Periodic Reporting for period 1 - POPHEALTH (Understanding the origins of persistent organic pollutants (POPs) exposure in wild migratory birds and their health consequences)
Reporting period: 2021-07-01 to 2023-06-30
Anthropogenic pollution, which is the introduction in natural environments of contaminants that can alter the health, reproduction and survival of free living organisms. Consequently, there is increasing concerns about the sources of exposure to persistent organic pollutants (POPs) and about their consequences on human health and on natural populations and ecosystems. POPs are known to persist in the environment and to bioaccumulate through the lifetime of organisms as well as to increase in concentration with each successive step in the food chain (biomagnification), therefore top predators as birds are used as bioindicators. Moreover, migratory animals as birds don’t have borders, and hence, one growing issue is that European breeding species may also become exposed to POPs when visiting non-European ecosystems, such as during migration to Africa where many POPs banned in the EU are still used there as pesticides. POPs can be measured in different tissues (e.g. feathers, preen oil, and blood), although it is less clear to which extent these measure. For instance, blood samples are expected to reflect rather recent exposure to POPs. Currently, no study has addressed how POPs accumulate in different tissues using repeated measures from the same individuals, and as such explore what types of samples are best describing POPs bioaccumulation. Therefore, by applying in a European migratory bird species (the Alpine swift, Tachymarptis melba) new tracking technologies and state-of-the-art physiological and biomolecular tools, the overarching aims of POPHEALTH are to improve our understanding of how wintering and breeding areas influence the exposure to POPs in the wild, to validate which tissue best describe exposure to POPs in birds, and to provide novel insights on the health and fitness consequences of exposure to POPs in a long-term perspective accounting for sex differences and senescence. POPHEALTH is likely to be of great interest for the general public, scientific community, policy-makers and NGOs. Results will improve sustainable development policies for nature conservation, novel bio-logger devices and harnesses designs for birds will lead to scientific and innovative European excellence, and the novel approach accounting for sex-specific and senescence status will reinterpret wildlife physiological ecotoxicology.
POPHEALTH found effects of POPs in Alpine swifts accounting for sex differences and senescence (i.e. controlling for the confounding effect of age on telomere length and rate of telomere erosion over seasons), traits so far unstudied in detail in natural bird populations exposed to POPs. An amount of 45 POPs were analyzed in preen oil samples of Apline swifts breeding in Switzerland, specifically, 26 organochlorine pesticides (OCPs: 4 HCH, 6 DDTs, HCB, 4 CHLs, 9 HCCPDs, 2 dicofols) and 19 Polychlorinated biphenyls (PCBs), and a maximum of 224 blood samples from 169 adults sampled between 2017-2021 were used to assess comprehensive markers of health.
Our repeated preen oil sampling (2016-2020) of the same individual over at least 2 different years allowed us to control for high between-individual variation while studying exposure across and within years. In summary, neither wintering grounds nor urbanization surrounding breeding areas showed strong contribution to POPs’ exposure, thus other overlooked factors as agricultural transmission of pollutants towards lower food web levels could be more explicative. Time of year and sex do not seem to be so important either, but age showed some signs of POP-specific bioaccumulation (total chlordane and HCB) and POP-specific disappearance (Hexa- and Penta-PCBs) on individuals.
As a summary of the health and fitness consequences we will describe our results in telomere dynamics. Telomeres are repeated non-coding DNA sequencing that protect the end of eukaryotic chromosomes and its preservation has been associated to survival and senescence and thus, age is a main contributor of the variation of telomere length. We defined non-senescent and senescent individuals as < or ≥ 9 years old, respectively. Then, we were able to study how relationships between POPs and telomere dynamics differed in those groups because stressors as pollution may disrupt the rate at which telomeres are eroded over time, resulting in faster aging with likely consequences on reproduction and survival. Our results showed that the effects of POPs on telomere dynamics are age- and sex-specific, and these effects are themselves POP-specific. POPs were associated to elongation of telomeres rather than erosion, although depending on sex and senescent status. Higher exposures of total PCBs, total Hexa-PCBs, and total Hepta-PCBs elongated telomeres in females and senescent males, but eroded telomeres in pre-senescent male. This means that females and senescent males have different strategies than pre-senescent males when facing stressors as pollution in relation with aging. Most likely, the former individuals upregulate telomerase activity (a reverse transcriptase enzyme involved in telomere maintenance) to elongate telomeres when exposed to specific PCBs.
Our repeated preen oil sampling (2016-2020) of the same individual over at least 2 different years allowed us to control for high between-individual variation while studying exposure across and within years. In summary, neither wintering grounds nor urbanization surrounding breeding areas showed strong contribution to POPs’ exposure, thus other overlooked factors as agricultural transmission of pollutants towards lower food web levels could be more explicative. Time of year and sex do not seem to be so important either, but age showed some signs of POP-specific bioaccumulation (total chlordane and HCB) and POP-specific disappearance (Hexa- and Penta-PCBs) on individuals.
As a summary of the health and fitness consequences we will describe our results in telomere dynamics. Telomeres are repeated non-coding DNA sequencing that protect the end of eukaryotic chromosomes and its preservation has been associated to survival and senescence and thus, age is a main contributor of the variation of telomere length. We defined non-senescent and senescent individuals as < or ≥ 9 years old, respectively. Then, we were able to study how relationships between POPs and telomere dynamics differed in those groups because stressors as pollution may disrupt the rate at which telomeres are eroded over time, resulting in faster aging with likely consequences on reproduction and survival. Our results showed that the effects of POPs on telomere dynamics are age- and sex-specific, and these effects are themselves POP-specific. POPs were associated to elongation of telomeres rather than erosion, although depending on sex and senescent status. Higher exposures of total PCBs, total Hexa-PCBs, and total Hepta-PCBs elongated telomeres in females and senescent males, but eroded telomeres in pre-senescent male. This means that females and senescent males have different strategies than pre-senescent males when facing stressors as pollution in relation with aging. Most likely, the former individuals upregulate telomerase activity (a reverse transcriptase enzyme involved in telomere maintenance) to elongate telomeres when exposed to specific PCBs.
The most innovative aspect of POPHEALTH is that it accounted for sex-specific and senescence status differences, traits previously unstudied in natural bird populations. The scientific community will be able to benefit from it and extend the impact of our results beyond our work. The novelty of our research also falls on the importance of our study system, one of the few long-term monitoring with detailed knowledge on the age and reproductive success of individuals in the wild. Results can also be used to improve sustainability issues, and to better manage the environment and the European policy resulting in great benefits for society. The use and design of state-of-the-art biologging devices (GLS) by collaborators at the Swiss Ornithological Institute resulted in detailed movement information of Alpine swifts in Africa, allowing us to test the contribution of wintering or breeding areas on levels of exposure to POPs. This approach is novel in itself and contributes to the state of the art of wildlife ecotoxicology.
This project also developed candidate’s management skills, in terms of financial and human resources, improved his written and spoken communication skills in English and French, and strengthened his meeting organization skills by organizing "AGE meetings". Meetings to discuss about results, ideas, and projects with the host team and Canadian collaborators. His supervisory and teaching skills has been enhanced by incorporating PhD students of the supervisory team and by personally training other PhD fellows with his protocols, what strengthened research axis at the host institute (ADAGE team and the French Polar Institute program, IPEV 119) and promoted new strategic and durable collaborations. He also created external side-project collaborations, for example, with L Ilahiane and I Pellegrino (University of Piemonte Orientale, Italy) to look for haemosporidian infection in swift (Parasitol. Res. 2023 Aug; 122(8):1787-1794; doi: 10.1007/s00436-023-07874-8). The career development plan has been successful because the candidate has already secured two post-doctoral research talent positions in Spain (Beatriu de Pinós, 150k€; and CDEIGENT programme, 340k€).
This project also developed candidate’s management skills, in terms of financial and human resources, improved his written and spoken communication skills in English and French, and strengthened his meeting organization skills by organizing "AGE meetings". Meetings to discuss about results, ideas, and projects with the host team and Canadian collaborators. His supervisory and teaching skills has been enhanced by incorporating PhD students of the supervisory team and by personally training other PhD fellows with his protocols, what strengthened research axis at the host institute (ADAGE team and the French Polar Institute program, IPEV 119) and promoted new strategic and durable collaborations. He also created external side-project collaborations, for example, with L Ilahiane and I Pellegrino (University of Piemonte Orientale, Italy) to look for haemosporidian infection in swift (Parasitol. Res. 2023 Aug; 122(8):1787-1794; doi: 10.1007/s00436-023-07874-8). The career development plan has been successful because the candidate has already secured two post-doctoral research talent positions in Spain (Beatriu de Pinós, 150k€; and CDEIGENT programme, 340k€).