;Sagerup et al., 2009), and oxidative stress (Costantini et al., 2014;Fenstad et al., 2016;Sletten et al., 2016). While the relationship between POP exposure and telomere lengths has been investigated in some avian species (Blevin et al., 2016(Blevin et al., , 2017Sebastiano et al., 2020;Sletten et al., 2016), findings are often inconsistent or inconclusive (Louzon et al., 2019), and wildlife ecotoxicology lacks long-term studies on how telomere lengths may fluctuate both over time and in relation to POP exposure. ...
Telomeres are used as biomarkers of vertebrate health because of the link between their length, lifespan, and survival. Exposure to environmental stressors appears to alter telomere dynamics, but little is known about telomere length and persistent organic pollutant (POP) exposure in wildlife. The white-tailed eagle (WTE; Haliaeetus albicilla) is an avian top predator that accumulates high levels of POPs and may subsequently suffer adverse health effects. Here we study the Baltic WTE population that is well documented to have been exposed to large contaminant burdens, thereby making it a promising candidate species for analyzing pollutant-mediated effects on telomeres. We investigated telomere lengths in WTE nestlings (n = 168) over 19 years and examined legacy POP concentrations (organochlorines and polybrominated diphenyl ethers) in whole blood and serum as potential drivers of differences in telomere length. Although we detected significant year-to-year variations in telomere lengths among the WTE nestlings, telomere lengths did not correlate with any of the investigated POP concentrations of several classes. Given that telomere lengths did not associate with POP contamination in the Baltic WTE nestlings, we propose that other environmental and biological factors, which likely fluctuate on a year-to-year basis, could be more important drivers of telomere lengths in this population.
... ng g − 1 ; Monclús et al., 2018a) and adult red kites (Milvus milvus) in Spain ( ∑ 5 PCBs range 0.56-122.44 ng g − 1 ;Monclús et al., 2018b)]. Concentrations of OPEs were in the range as previously reported in nestling white-tailed eagles (median concentrations range 4.3-110 ng g − 1 ;Eulaers et al., 2014) and adult northern goshawks (median concentrations range 25.5-206 ng g − 1 ;Briels et al., 2019) in Norway, and much higher than described in nestling cinereous vultures in Spain (median concentrations ranges 2.3-13.4 ...
The occurrence of organohalogenated compounds (OHCs) in wildlife has received considerable attention over the last decades. Among the matrices used for OHC biomonitoring, feathers are particularly useful as they can be collected in a minimally or non-invasive manner. In this study, concentrations of various legacy OHCs –polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs) and polybrominated diphenyl ethers (PBDEs)–, as well as emerging OHCs –per- and polyfluoroalkyl substances (PFAS) and organophosphate ester flame retardants (OPEs)– were determined in feathers of 72 Eurasian eagle-owls (Bubo bubo) from Norway, with the goal of studying spatiotemporal variation using a non-invasive approach. Molted feathers were collected at nest sites from northern, central and southern Norway across four summers (2013–2016). Additionally, two museum-archived feathers from 1979 to 1989 were included. Stable carbon (δ13C) and nitrogen isotopes (δ15N) were used as dietary proxies. In total, 11 PFAS (sum range 8.25–215.90 ng g⁻¹), 15 PCBs (4.19–430.01 ng g⁻¹), 6 OCPs (1.48–220.94 ng g⁻¹), 5 PBDEs (0.21–5.32 ng g⁻¹) and 3 OPEs (4.49–222.21 ng g⁻¹) were quantified. While we observed large variation in the values of both stable isotopes, suggesting a diverse diet of the eagle-owls, only δ 13C seemed to explain variation in PFAS concentrations. Geographic area and year were influential factors for δ15N and δ13C. Considerable spatial variation was observed in PFAS levels, with the southern area showing higher levels compared to northern and central Norway. For the rest of OHCs, we observed between-year variations; sum concentrations of PCBs, OCPs, PBDEs and OPEs reached a maximum in 2015 and 2016. Concentrations from 1979 to 1989 were within the ranges observed between 2013 and 2016. Overall, our data indicate high levels of legacy and emerging OHCs in a top predator in Norway, further highlighting the risk posed by OHCs to wildlife.
... A study of free-living adult kites corroborated the in ovo data by proving there is a positive association between adrenal hormones and PCB levels indicating an increase in corticosterone is the kite's way of coping with the stress of contaminant accumulation as well as that there are PCBs accumulated in adult feathers. 25 This would suggest that PCBs continue to accumulate in adult birds and have demonstrable negative consequences which provides further support for PCBs being linked to the sharp population decline. ...
Cell-based models in avian species have historically focused on virology due to the demands of animal agriculture and vaccine production industries. Recent years have witnessed a gradual rise in the use of these models ( in ovo, cell lines, primary cell cultures, organ slices, and organ-on-a-chip) in ecotoxicological studies as scientists and governments begin the shift to new approach methodologies, a shift validated by the recent memo by the Environmental Protection Agency announcing the end of mammalian testing in the next two decades. This rise has been hindered by the limited standards available for avian species and the unknowns surrounding cell-based assay applicability in extrapolation to in vivo. Toxicologists have incorporated these models in many different studies, including maternal deposition, mechanistic, metabolic, and non-target analysis methods, demonstrating the broad utility of cell-based assays. In ovo methods are ideal for reproductive and early life stage development studies, primary cell cultures for metabolic analysis, cell lines for long term studies requiring culture, organ slices for metabolic research, and organ-on-a-chip models for predictive analysis. These models all have their limitations that researchers need to consider when choosing which is most appropriate for the intended research, however. The current indications are that future avian cell-based model testing would benefit from expanding the species diversity available in cell lines and increasing metabolic conservation in full replacement methods. In ovo and primary cell culture methods should also be examined to increase efficiency and further reduce animal usage. This review examines the use, limitations, and published applications of these models in an ecotoxicological context to understand the current state of avian cell-based models to explain what future directions should be taken and how best to apply the methods available to current problems that avian researchers are approaching.
... Decreased DHEA-S has also been described with several diseases, including renal (Zumoff et al. 1980) and liver disease (Floreani et al. 1991), diabetes mellitus (Yamauchi et al. 1996), coronary artery disease (Herrington et al. 1990), rheumatoid arthritis (Masi 1995), and Alzheimer's disease (Svec and Lopez 1989). Studies in other taxa suggest that acute and chronic stress may also increase DHEA-S concentrations in rhesus macaques (Maninger et al. 2010) and in birds (Monclús et al. 2018;Newman et al. 2008), while clinical pathology is associated with decreased DHEA in cattle (Almeida et al. 2008). Increased DHEA occurs following ACTH stimulation (Yon et al. 2007b) and during the physiological state of musth in Asian bull elephants (Yon et al. 2007a). ...
To reverse the trend of declining wildlife populations globally, individuals must be provided with conditions that allow them to not just survive, but to thrive. It is no longer only the remit of captive breeding programs to ensure animal well-being; in situ conservation efforts also must consider how environmental and anthropogenic pressures impact wild populations, and how to mitigate them—especially with regards to reproduction and survival. Stress and welfare are complex concepts that necessitate an understanding of how stressors affect animals on both individual and population levels. There are species differences in how factors impact well-being, related in part to natural history, which also are shaped by individual perceptions and coping abilities. A multitude of stress-related responses then have the potential to disrupt fertility on many levels, and ultimately fitness. A major limitation to advancing welfare science is the lack of definitive tests to verify welfare status; i.e., is the animal happy or not? While analyses of circulating or excreted glucocorticoids have for decades been the primary method of assessing stress, today we recognize the need for more objective indicators that incorporate multiple physiological systems, including behavior, to assess both negative and positive welfare states. In this chapter, we discuss the potential for stress to disrupt, and sometimes facilitate reproduction, including the key role that glucocorticoids play. We then discuss a number of physiological biomarkers, which in addition to glucocorticoids, have the potential to assess well-being and the role of stress on reproduction. Finally, we discuss allostatic load, a method by which multiple physiological markers are used to inform on morbidity and mortality risk in humans, which if applied to wildlife, could be a powerful tool for conservation.
Bearded vulture (Gypaetus barbatus) populations are declining worldwide primarily due to anthropogenic factors. A captive breeding program has been established in Spain, a country with one of the largest free-living populations in Europe, to further enhance the conservation efforts of this emblematic species. However, captive vulture populations can be exposed to different risks through food, such as drug residues and antimicrobial-resistant (AMR) bacteria. Health surveillance of species involved in captive breeding programs is important to face introduction of healthy animals in situ and to obtain baseline clinical data. The objective of this study was to assess the general health status of bearded vultures held in captivity in Catalonia (northeastern Spain) by carrying out hematologic, biochemical, toxicologic, and bacteriologic analyses. A total of 16 bearded vultures were sampled; the data obtained from one vulture, with a chronic tibiotarsal fracture, were excluded from the statistical analysis. Hematologic and biochemical parameters of the bearded vultures were mostly within the range of standard values as stated in previous studies. Basal feather and serum corticosterone levels were analyzed and described for the first time in this species. A total of 15 Escherichia coli isolates were obtained that were resistant to fluoroquinolones (80%), tetracycline (60%), trimethoprim and ampicillin (40%), sulfamethoxazole (33%), and colistin (20%), with 40% of them being multidrug resistant. Three of 15 isolates were carriers of the mcr-1 gene. Only the injured bird previously treated with enrofloxacin was positive for fluoroquinolone residues. Periodic monitoring for the presence of AMR bacteria would be recommended in captive breeding programs as a preventive action to establish future therapies.
Organisms face energetic challenges of climate change in combination with suites of natural and anthropogenic stressors. In particular, chemical contaminant exposure has neurotoxic, endocrine-disrupting, and behavioral effects which may additively or interactively combine with challenges associated with climate change. We used a literature review across animal taxa and contaminant classes, but focused on Arctic endotherms and contaminants important in Arctic ecosystems, to demonstrate potential for interactive effects across five bioenergetic domains: (1) energy supply, (2) energy demand, (3) energy storage, (4) energy allocation tradeoffs, and (5) energy management strategies; and involving four climate change-sensitive environmental stressors: changes in resource availability, temperature, predation risk, and parasitism. Identified examples included relatively equal numbers of synergistic and antagonistic interactions. Synergies are often suggested to be particularly problematic, since they magnify biological effects. However, we emphasize that antagonistic effects on bioenergetic traits can be equally problematic, since they can reflect dampening of beneficial responses and result in negative synergistic effects on fitness. Our review also highlights that empirical demonstrations remain limited, especially in endotherms. Elucidating the nature of climate change-by-contaminant interactive effects on bioenergetic traits will build toward determining overall outcomes for energy balance and fitness. Progressing to determine critical species, life stages, and target areas in which transformative effects arise will aid in forecasting broad-scale bioenergetic outcomes under global change scenarios.
Synopsis
Chemical defense is a crucial component of fitness in many organisms, yet the physiological regulation of defensive toxin synthesis is poorly understood, especially in vertebrates. Bufadienolides, the main defensive compounds of toads, are toxic to many predators and other natural enemies, and their synthesis can be upregulated by stressors, including predation risk, high conspecific density, and pollutants. Thus, higher toxin content may be the consequence of a general endocrine stress response in toads. Therefore, we hypothesized that bufadienolide synthesis may be stimulated by elevated levels of corticosterone (CORT), the main glucocorticoid hormone of amphibians, or by upstream regulators that stimulate CORT production. To test these alternatives, we treated common toad tadpoles with exogenous CORT (exoCORT) or metyrapone (MTP, a CORT-synthesis inhibitor that stimulates upstream regulators of CORT by negative feedback) in the presence or absence of predation cues for 2 or 6 days, and subsequently measured their CORT release rates and bufadienolide content. We found that CORT release rates were elevated by exoCORT, and to a lesser extent also by MTP, regardless of treatment length. Bufadienolide content was significantly decreased by treatment with exoCORT for 6 days but was unaffected by exposure to exoCORT for 2 days or to MTP for either 6 or 2 days. The presence or absence of predation cues affected neither CORT release rate nor bufadienolide content. Our results suggest that changes in bufadienolide synthesis in response to environmental challenges are not driven by CORT but may rather be regulated by upstream hormones of the stress response.
La mayoría de los milanos reales del viejo continente son migradores. Tienen sus áreas de reproducción en Centroeuropa y de invernada en el sur del con-tinente, pero tanto en un lugar como en otro existen pequeñas poblaciones sedentarias que no realizan estas migraciones intracontinentales. En el caso de España, existen alrededor de 2.312-2.440 parejas reproductoras (Molina, 2015) que no abandonan la península en ningún momento de su ciclo de vida. A dicha población se dedica este capítulo, tratando de comprender cómo son los movimientos de individuos adultos reproductores de ambos sexos durante esta fase fundamental de su ciclo vital. Los milanos reales suelen comenzar a reproducirse a partir del segundo año, aunque ha habido casos de milanos que se han reproducido con un año, o al-gunos que no lo han hecho hasta los siete años de edad (Newton et al., 1989; Evans et al., 1999). En cualquier caso, la época de cría comienza, como en la mayoría de rapaces, a principios de primavera. Tras la selección de pareja y el establecimiento del nido, el periodo de incubación suele producirse entre marzo y abril (Veiga y Hiraldo, 1990, Newton et al., 1996). Los milanos reales ponen entre uno y tres huevos, excepcionalmente hasta cinco (Newton et al., 1996). La puesta es incubada alrededor de un mes y el desarrollo de los pollos se completa aproximadamente dos meses después (Bustamante, 1993). De esta forma, los juveniles comienzan a sobrevolar las inmediaciones del nido natal durante el verano, cuando progresivamente irán independizándose del cuidado paterno. Esta parte del análisis de los movimientos generales de la especie, la época repro-ductora, fue realizada con 29 ejemplares adultos que se reproducían en España (6 machos y 22 hembras), capturados y marcados en distintas provincias entre 2009 y 2017 (tabla 1, anexo 1). Con el objetivo de homogeneizar los análisis, se consideró que el periodo de cría del milano abarcaba desde el 1 de marzo al 30 de junio. Por tanto, este trabajo engloba, al menos, las principales fases del periodo reproductivo: incubación y cuidado de los pollos, así como la fase previa a la independización de los juveniles. MOVIMIENTOS DURANTE EL PERIODO REPRODUCTOR Machos y hembras de milano real son prácticamente idénticos desde el punto de vista físico, pero los datos obtenidos demuestran que asumen roles diferen-ciados en la reproducción, como ocurre con otras muchas aves. Normalmente, son las hembras las que permanecen cerca del nido, protegiendo la puesta y los pequeños pollos. Los machos, por su parte, se ocupan de traer el alimento desde sitios más alejados del nido. Aunque ambos participan en la alimentación ECOLOGÍA ESPACIAL EN EL PERIODO REPRODUCTIVO
La dispersión juvenil o dispersión natal es el conjunto de movimientos explora-torios que realizan las aves antes de llegar a la edad adulta. En esta etapa, los juveniles tienen un comportamiento distinto al de los adultos, por lo que se la considera una etapa diferenciada con características propias. Los movimientos dispersivos juveniles se caracterizan por ser exploratorios, sin periodicidad ni rumbo fijo como es el caso de las migraciones. Los individuos juveniles realizan movimientos de aparente vagabundeo por un vasto territorio alejados de los nidos de sus padres. La dispersión juvenil comienza cuando las aves abandonan las inmediaciones del nido en el que nacieron. En el caso de los pollos de milano real, tras haber crecido lo suficiente y haber completado el desarrollo del plumaje, pasan un periodo de alrededor de 3-4 semanas en que realizan sus primeros vuelos bajo el cuidado y atención de los padres, cerca del nido (Bustamante, 1993). Tras ello, comienza la dispersión juvenil propiamente dicha, que engloba el abandono del territorio del nido, los movimientos exploratorios lejos de este y el posible asentamiento en áreas temporales donde permanecen semanas o meses entre aquellos movimientos dis-persivos. La dispersión juvenil acaba con el establecimiento de la nueva área de cría del individuo potencialmente reproductor. No todos los milanos reales juveniles tienen este comportamiento. Los movimien-tos de los juveniles dependen, en gran medida, del origen de sus parentales. Los individuos juveniles nacidos en Centroeuropa realizan comúnmente una migración similar a la de los adultos e invernan en España y Francia, como ya se detalla en el capítulo correspondiente de las estrategias migratorias. A diferencia de ellos, los individuos nacidos en España realizan movimientos dispersivos por gran parte de la península Ibérica. La dispersión juvenil es una etapa fundamental para las dinámicas poblacionales de las aves rapaces, dado que estas dependen en gran medida de la cantidad de individuos que llegan a reproducirse (Penteriani y Del Mar Delgado, 2009), por lo que el conocimiento de los movimientos de los juveniles, en qué áreas temporales se establecen y dónde localizan sus nuevos nidos es fundamental para la conser-vación de esta especie en España. Este capítulo está dedicado a estos últimos movimientos dispersivos. Se analizan sus movimientos desde el momento que abandonan los nidos donde nacieron, hacia el final del verano, hasta que cumplen los dos años de edad, cuando alcanzan la edad reproductora (Newton et al., 1989). Aquí se comparan los parámetros tanto del primer como del segundo año, así como entre ellos. A pesar de que se contaba con 79 individuos marcados, la elevada mortalidad que caracteriza a los juveniles y algunos fallos de los emisores, originó que el número de individuos que alcanzaron el primer y segundo año de edad se redujo a 44 y 21, respectivamente.
Polychloro-1,3-butadienes (polyCBDs) are attracting increasing concern due to their high toxicity. However, research on multiple polyCBDs in aquatic biota is still extremely limited. In this study, a sensitive method for simultaneous determination of nine polyCBD (Cl4–Cl6) congeners, including six tetrachlorobutadiene (TeCBD) isomers, two pentachlorobutadiene (PeCBD) isomers, and hexachlorobutadiene (HCBD), in shellfish was developed based on accelerated solvent extraction (ASE), solid-phase extraction (SPE) clean-up and gas chromatography-triple quadrupole mass spectrometry (GC-QqQ-MS/MS). Low method limits of detection (MDLs) in the range 0.03–0.21 ng/g dry weight for target analytes with satisfactory recoveries (47.7 %–70.6 %) were achieved. The valid method was then applied to analyze nine polyCBDs congeners in 42 shellfish and 11 fish samples collected from markets in eight coastal cities, China. Trace HCBD was detected in 14 samples, while TeCBDs and PeCBDs were under the MDLs in all the samples, indicating little contamination of these pollutants in the marketed shellfish and fish in China. Multiple polyCBDs especially TeCBDs and PeCBDs were firstly involved in the proposed method and investigation here, which lay the groundwork for future research on the environmental behavior and exposure risks of polyCBDs in aquatic biotas.
六氯丁二烯是一种持久性有机污染物,于2015年和2017年分别被列入《斯德哥尔摩公约》附件A和附件C的受控污染物名单中。六氯丁二烯的来源、环境赋存和影响等研究对控制该新增受控持久性有机污染物污染具有重要意义,而灵敏可靠的六氯丁二烯分析方法是开展相关研究的前提和基础。近年来已有不少学者将六氯丁二烯作为分析目标物之一进行了检测或方法学研究。基于这些研究成果,该文综述了六氯丁二烯分析方法的研究进展,其中重点介绍了空气、水体、土壤、污泥、生物组织等多种介质中六氯丁二烯的样品前处理方法,并比较了各方法的优缺点,以期为该领域的进一步研究提供参考。空气中六氯丁二烯主要由泵抽气通过吸附管而采集,再经热脱附后进行仪器分析,检出限在ng/m³水平。也有研究应用聚氨酯泡沫被动采样器和吸附剂填充聚氨酯泡沫被动采样器采集大气中六氯丁二烯及其他污染物。基于吸附剂填充聚氨酯泡沫被动采样器的分析方法灵敏度较高,其对六氯丁二烯的检出限低至0.03 pg/m³。然而目前被动采样体积仅根据六氯丁二烯的log KOA系数估算,未来仍需进一步实验校正。水体样品前处理通常也较简单,通过吹扫捕集、液-液萃取或固相萃取目标物后进行仪器分析。固相萃取法能够同步实现目标物的提取、净化和浓缩,在水样中六氯丁二烯分析方面具有明显优势。固相萃取柱类型以及干燥步骤中柱中残留水分去除率均会影响六氯丁二烯的回收率。灰尘、土壤、沉积物、污泥和生物组织等固体介质样品基质最为复杂,需联合多种方法进行前处理。固体样品中六氯丁二烯提取方法包括索氏提取,加速溶剂萃取和超声萃取,其中超声萃取法应用最为广泛。固体基质净化方面主要采用层析柱色谱法,多根净化柱联用或多层复合柱能够提升净化效果。仪器分析方面,六氯丁二烯主要采用气相色谱和质谱联用检测,高性能质谱检测器如串联质谱能够大大提高六氯丁二烯的检测灵敏度,具有较大的应用潜力。
The use of a non-invasive approach to collect biological samples from natural populations represents a great means of gathering information while avoiding handling animals. Even if corticosterone is the main glucocorticoid investigated in birds, it has been observed a proportional direct link between corticosterone and cortisol concentrations. Dehydroepiandrosterone (DHEA) can be produced by the adrenal cortex and should have prominent antiglucocorticoid properties also in birds. The aim of this study was to verify if there is any difference in the cortisol and DHEA feather concentrations between clinically normal and physiologically compromised Griffon vultures ( Gyps fulvus ) through the non-invasive approach of collecting moulted feathers without having to pluck them from the bird. The study was carried out using 8 physiologically compromised (PC) Griffons and 9 clinically normal Griffons considered as the control (CTRL) group that were necropsied or from the wildlife rehabilitation centre. Primary and secondary covert feathers were either collected directly from the birds’ cage floors, or, in the case of dead Griffons, they were plucked off the animals. The results, obtained by RIA, revealed that both cortisol (P<0.01) and DHEA (P<0.05) feather concentrations were higher in the PC than in the CTRL group. No difference was observed by comparing the cortisol/DHEA ratio between the two evaluated groups (P=0.15). Pearson’s correlation coefficients showed no correlation between feather hormone concentrations in the PC group (r=0.01, P=0.96) while a positive correlation in the CTRL group (r=0.65, P=0.006) was observed. In conclusion, our study reveals that moulted feathers can be a non-invasive and an interesting tool to evaluate the allostatic load of wild birds and they allowed to better understand the relationship between hormones of the hypothalamic–pituitary–adrenal axis and the physiological status of the birds.
Research on hexachlorobutadiene (HCBD) has increased since its listing in the Stockholm Convention on Persistent Organic Pollutants in 2011. However, thorough reports on recent data regarding this topic are lacking. Moreover, potential associations between HCBD and some chlorinated organics have usually been ignored in previous research. In this review, possible formation pathways and sources, current environmental occurrences and human exposure risks of HCBD are discussed, as well as the association with several organochlorine compounds. The results reveal that unintentional production and emission from industrial activities and waste treatments are the main sources of HCBD. Similar precursors are found for HCBD and chlorobenzenes, indicating the presence of common sources. Although recent data indicates that levels of HCBD in the environment are generally low, risks from human exposure to HCBD, together with other pollutants, may be high. More attention in the future needs to be paid to the mixed contamination of HCBD and other pollutants from common sources.
To overcome unpredictable stressful transitory events, animals trigger an allostatic response involving the hypothalamic-pituitary-adrenal cortex. This hormonal response, which involves the release of glucocorticoids which in turn mediate between the main physiological mechanisms that regulate the energetic demands and resource allocation trade-off with behavioural responses to environmental perturbations and may ultimately lead to variation in fitness. We have used the Cory's shearwater Calonectris borealis, a sexually dimorphic pelagic seabird with a partial migratory strategy, as a model bird species to analyse a number of traits related to the stress response. We investigated whether the activation of a stressful response, mediated by corticosterone, during the wintering period (1) correlated with the previous breeding success, (2) was affected by the migratory behaviour of male birds and (3) had consequences in the fitness of the birds. Corticosterone levels in feathers grown overwinter were analysed in 61 adult birds during three consecutive migratory periods (2009-2012) and in 14 immature birds in the wintering period 2010-2011. Moreover, the levels of corticosterone were analysed in experimental birds which were freed from their reproductive duties and compared with control birds which raised fledglings to the end of the breeding period. The results show that the levels of corticosterone were sex dependent, differed between years and were affected by the migratory strategy performed by the birds. The activation of the stressful response over the wintering period generated residual carry-over effects that positively affected the reproductive output in the subsequent breeding stage, a phenomenon previously undescribed in a long-lived pelagic seabird. Our study provides evidence that the analysis of corticosterone from feathers is a useful tool to evaluate carry-over effects in birds far away from breeding sites, opening new possibilities for future studies in this field.
Biomonitoring using birds of prey as sentinel species has been mooted as a way to evaluate the success of European Union directives that are designed to protect people and the environment across Europe from industrial contaminants and pesticides. No such pan-European evaluation currently exists. Coordination of such large scale monitoring would require harmonisation across multiple countries of the types of samples collected and analysed-matrices vary in the ease with which they can be collected and the information they provide. We report the first ever pan-European assessment of which raptor samples are collected across Europe and review their suitability for biomonitoring. Currently, some 182 monitoring programmes across 33 European countries collect a variety of raptor samples, and we discuss the relative merits of each for monitoring current priority and emerging compounds. Of the matrices collected, blood and liver are used most extensively for quantifying trends in recent and longer-term contaminant exposure, respectively. These matrices are potentially the most effective for pan-European biomonitoring but are not so widely and frequently collected as others. We found that failed eggs and feathers are the most widely collected samples. Because of this ubiquity, they may provide the best opportunities for widescale biomonitoring, although neither is suitable for all compounds. We advocate piloting pan-European monitoring of selected priority compounds using these matrices and developing read-across approaches to accommodate any effects that trophic pathway and species differences in accumulation may have on our ability to track environmental trends in contaminants.
Electronic supplementary material
The online version of this article (doi:10.1007/s10646-016-1636-8) contains supplementary material, which is available to authorized users.
Endocrine disrupting chemicals (EDC) are released into environment from different sources. They are mainly used in packaging industries, pesticides and food constituents. Clinical evidence, experimental models, and epidemiological studies suggest that EDC have major risks for human by targeting different organs and systems in the body. Multiple mechanisms are involved in targeting the normal system, through estrogen receptors, nuclear receptors and steroidal receptors activation. In this review, different methods by which xenobiotics stimulate signaling pathways and genetic mutation or DNA methylation have been discussed. These methods help to understand the results of xenobiotic action on the endocrine system. Endocrine disturbances in the human body result in breast cancer, ovarian problems, thyroid eruptions, testicular carcinoma, Alzheimer disease, schizophrenia, nerve damage and obesity. EDC characterize a wide class of compounds such as organochlorinated pesticides, industrial wastes, plastics and plasticizers, fuels and numerous other elements that exist in the environment or are in high use during daily life. The interactions and mechanism of toxicity in relation to human general health problems, especially endocrine disturbances with particular reference to reproductive problems, diabetes, and breast, testicular and ovarian cancers should be deeply investigated. There should also be a focus on public awareness of these EDC's risks and their use in routine life. Therefore, the aim of this review is to summarize all evidence regarding different physiological disruptions in the body and possible involved mechanisms, to prove the association between endocrine disruptions and human diseases.
Despite their long-term ban, persistent organochlorine compounds like hexachlorobenzene (HCB), p,p′-dichlorodiphenylethylene (DDE) as well as polychlorinated biphenyls (PCBs) are still of environmental concern. For the evaluation of potential occupational or environmental exposures to these substances, it is essential to know the current background burden of the general population. As representative and up-to-date information is missing for Germany, we have analysed a large dataset generated in studies on potential exposure to lower chlorinated PCBs to fill this gap for the levels of HCB, DDE as well as PCB 138, PCB 153 and PCB 180.
1. The concentration of the glucocorticoid hormone corticosterone (CORT) is increasingly used in ecology and conservation biology as an integrated measure of the historical record of an individual’s hypothalamo-pituitary-adrenal (HPA) activity during feather growth. However, where and how CORT is incorporated in feathers is incompletely known.
2. We therefore examined whether CORT is reliably measured with an enzyme immunoassay, where CORT is incorporated in the feather and where it affects feather quality, and whether CORT incorporation is related to plasma CORT levels, feather growth rate and melanin pigmentation.
3. During regrowth of plucked tail feathers, we injected pigeons with tritium-labelled CORT, and implanted a CORT-releasing pellet to increase plasma CORT concentration for about three days. In feather segments we measured labelled CORT (DPM3H) and we quantified CORT with an enzyme immunoassay EIA (CORTEIA) and double-checked the results with ultra-high performance liquid chromatography-tandem mass spectrometry (LCMS) (CORTMS).
4. Administered CORT affected feather structure and colour at the very base of the feather (epidermal collar, ramogenic zone) and reduced growth rate. In contrast, incorporation of CORT into the feather happened mainly in the blood quill, as shown with all three methods (DPM3H, CORTEIA, and CORTMS).
5. Incorporation of CORT into feathers was only roughly proportional to plasma concentration, proportional to feather-growth rate and increased with melanin pigmentation.
6. Measuring CORT in feather is a way to reveal past events of increased stress during feather growth in birds.
In nest-bound avian offspring food shortages typically trigger a release of the stress hormone corticosterone (CORT). Recent studies indicate that CORT is passively deposited in the tissue of growing feathers and thus may provide an integrated measure of stress incurred during development in the nest. The current hypothesis predicts that, assuming a constant rate of feather growth, elevated CORT circulating in the blood corresponds to higher levels of CORT in feather tissue, but experimental evidence for nutritionally stressed chicks is lacking. Here we examine how food limitation affects feather CORT content in the rhinoceros auklet (Cerorhinca moncerata). We i) used captive chicks reared on control vs. restricted diets, and ii) applied this technique to free-living chicks with unknown nutritional histories that fledged at three separate colonies. We found that i) feather growth was not affected by experimentally-induced nutritional stress; ii) captive chicks raised on a restricted diet had higher levels of CORT in their primary feathers; iii) feather CORT deposition is a sensitive method of detecting nutritional stress; and iv) free-living fledglings from the colony with poor reproductive performance had higher CORT in their primary feathers. We conclude that feather CORT is a sensitive integrated measure revealing the temporal dynamics of food limitations experienced by rhinoceros auklet nestlings. The use of feather CORT may be a powerful endocrine tool in ecological and evolutionary studies of bird species with similar preferential allocation of limited resources to feather development.
Among European breeding birds, those wintering in the Sahel region have undergone a sustained and severe decline. Long‐term data show that variation in primary production of the Sahelian staging area significantly affects survival of many species, a relationship probably mediated by trophic resource availability. However, the physiological, hormonal and behavioural responses underlying this relationship remain unexplored. We present a potential explanation for the importance of prevailing conditions during winter to understand the population ecology and current trends of migratory species. We measured corticosterone levels in feathers of Egyptian vultures Neophron percnopterus grown in Africa and Europe, showing how conditions faced by birds during wintering periods result in the release of more corticosterone over time than when those individuals were on their summering grounds. This pattern was concordant with home‐range size differences (c. 33 times larger in Africa than in Europe). We suggest that as wintering habitat of Egyptian vultures in the Sahel region has degraded during recent times, food availability has also been reduced. An increase in corticosterone during winter with a consequent increase in locomotor activity, for example, food searching behaviour, may normally be adaptive. However, enlarging home ranges could be futile if conditions are not better in the dispersal area, and costs of the higher corticosterone level, including energy expenditure from enhanced activity, may pose a significant trade‐off. These physiological responses may be characteristic of other European trans‐Saharan migrant birds that have undergone significant population declines.
The timing of moult in birds is thought to be constrained by physiological trade-offs.
We studied barn swallows in central Spain to assess whether (a) body moult tends to
be temporally separated from migration in adult and first-year birds, (b) it is related to
an impaired fattening, and (c) its overlap with migration may involve adverse
energetic effects. First-year swallows tended to moult early in the post-breeding
period: the proportion of first-year birds in active moult was highest in July, and it
decreased progressively until September. On the other hand, adult swallows tended to
avoid moulting both in the post-breeding (July) and the migratory period (September),
concentrating their moulting period in August. In all periods, swallows in active
moult stored less fat than non-moulting ones, suggesting a faster depletion of energy
resources by moulting birds. Swallows in active moult showed a better body
condition — measured as body mass relative to body size and fat content — than nonmoulting
ones before migration (coinciding with the periods of highest frequency of
moulting individuals), but the opposite was found during autumn migration. Our
results support the existence of a physiological trade-off between body moult and
migration, which could have fitness consequences; thus, if these activities overlap it
would impair migration performance of swallows.
1. Life-history theory predicts a trade-off between costs of current reproduction and future survival of individuals. Studies of short-lived animals in general support this prediction. However, the effect of nutritional stress during reproduction on survival of long-lived animals is poorly understood.
2. We examined the link between nutritional stress, fecundity and return to a breeding colony (hereafter ‘survival’) of black-legged kittiwakes (Rissa tridactyla) at two colonies with contrasting patterns in adult survival, fecundity, and numerical trends.
3. We tested the observational (at Duck and Gull Is., Cook Inlet, Northern Gulf of Alaska) and experimental (at Middleton I., Gulf of Alaska) relationships between variations in the secretion of the stress hormone corticosterone (CORT) and food abundance. Then, we examined the relationships between nutritional stress (as reflected in CORT), reproduction, and survival of individuals.
4. On average, CORT was higher in kittiwakes breeding on Duck I. (declining, low fecundity, high survival) compared to those breeding on Gull I. (increasing, high fecundity, low survival).
5. At both colonies, CORT was directly negatively correlated with food abundance quantified at sea. Experimental feeding of individuals ad libitum resulted in a reduction of CORT in birds breeding on Middleton I. These results suggest that CORT is a reliable measure of food availability and defines nutritional stress (stress) in kittiwakes.
6. On Gull I., where survival is low (86%), production of young declined as stress increased. On Duck I., where survival is high (93%), parents always failed in raising young, though they experienced a wide range of stress levels.
7. Survival of individuals is linked to their CORT levels during reproduction. High levels of CORT predicted disappearance of individuals from both colonies.
8. The results support the hypothesis that nutritional stress during reproduction affects both survival and reproduction in long-lived animals. However, even within a species the ways in which survival and reproduction trade-off against each other may vary among populations. Results suggest that reproductive consequences of nutritional stress might differ between declining and increasing populations, which should be tested. We conclude that severity of nutritional stress during reproduction is one of the major factors defining population processes in kittiwakes.
-: DOI: http://dx.doi.org/10.1065/espr2006.01.015
Species that are at high levels of the food web have often been used as bioindicators to evaluate the presence of persistent contaminants in ecosystems. Most of these species are long-lived, so pollutant burdens may be integrated in some complex way over time. This makes them particularly sensitive to deleterious effects of Persistent Organic Pollutants (POPs). Birds have been suggested as useful organisms for monitoring pollutant levels. Traditionally such studies have been carried out with raptors such as osprey (Pandion haliaetus), peregrine falcon (Falco peregrinus), bald eagle (Haliaetus leucocephalus), etc. In this paper we present the results of a monitoring study conducted on two raptor species, osprey (Pandion haliaetus) and red kite (Milvus milvus), inhabiting a Mediterranean island (Menorca, Spain). These two species have different feeding habits; ospreys prey on fish and red kites feed on terrestrial species. This study constitutes a good opportunity to investigate if differences in feeding habits (aquatic vs. terrestrial) influences the contaminants pattern in two species inhabiting the same area.
The study was conducted in a non-destructive way, using only failed eggs, to avoid the damage of the population stability. Eggs were collected during the period 1994-2000. The contaminants examined were dichlorodiphenyltrichloroethanes (DDTs, including DDT and its main metabolite, DDE), polychlorinated biphenyls (PCBs), including ortho PCBs (PCBs with at least one Chlorine atom in the ortho position): #28, 52, 95, 101, 123+149, 118, 114, 153, 132+105, 138, 167, 156, 157, 180, 170, 189, 194; and non ortho PCBs (PCBs with no Chlorine atom in the ortho position): #77, 126, 169 and all the polychlorinated dibenzo-p-dioxins (PCDDs) and polychlorinated dibenzofurans (PCDFs) with Chlorine atoms at the 2,3,7 and 8 position (2,3,7,8-substituted PCDDs and PCDFs). The analysis of organochlorine compounds was performed using a sample treatment based on a Solid Phase Matrix Dispersion procedure. Ortho PCBs and DDTs were determined by HRGC-µECD; non ortho PCBs and PCDD/Fs were determined by HRGC-HRMS.
The sum of the ortho PCB congeners analysed ranged from 0.94 to 15.03 µg/g wet weight (ww) for ospreys and from 1.0 to 11.2 µg/g ww for red kites. In both species, PCB congeners #153, #138 and #180 accounted about 75% to total ortho PCB concentrations. Regarding non ortho PCBs, for ospreys, concentrations ranged from 0.16 to 1.39 ng/g wet weight (ww) and for red kites from 0.12 to 0.51 ng/g ww, being congener #126 the most abundant. Concerning DDTs, concentration for ospreys ranged from 0.07 to 1.03 µg/g ww; and for red kites ranged from 0.90 to 2.10 µg/g ww, representing DDE more than 95% of the total DDTs, which proves a past use of DDT in the study area. Differences in contaminant levels between species are probably associated to feeding habits. The fish-eating species presents the highest PCB levels, whereas the terrestrial species exhibits the highest DDT levels. PCDD/Fs in ospreys were in the range 2.6-14.2 pg/g ww, while in red kites the range was slightly wider (22.2-43.2 pg/g ww), being PCDDs the major contributors in black kites. Ospreys had PCDDs similar to PCDF concentrations. PCDD/F profiles were mostly influenced by OCDD in both species. Non ortho PCBs were the major contributors to calculated Toxic Equivalent Quantity (TEQs) in both species.
In both species studied, ortho-PCBs could represent a problem of concern since 57% of the eggs exhibited levels higher than 4 µg/g ww, reported as the level that could cause reduced hatchability, embryo mortality, and deformities in birds.
Results found in this study suggest that a more detailed study to clear up possible deleterious effects of PCBs on the bird populations studied here should be done.
Stress responses play a key role in allowing animals to cope with change and challenge in the face of both environmental certainty and uncertainty. Measurement of glucocorticoid levels, key elements in the neuroendocrine stress axis, can give insight into an animal's well-being and can aid understanding ecological and evolutionary processes as well as conservation and management issues. We give an overview of the four main biological samples that have been utilized [blood, saliva, excreta (feces and urine), and integumentary structures (hair and feathers)], their advantages and disadvantages for use with wildlife, and some of the background and pitfalls that users must consider in interpreting their results. The matrix of choice will depend on the nature of the study and of the species, on whether one is examining the impact of acute versus chronic stressors, and on the degree of invasiveness that is possible or desirable. In some cases, more than one matrix can be measured to achieve the same ends. All require a significant degree of expertise, sometimes in obtaining the sample and always in extracting and analyzing the glucocorticoid or its metabolites. Glucocorticoid measurement is proving to be a powerful integrator of environmental stressors and of an animal's condition.
There have been several case studies of the impact of chemical contaminants on birds at the level of individuals or populations. While many of the chemicals involved in these incidents have been classified as endocrine-disrupting chemicals or endocrine active sub- stances (EASs) the mechanisms by which these chemicals affect birds are not clearly or fully understood.
Sixteen organochlorine pesticides (OC) were analyzed in several tissue types (abdominal and subcutaneous fat, liver and brain) from juvenile (n=14), immature (n=9), subadult (n=7) and adult (n=20) razorbill (Alca torda) collected from the southwestern Mediterranean coastline, in the East of Spain (La Marina, Elche, Alicante, Spain). These razorbills had drowned in fishing nets (most probably) while searching for food. The objective was to assess the exposure to organochlorine pesticide residues in this wintering population of marine birds. This paper presents, as far as we are aware, the first published data on OC concentrations in razorbills. The highest levels were found in abdominal fat followed by subcutaneous fat, liver and brain. A significant positive relationship was found between age and OC levels in tissues, and with the highest levels in adults. The group of sigma Drins had the highest concentrations, followed by sigma DDT, sigma Endosulfan, sigma HCH and sigma Heptachlor, with endrin aldehyde being the compound which reached the highest levels. The p,p'-DDE/p,p'-DDT ratio in fatty tissues suggests exposure to non-degraded DDT and thus is present in the environment despite its prohibition. The OC levels detected were higher than those found in other studies on Alcidae, which may be explained by the Mediterranean habitat in which the birds were found. However, these levels are below concentrations for which any observable effect has been described.
Persistent organic pollutants (POPs) encompass an array of anthropogenic organic and elemental substances and their degradation and metabolic byproducts that have been found in the tissues of exposed animals, especially POPs categorized as organohalogen contaminants (OHCs). OHCs have been of concern in the circumpolar arctic for decades. For example, as a consequence of bioaccumulation and in some cases biomagnification of legacy (e.g., chlorinated PCBs, DDTs and CHLs) and emerging (e.g., brominated flame retardants (BFRs) and in particular polybrominated diphenyl ethers (PBDEs) and perfluorinated compounds (PFCs) including perfluorooctane sulfonate (PFOS) and perfluorooctanic acid (PFOA) found in Arctic biota and humans. Of high concern are the potential biological effects of these contaminants in exposed Arctic wildlife and fish. As concluded in the last review in 2004 for the Arctic Monitoring and Assessment Program (AMAP) on the effects of POPs in Arctic wildlife, prior to 1997, biological effects data were minimal and insufficient at any level of biological organization. The present review summarizes recent studies on biological effects in relation to OHC exposure, and attempts to assess known tissue/body compartment concentration data in the context of possible threshold levels of effects to evaluate the risks. This review concentrates mainly on post-2002, new OHC effects data in Arctic wildlife and fish, and is largely based on recently available effects data for populations of several top trophic level species, including seabirds (e.g., glaucous gull (Larus hyperboreus)), polar bears (Ursus maritimus), polar (Arctic) fox (Vulpes lagopus), and Arctic charr (Salvelinus alpinus), as well as semi-captive studies on sled dogs (Canis familiaris). Regardless, there remains a dearth of data on true contaminant exposure, cause-effect relationships with respect to these contaminant exposures in Arctic wildlife and fish. Indications of exposure effects are largely based on correlations between biomarker endpoints (e.g., biochemical processes related to the immune and endocrine system, pathological changes in tissues and reproduction and development) and tissue residue levels of OHCs (e.g., PCBs, DDTs, CHLs, PBDEs and in a few cases perfluorinated carboxylic acids (PFCAs) and perfluorinated sulfonates (PFSAs)). Some exceptions include semi-field studies on comparative contaminant effects of control and exposed cohorts of captive Greenland sled dogs, and performance studies mimicking environmentally relevant PCB concentrations in Arctic charr. Recent tissue concentrations in several arctic marine mammal species and populations exceed a general threshold level of concern of 1 part-per-million (ppm), but a clear evidence of a POP/OHC-related stress in these populations remains to be confirmed. There remains minimal evidence that OHCs are having widespread effects on the health of Arctic organisms, with the possible exception of East Greenland and Svalbard polar bears and Svalbard glaucous gulls. However, the true (if any real) effects of POPs in Arctic wildlife have to be put into the context of other environmental, ecological and physiological stressors (both anthropogenic and natural) that render an overall complex picture. For instance, seasonal changes in food intake and corresponding cycles of fattening and emaciation seen in Arctic animals can modify contaminant tissue distribution and toxicokinetics (contaminant deposition, metabolism and depuration). Also, other factors, including impact of climate change (seasonal ice and temperature changes, and connection to food web changes, nutrition, etc. in exposed biota), disease, species invasion and the connection to disease resistance will impact toxicant exposure. Overall, further research and better understanding of POP/OHC impact on animal performance in Arctic biota are recommended. Regardless, it could be argued that Arctic wildlife and fish at the highest potential risk of POP/OHC exposure and mediated effects are East Greenland, Svalbard and (West and South) Hudson Bay polar bears, Alaskan and Northern Norway killer whales, several species of gulls and other seabirds from the Svalbard area, Northern Norway, East Greenland, the Kara Sea and/or the Canadian central high Arctic, East Greenland ringed seal and a few populations of Arctic charr and Greenland shark.
Environmental conditions affect growth and development and, through developmental plasticity, create phenotypic variation. In suboptimal conditions current survival is traded-off against development. Corticosterone, the main glucocorticoid in birds, may be involved in the reallocation of energy from growth to maintenance, but its effect on growth has rarely been investigated in altricial birds under natural conditions in the wild. In free-living Eurasian kestrel Falco tinnunculus nestlings, we artificially elevated corticosterone to stress-induced levels over 2-3 days in the middle of the nestling stage by implanting biodegradable implants, controlling the treatment with a placebo group. We measured the length of primary feather 8, hand length, tarsus length, body mass and subcutaneous fat stores from day 10 to 25. During corticosterone elevation, primary growth of cort-nestlings was significantly reduced to 71% of placebo-nestlings, hand and tarsus growth were significantly reduced to 14% and 26% of placebo-nestlings, respectively, and body mass increase stopped, while subcutaneous fat-store growth was not affected. Over the following 5 days, primary growth was still significantly suppressed to 84% of placebo-nestlings, while hand, tarsus and body mass growth were back to normal. During the subsequent 4 days, cort-nestlings partly compensated for the lag in body mass by significantly accelerating the body mass increase compared with placebo-nestlings. Before fledging, primary length was 10% shorter, hand and tarsus 5% and 4% shorter and body mass 8.5% lower in cort-nestlings than in placebo-nestlings, while fat score did not differ significantly between the two groups. Thus, we have shown that in free-living, altricial nestlings a few days of elevated plasma corticosterone levels alone, without food restriction, suppressed growth and this could only partly be compensated for afterwards. Feather, bone and body mass growth were reduced to different degrees, indicating that corticosterone had a differential effect on different structures. This demonstrates that corticosterone is probably involved in the control of developmental plasticity.
Birds are difficult to sex. Nestlings rarely show sex-linked morphology and we estimate that adult females appear identical to males in over 50% of the world's bird species. This problem can hinder both evolutionary studies and human-assisted breeding of birds. DNA-based sex identification provides a solution. We describe a test based on two conserved CHD (chromo-helicase-DNA-binding) genes that are located on the avian sex chromosomes of all birds, with the possible exception of the ratites (ostriches, etc.; Struthioniformes). The CHD-W gene is located on the W chromosome; therefore it is unique to females. The other gene, CHD-Z, is found on the Z chromosome and therefore occurs in both sexes (female, ZW; male, ZZ). The test employs PCR with a single set of primers. It amplifies homologous sections of both genes and incorporates introns whose lengths usually differ. When examined on a gel there is a single CHD-Z band in males but females have a second, distinctive CHD-W band.
The levels of several different persistent organochlorines (OCs) in Black Guillemots Cepphus grylle, collected during the summers of 1976-1996 at Breioafjörour in W-Iceland, were investigated. The levels of about 40 different organochlorines (PCBs, DDTs, chlordanes, toxaphenes, HCH, HCB) were compared with respect to age, sex, fat content, and year of collection. The levels of PCBs correlated very closely with those of DDE, indicating long-range transport as the major source of these contaminants in Iceland, with the ratio PCBs/DDE mostly in the range of 2-5. Unlike the Gyrfalcon Falco rusticolus, the organochlorine levels did not seem to accumulate substantially with age, neither in males nor females. The variation in the levels of OCs at the age of 2 years was even greater than the variation in OC levels over an age range of 12 years. In immature birds the levels of PCBs, DDE, HCB and beta-HCH declined very slowly (T(1/2) from 12 to 20 years) over the years 1976-1996, whereas the levels of alpha-HCH and p,p'-DDT declined much faster. The levels of trans-nonachlor, alpha-chlordane, gamma-chlordane, oxychlordane, and toxaphene did not correlate with the year of collection. As the Black Guillemot is mostly a resident seabird, feeding mainly on small fish and invertebrates, this investigation should give a good indication of the temporal trends of organochlorine pollution at Breioafjörour, Iceland, during this 20 year period and is likely to reflect baseline trends in the marine environment of the North-Atlantic Ocean.
Due to their high trophic level, raptor species may serve as important indicators of environmental contamination by heavy metals. This study was conducted to determine if the habitat of the black kite (Milvus migrans) is contaminated by heavy metals and arsenic and to assess the degree and type of exposure that may be present. For this purpose, this study was conducted on a group of captive birds (n = 12) and on a group of free-living birds admitted to two wildlife rehabilitation centers (n = 31). Blood samples were taken for analysis of arsenic (As), mercury (Hg) and lead (Pb) concentrations by inductively coupled plasma mass spectrometry (ICP-MS). Captive birds had the lowest blood concentrations for all toxic elements examined, but significant differences from the concentrations found in free-living birds were only observed for Hg and Pb (p < 0.01). Arsenic concentrations were almost three times higher in free-living birds (4.521 ± 5.695 µg/dl) then in captive birds (1.566 ± 0.753 µg/dl). In all the samples of captive birds' mercury was not detected, while in free-living birds we observed a concentration of 7.493 ± 8.464 µg/dl (p < 0.01). Regarding lead, we observed a concentration almost four-fold higher in free-living birds (19.430 ± 29.294 µg/dl) then in captive birds (4.449 ± 1.987 µg/dl) (p < 0.01). Therefore, available sources of Pb and Hg seem to be present in the habitat of the black kite.
The aim of the present work was to comparatively assess the occurrence and impact of persistent organic pollutants (POPs) in nine natural and national parks from Spain and Portugal using gull eggs (Larus michahellis and L. audouinii) as bioindicators of environmental contamination. Sampling was performed during the breeding season of 2016. Compounds studied include polychlorinated biphenyls (PCBs), organochlorinated pesticides (OC pesticides), perfluorooctane sulfonic acid (PFOS) and polybrominated diphenyl ethers (PBDEs), and were analyzed using mass spectrometric based techniques. The results showed a high contamination by PCBs in all colonies, with total levels ranging from 59 to 1278ng/g wet weight (ww), despite their use is not currently authorized. OC pesticides were also present in all colonies, with a high incidence of 4,4'-DDE in gull eggs at levels up to 218±50ng/g ww in L. michahellis and 760±412ng/g ww in L. audouinii from the Ebro Delta natural park. PBDEs and PFOS were also detected at levels up to 91.7±21.3ng/g ww, which can be attributed to a more recent use. Except for PBDEs, the POP levels in eggs from L. audouinii were higher than in L. michahellis, presumably associated to the fish-based diet of the former. Finally, the effect of POP levels on eggshell parameters (volume, eggshell thickness and desiccation index) were investigated for each colony and gull species in order to evaluate the egg viability and, therefore, the reproduction success.
In birds, integrated levels of corticosterone (CORT) measured in feathers (CORTf) allow us to make inferences on past levels of stress demands. It has been suggested that levels of CORTf track carry-over effects across seasons. Nevertheless, our understanding of how this measure can be used to assess future health status is far from complete. In this study, we aimed to investigate whether CORT deposited in feathers over the moulting period was related to subsequent mortality and health status in wild raptors admitted to rehabilitation centres. Thirty-four Eurasian Sparrowhawks (Accipiter nisus) admitted during the non-moulting period were sampled. Body condition (BC) was used as an indicator of health status to classify individuals’ health as good, poor or cachexia depending on their pectoral muscle score. Mortality was recorded over the non-moulting period. Other potential sources of CORTf variation were assessed, such as sex, age and feather type, primary or body covert feathers. While CORTf did not vary with age or sex, significant differences were found between primary and body feathers, highlighting the importance of sampling the same feather type. Our results also revealed that birds in poor BC showed higher CORTf levels than individuals in good condition; however, CORTf levels in cachectic birds did not differ from those in good condition. This finding suggests caution when assuming that only high CORTf levels represent individuals in poor condition, and limits the utility of CORTf for the prediction of BC. The present study also showed that individuals which died following admission had higher CORTf levels than individuals which survived, suggesting the potential utility of CORTf as a metric for the study of subsequent mortality.
After dealing with the initial fallout from the collapse of the Soviet Union and the disappearance of the "Iron Curtain", particularly in the Balkans and even today in Ukraine, the European Union now finds itself directly affected by proliferating conflicts and disorder on its south-eastern flank. With civil war in Syria, a jihadist offensive in Iraq and the possible emergence of an autonomous Kurdistan, the Middle East remains a powder keg. The roots of this situation go back into European history, and the way it develops in the future will have consequences for the "old continent" in terms of politics, economics and migration. This month, Jean-François Drevet devotes his column to the various Middle-Eastern hotspots that have significant implications for Ell foreign policy. As he stresses, there is hardly any other option than to intervene, but it is not easy either to say what form such intervention should take to stem the current tide of troubles or to agree on effective neighbourhood policies in such a context.
The present study investigated the current-use brominated flame retardants (BFRs) tetrabromobisphenol A (TBBPA) and hexabromocyclododecane (HBCD), simultaneously with legacy polybrominated diphenyl ethers (PBDEs), in Barn Owls (Tyto alba) collected from two regions with a contrasting degree of urbanisation and vicinity to point sources (Flanders in Belgium versus Normandy in France). Both tissues (muscle, liver, adipose and preen gland) and feathers (primary, tail and body feathers) showed elevated HBCD concentrations in Flanders, close to Europe's sole HBCD production plant in the Netherlands, and identified Normandy as a historical source region for PBDEs. In sharp contrast, the reactive BFR TBBPA bioaccumulated poorly (2.3%) in tissue samples, but was present in 96% of all body feather samples (0.36-7.07ngg-1dw), equally in both regions. PBDE concentrations in tissues (7.46-903ngg-1lw) were considerably lower in the investigated Flemish Barn Owls, collected in 2008/2009, compared to specimens collected in 2003/2004 (46-11,000ngg-1lw), possibly suggesting the effectiveness of the 2004 European ban of Penta- and Octa-BDE mixtures. Feathers showed a similar trend and additionally exhibited HBCD concentrations (0.02-333ngg-1dw) surpassing those of PBDEs (0.50-10.4ngg-1dw). While body feathers were a reliable matrix to predict both internal PBDE (0.21≤R2≤0.67) and HBCD body burdens (0.20≤R2≤0.37), the suitability of primary and tail feathers appeared to be confounded by external contamination and moult. In conclusion, the present study clearly showed that the reactive versus additive use of BFRs results in contrasting exposure scenarios in a species higher up the food chain, and therefore may have profound implications for environmental health. In addition, the presented results extend the promising use of feathers as a non-destructive sampling strategy for current-use BFRs, and show that birds of prey are valid early-warning systems for environmental contamination.
Lindane [γ-hexachlorocyclohexane (γ-HCH)] is an organochlorine pesticide with toxic effects on humans. It is bioaccumulative and can remain in soils for long periods, and although its use for crop spraying was banned in France in 1998, it is possible that residues from before this time remain in the soil. The RMQS soil monitoring network consists of soil samples from 2200 sites on a 16km regular grid across France, collected between 2002 and 2009. We use 726 measurements of the Lindane concentration in these samples to (i) investigate the main explanatory factors for its spatial distribution across France, and (ii) map this distribution. Geostatistics provides an appropriate framework to analyze our spatial dataset, though two issues regarding the data are worth special consideration: first, the harmonization of two subsets of the data (which were analyzed using different measurement processes), and second, the large proportion of data from one of these subsets that fell below a limit of quantification. We deal with these issues using recent methodological developments in geostatistics. Results demonstrate the importance of land use and rainfall for explaining part of the variability of Lindane across France: land use due to the past direct input of Lindane on cropland and its subsequent persistence in the soil, and rainfall due to the re-deposition of volatilized Lindane. Maps show the concentrations to be generally largest in the north and northwest of France, areas of more intensive agricultural land. We also compare levels to some contamination thresholds taken from the literature, and present maps showing the probability of Lindane concentrations exceeding these thresholds across France. These maps could be used as guidelines for deciding which areas require further sampling before some possible remediation strategy could be applied.
Although experimental studies show that organochlorines (OC) can affect bird behaviour, field assessments are invariably confounded by ecological differences between contaminated and uncontaminated sites. The behaviour of individual birds in the field has rarely been related to the contaminant burden.
We examined individual patterns of incubation and nest‐site attentiveness in relation to OC burden, measured as polychlorinated biphenyl (PCB) concentration in the blood, of 27 glaucous gulls Larus hyperboreus in two breeding areas at Bear Island, in the north‐eastern Atlantic.
Blood PCB concentrations ranged from 52 ng g ‐1 to 1079 ng g ‐1 (wet weight). There were significant differences between the two breeding areas, and females had significantly lower concentrations than males.
Gull behaviour differed significantly between breeding areas and sexes independently of PCB. Females incubated more than males (54% vs. 46%) but spent more time away from the nest site than males, both overall (23% vs. 12%) and when not incubating (50% vs. 21%). They were also absent for longer periods (4·5 vs. 2·8 h). Moreover, length of incubation bouts (6·4 vs. 4·4 h), the amount of time absent from the nest site when not incubating (51% vs. 25%) and length of absences (5·6 vs. 1·8 h) differed between breeding areas, probably due to different feeding specializations.
After controlling for these area and sex effects, the proportion of time absent from the nest site when not incubating, and the number of absences, were both significantly related to blood concentration of PCB.
Increased absence from the nest site in individual glaucous gulls with high blood concentrations of OC suggests effects on reproductive behaviour. We speculate that endocrine disruption or neurological effects might be involved, leading to increased energetic costs during incubation and reduced reproductive output.
Summary • Stress has pervasive consequences for the well-being of animals. Currently, understanding how individuals cope with stressors is typically accomplished via short-term quantification of blood glucocorticoids released after activation of the hypothalamic–pituitary–adrenal (HPA) axis. • We investigated whether the amount of corticosterone (CORT) deposited in growing feathers provides a long-term, integrated measure of HPA activity in birds using captive red-legged partridges Alectoris rufa as a model species. • We examined CORT levels in primary feathers induced to grow at the same time as stress series were performed with a capture and restraint protocol. Plasma CORT titres after stress-induced stimulation, but not baseline values, correlated with feather CORT. Feather levels showed the same pattern as plasma of decline across the breeding season, but more severely. • For females, CORT in naturally moulted flank feathers was highly and positively correlated with the number of eggs laid in the previous few months, but not clutch size of the following year. For males, the amount of black on a feather, known to be a social signal, was positively correlated with its CORT level. • The analysis of feather CORT is a novel methodology that allows for meaningful interpretations of how individuals respond to environmental perturbations and adjust to life-history stages. • The analysis of feather hormones has the unique advantages of allowing for experimentation and sampling at any time of the year with minimal investigator-induced impacts and artefacts, and shows the HPA activity of an individual with a flexible time frame from days to months depending on the length of time taken to grow the feather. As this technique can be applied to living or dead birds, or feathers picked up after moult, it provides the ultimate non-invasive physiological measure of considerable benefit in terms of animal welfare and sampling effort.
To circumvent difficulties associated with monitoring adult predatory birds, we investigated the feasibility of different non-destructive strategies for nestling white-tailed eagles (Haliaeetus albicilla). We were able to quantify polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs) and organochlorinated pesticides (OCPs) in body feathers (16.92, 3.37 and 7.81ngg(-1) dw, respectively), blood plasma (8.37, 0.32 and 5.22ngmL(-1) ww, respectively), and preen oil (1157.95, 30.92 and 440.74ngg(-1) ww, respectively) of all nestlings (N=14). Strong significant correlations between blood plasma and preen oil concentrations (0.565≤r≤0.801; P<0.05) indicate that preen oil levels closely reflect the internal state of contamination. We found fewer significant correlations between body feather and blood plasma concentrations, which were almost exclusively between PCB concentrations (0.554≤r≤0.737; P<0.05). These results differ from a previous study on younger nestlings, and may indicate that the nestlings studied here, ready to fledge the nest, were possibly undergoing certain physiological changes that may have confounded the use of body feathers as biomonitor matrix. Finally, we provide an integrated discussion on the use of body feathers and preen oil as non-destructive biomonitor strategies for nestling predatory birds.
We investigated the variation in concentrations and profiles of various classes of organohalogenated compounds (OHCs) in different feather types, muscle tissue and preen oil from 15 white-tailed eagle (Haliaeetus albicilla) carcasses from Greenland. The influence of moult patterns and potential external contamination onto the feather surface was examined, while the present study is also the first to investigate the use of body feathers for OHC monitoring. Concentrations of sum polychlorinated biphenyls (PCBs) in feathers from white tailed eagles ranged from 2.3 ng/g in a primary wing feather to 4200 ng/g in body feathers. Using 300 mg of body feathers, almost 50 different OHCs could be quantified and median concentrations in body feathers were 10 fold higher than concentrations in tail feathers (rectrices) or primary wing feathers. Body feathers could be very useful for biomonitoring taking into account their easy sampling, short preparation time and high levels of OHCs. In addition, the effects of confounding variables such as feather size, moult and age are also minimised using body feathers. Correlations with concentrations in muscle tissue and preen oil were high and significant for all feather types (r ranging from 0.81 to 0.87 for sum PCBs). Significant differences in concentrations and profiles of OHCs were found between different primary feathers, indicating that the accumulation of OHCs in feathers varies over the moulting period (maximum three years). Washing of feathers with an organic solvent (acetone) resulted in a significant decrease in the measured concentrations of OHCs in feathers. However, our results indicated that preen oil is probably not the only contributor to the external contamination that can be removed by washing with acetone. Possibly dust and other particles may be of importance and may be sticking to the preened feathers. Rectrices washed only with water showed high and significant correlations with concentrations in muscle and preen oil as well. Washing with acetone therefore does not seem to be of great influence when relating to internal tissue concentrations. We recommend washing feathers only with distilled water in order to remove dirt and dust particles before analysis.
Female common eiders (Somateria mollissima) starve during the nesting stage and may loose 30-45% of their initial body mass, mostly through lipid mobilization. In this study, the effects of fasting on the blood concentrations of three lipid-soluble organochlorines (OCs: polychlorinated biphenyl [PCB]-153; 1-dichloro-2,2-bis (p-chlorophenyl) ethylene [p,p'-DDE]; and hexachlorobenzene [HCB]) were examined in eiders breeding in the high Arctic. Blood samples were taken from females (n=47) at day 5 and day 20 of the incubation period. The mean wet weight concentrations of PCB-153 and p,p'-DDE increased strongly between day 5 and day 20 (3.6 and 8.2-fold, respectively), while HCB increased less (1.7-fold). There was a strong negative association between daily increase in PCB-153 and clutch size, and a weaker relationship for p,p'-DDE, suggesting that maternal transfer to the eggs is a significant pathway of elimination of OCs in eiders. Moreover, poor body condition (body mass controlled for body size) late in the incubation period was associated with strong daily increase of both p,p'-DDE and PCB-153, which may suggest that the release of these compounds increases when lipid reserves become depleted. For HCB, the increase was mainly associated with increase in blood lipid concentrations, and weakly to the amount of burned lipids. The causes for the differences between the compounds are, however, poorly understood. Although the absolute levels of OCs in eiders were relatively low, their rapid build up during incubation is worrying as it coincides with poor body condition and weakened immune systems.
Unpredictable changes in the environment stimulate the avian hypothalamo-pituitary-adrenal axis to produce corticosterone, which induces behavioural and metabolic changes that enhance survival in the face of adverse environmental conditions. In addition to profound environmental perturbations, such as severe weather conditions and unpredictable food shortages, many Arctic-breeding birds are also confronted with chronic exposure to persistent organic pollutants (POPs), some of which are known to disrupt endocrine processes. This study investigated the adrenocortical function of a top predator in the Arctic marine environment, the glaucous gull (Larus hyperboreus). High concentrations of organochlorines, brominated flame retardants and metabolically-derived products in blood plasma of incubating glaucous gulls were associated with high baseline corticosterone concentrations in both sexes and a reduced stress response in males. Contaminant-related changes in corticosterone concentration occurred over and above differences in body condition and seasonal variation. Chronically high corticosterone concentrations and/or a compromised adrenocortical response to stress can have negative effects on the health of an individual. The results of the present study suggest that exposure to POPs may increase the vulnerability of glaucous gulls to environmental stressors and thus could potentially compromise their ability to adapt to the rapidly changing environmental conditions associated with climate change that are currently seen in the Arctic.
Feathers have recently been shown to be potentially useful non-destructive biomonitoring tools for organic pollutants. However, the suitability of feathers to monitor regional variations in contamination has not been investigated until now. Here concentrations of organic pollutants were compared in feathers of common magpies (Pica pica) between urban and rural areas in Flanders, Belgium. The results showed that concentrations of p,p'-dichlorodiphenyldichloroethylene (DDE) were significantly higher in the rural areas (rural: 12-140 ng/g feather, urban: 1.1-7.2 ng/g feather), while polychlorinated biphenyls (PCBs) were significantly more available in an urban environment (sum PCBs--rural: 2.9-22 ng/g feather, urban: 41-240 ng/g feather). This pattern agrees with previous studies using other tissues than feathers as a biomonitoring tool. In addition, differences in PCBs and PBDEs profiles were found with lower halogenated congeners being more prominent in the urban areas in comparison to the rural areas. In summary, feathers seem to reflect regional variations in contamination, which strengthens their usefulness as a non-destructive biomonitor for organic pollutants.
In the present study, we have (i) examined the biological effects of repeated immobilization stress, and (ii) tested the hypothesis that the adrenal steroid hormone dehydroepiandrosterone (DHEA) is an anti-stress hormone, using male Sprague-Dawley rats. Rats (N = 6) were divided into the following four groups: (i) control, (ii) repeated immobilization stress (2 hr daily, for 60 days), (iii) repeated immobilization stress (2 hr daily, for 60 days) plus daily i.p. administration of 5 mg DHEA/0.1 mL DMSO, and (i.v.) daily i.p. administration of 5 mg DHEA/0.1 mL DMSO alone. Results obtained showed that repeated immobilization stress resulted in a significant (25%) inhibition in body weight gain, a significant increase in adrenal weight, an increase in glucocorticoid receptor (GR) in the liver, thymus, and spleen, decreased plasma triglyceride levels, and increased lipid peroxidation in the liver and heart as compared with control unstressed animals. Interestingly, DHEA administration resulted in a significant reversal in stress-induced inhibition in body weight gain, adrenal weight, GR levels in liver, thymus, and spleen, and lipid peroxidation levels in the liver and heart. In addition, animals treated with DHEA alone without stress showed a significant (15%) inhibition in body weight gain and an almost 60% decrease in plasma triglyceride levels as compared with control unstressed animals. It is concluded that DHEA acts as an anti-stress hormone in rats, as shown in its antagonizing the effects of repeated immobilization stress on total body weight, adrenal weight, GR levels, and free radical generation.
Stress is commonly associated with a variety of psychiatric conditions, including major depression, and with chronic medical conditions, including diabetes and insulin resistance. Whether stress causes these conditions is uncertain, but plausible mechanisms exist by which such effects might occur. To the extent stress-induced hormonal alterations (e.g., chronically elevated cortisol levels and lowered dehydroepiandrosterone [DHEA] levels) contribute to psychiatric and medical disease states, manipulations that normalize these hormonal aberrations should prove therapeutic. In this review, we discuss mechanisms by which hormonal imbalance (discussed in the frameworks of "allostatic load" and "anabolic balance") might contribute to illness. We then review certain clinical manifestations of such hormonal imbalances and discuss pharmacological and behavioural treatment strategies aimed at normalizing hormonal output and lessening psychiatric and physical pathology.
In response to a stressor, physiological changes are set into motion to help an individual cope with the stressor. However, chronic activation of these stress responses, which include the hypothalamic–pituitary–adrenal axis and the sympathetic–adrenal–medullary axis, results in chronic production of glucocorticoid hormones and catecholamines. Glucocorticoid receptors expressed on a variety of immune cells bind cortisol and interfere with the function of NF-κB, which regulates the activity of cytokine-producing immune cells. Adrenergic receptors bind epinephrine and norepinephrine and activate the cAMP response element binding protein, inducing the transcription of genes encoding for a variety of cytokines. The changes in gene expression mediated by glucocorticoid hormones and catecholamines can dysregulate immune function. There is now good evidence (in animal and human studies) that the magnitude of stress-associated immune dysregulation is large enough to have health implications.
Living organisms have regular patterns and routines that involve obtaining food and carrying out life history stages such as breeding, migrating, molting, and hibernating. The acquisition, utilization, and storage of energy reserves (and other resources) are critical to lifetime reproductive success. There are also responses to predictable changes, e.g., seasonal, and unpredictable challenges, i.e., storms and natural disasters. Social organization in many populations provides advantages through cooperation in providing basic necessities and beneficial social support. But there are disadvantages owing to conflict in social hierarchies and competition for resources. Here we discuss the concept of allostasis, maintaining stability through change, as a fundamental process through which organisms actively adjust to both predictable and unpredictable events. Allostatic load refers to the cumulative cost to the body of allostasis, with allostatic overload being a state in which serious pathophysiology can occur. Using the balance between energy input and expenditure as the basis for applying the concept of allostasis, we propose two types of allostatic overload. Type 1 allostatic overload occurs when energy demand exceeds supply, resulting in activation of the emergency life history stage. This serves to direct the animal away from normal life history stages into a survival mode that decreases allostatic load and regains positive energy balance. The normal life cycle can be resumed when the perturbation passes. Type 2 allostatic overload begins when there is sufficient or even excess energy consumption accompanied by social conflict and other types of social dysfunction. The latter is the case in human society and certain situations affecting animals in captivity. In all cases, secretion of glucocorticosteroids and activity of other mediators of allostasis such as the autonomic nervous system, CNS neurotransmitters, and inflammatory cytokines wax and wane with allostatic load. If allostatic load is chronically high, then pathologies develop. Type 2 allostatic overload does not trigger an escape response, and can only be counteracted through learning and changes in the social structure.
Keratinous tissues of mammals and humans, such as hair, have been used to determine the exposure to polychlorinated biphenyls (PCBs) and organochlorine pesticides. In the present study, we investigated the accumulation of persistent organic pollutants (POPs; PCBs, p,p'-DDT, p,p'-dichlorodiphenyldichloroethane [DDD], p,p'-dichlorodiphenyldichloroethylene [DDE], hexachlorobenzene [HCB], oxychlordane, trans-nonachlor, polybrominated diphenyl ethers, and polybrominated biphenyls [PBBs]) in feathers of the great tit (Parus major). The accumulation of POPs in feathers and fat samples of 27 adult great tits collected in April 2000 and December 2002 was compared with regard to possible temporal and spatial differences. Polybrominated diphenyl ethers, PBBs, trans-nonachlor, and HCB could not be quantified in feathers. Most PCB congeners and DDTs (p,p'-DDE, p,p'-DDD, and p,p'-DDT) could be determined in feathers, although concentrations in feathers were markedly lower (sigmaPCB concentration range, 28.2-87.1 ng/g) than concentrations in fat (sigmaPCB concentration range, 1244-10074 ng/g). Feathers had relatively higher levels of low-chlorinated PCBs (tetra- and pentachlorinated biphenyls) and p,p'-DDD compared to levels in fat, presumably reflecting levels in blood. Persistent organic pollutant concentrations did not increase with the age of the feather, suggesting that exogenous or aerial depositions of POPs onto the feather surface had no, or only minimal, influence on levels in feathers. For almost all compounds studied, POPs in feathers and fat were significantly positively correlated in samples collected during the breeding season but not in samples collected during the winter. This temporal difference may have been caused by seasonal changes in lipid reserves. Although further research is required, feathers appear to be a promising new, nondestructive biomonitor for PCBs and DDTs in avian wildlife.