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Responses to reduced industrial metal emissions: An ecotoxicological study on Pied Flycatcher (Ficedula hypoleuca, Aves)
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
2010 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Metals have been used by humans for thousands of years, and this has resulted in increased concentrations in the biosphere. The environment around point-sources, such as mines and smelters, are of particular concern, as metals may accumulate to high concentrations, and potentially reach levels toxic to the local flora and fauna. This thesis focuses on the effects on pied flycatcher populations of two such point-sources, a lead mine and enrichment plant, and a sulfide ore smelter. Mining activities at the lead mine ceased in 2001 and pied flycatcher populations were assessed before and after the closure. At the sulfide ore smelter, pied flycatchers were studied during the 1980s. Since then, the metal emissions to air from the smelter (e.g. arsenic, cadmium, copper, mercury, lead and zinc) have been greatly reduced (by 93 – 99%).

Pied flycatchers from these two contaminated environments differed in their responses to reduced atmospheric deposition. At the mine site, nestling responses reflected the reduced atmospheric deposition and less lead accumulated in their tissues. However, lead levels were still high enough to cause negative effects on blood status (δ-aminolevulinic acid dehydratase [ALAD], hemoglobin [Hb], hematocrit [ht], and mean cell hemoglobin concentration) and reproduction (reduced clutch size, increased mortality and reduced breeding success), as was observed when the mine was in operation. Along the pollution gradient away from the smelter, nestling concentrations reflected the metal load in the soil pool, accumulating over time, rather than the atmospheric deposition. This resulted in only a minor response to decreased metal deposition (slightly reduced liver lead concentrations at 3.5 – 90 km from the smelter). This suggests that in environments with highly polluted soils, decreased inputs of atmospheric metal deposition have only minor impacts, and recovery from contamination should not be expected within decades.

The high metal concentrations in the vicinity of the smelter contributed to poorer blood status (ALAD, Hb and ht), induced oxidative damage and defenses, and decreased reproduction (increased mortality and reduced breeding success). There were only minor improvements in blood and reproductive variables at 3.5 km from the smelter.

Abstract [sv]

Metaller är grundämnen som inte kan bildas eller förstöras av människan. De förekommer i mineraler i berggrunden och finns överallt på jorden. Människans användning av metaller har dock medfört att de återfinns i högre halter i miljön än de annars skulle gjort.

Trots att metallerna kan spridas och transporteras långa sträckor med luftmassorna, är det främst kring källorna, såsom metallindustrier, man kan hitta metaller i tillräckligt höga halter för att orsaka skada på växter och djur. I denna avhandling presenteras undersökningar av hur svartvit flugsnappare (Ficedula hypoleuca) påverkas kring två metallindustrier i norra Sverige. Det ena är en numera nedlagd blygruva med anrikningsverk i Laisvall, där vi studerade populationer av svartvit flugsnappare före och efter att industrin stängdes. Det andra är smältverket Rönnskärsverken, utanför Skelleftehamn, som varit i drift sedan 1930-talet. I föroreningsgradienten från smältverket studerades effekter av 20 års kraftigt minskade metallutsläpp till luften som följd av förbättrade reningstekniker.

Resultaten kring industrierna visar att fåglarna svarade olika på de minskade metallutsläppen. Kring blygruvan minskade halterna av bly i flugsnapparungar med samma takt som nedfallen (mätt i mossa) och bytesdjuren (myror). Däremot, kring smältverket, var fåglarna fortfarande exponerade för höga halter av de giftiga ämnena arsenik, kadmium, kvicksilver och bly, på i princip samma nivåer som 20 år tidigare, trots att utsläppen minskat med 93 – 98%. Orsaken till detta tros vara skillnader på föroreningsgraden i markens översta lager, mårskiktet. Vi kunde visa att flugsnapparna kring smältverket främst fick i sig metallerna från marken, som efter flera årtionden med utsläpp från industrin innehöll mycket höga metallhalter. Detta kan förklara att fåglarna trots att utsläppen var låga, fortfarande var utsatta för stor metallexponering. Det snabba svaret på minskad metallspridning (bly och zink) som flugsnapparna vid blygruvan visade, antar vi berodde på att mindre mäng metaller fanns i marken. Trots minskningen var metallhalterna i fåglarna vid gruvområdet fortfarande tillräckligt höga för att, liksom vid smältverket, påverka fåglarnas hälsa. De uppvisade bl.a. låga blodvärden och tecken på oxidativ stress. Vidare var ungdödligheten förhöjd, vilket ledde till lägre häckningsframgång.

Slutsatsen är att markens innehåll av metaller har stor betydelse för återhämtningsförloppet för svartvit flugsnappare efter minskat metallnedfall, och att en relativt snabb återhämtning kan förväntas i områden med något lägre metallhalter i mårskiktet, medan återhämtning i områden där marken är kraftigt förorenad inte kan förväntas förrän efter flera årtionden, även om nedfallet upphört nästan helt.

Place, publisher, year, edition, pages
Umeå: Umeå universitet, Institutionen för ekologi, miljö och geovetenskap , 2010. , 48 p.
National Category
Pharmacology and Toxicology Other Biological Topics
Research subject
Ecotoxicology; Animal Ecology; biology, Environmental Science
Identifiers
URN: urn:nbn:se:umu:diva-33767ISBN: 978-91-7264-983-5 (print)OAI: oai:DiVA.org:umu-33767DiVA: diva2:318033
Public defence
2010-05-29, KBC-huset, KB3A9, lilla hörsalen, Umeå universitet, Umeå, 10:00 (English)
Opponent
Supervisors
Available from: 2010-05-07 Created: 2010-05-05 Last updated: 2010-05-07Bibliographically approved
List of papers
1. Lead exposure and biological effects in pied flycatchers (Ficedula hypoleuca) before and after the closure of a lead mine in northern Sweden.
Open this publication in new window or tab >>Lead exposure and biological effects in pied flycatchers (Ficedula hypoleuca) before and after the closure of a lead mine in northern Sweden.
2010 (English)In: Environmental Pollution, ISSN 0269-7491, E-ISSN 1873-6424, Vol. 158, no 5, 1368-75 p.Article in journal (Refereed) Published
Abstract [en]

Mining activities affect the surrounding environment by increasing exposure to metals. In this study, metal accumulation and its effects on reproduction and health of pied flycatcher (Ficedula hypoleuca) nestlings were monitored before and up to five years after a lead mine and enrichment plant closed down. The lead concentration in moss, nestling blood, liver and feces all indicated decreased lead exposure by at least 31% after closure, although only blood lead decreased significantly. Although the birds responded fairly well to the changed atmospheric deposition (based on moss samples), concentrations were still higher compared with birds in a reference area, and breeding was affected at the mine (smaller clutches and higher mortality). Surviving nestlings suffered from lower hemoglobin levels, mean cell hemoglobin concentrations and inhibited delta-aminolevulinic acid dehydratase activity. Lead poisoning contributed to poor health and adverse reproductive effects, but other factors (e.g. increased parasitic load) probably also affected the birds.

Place, publisher, year, edition, pages
Elsevier Ltd, 2010
Identifiers
urn:nbn:se:umu:diva-33609 (URN)10.1016/j.envpol.2010.01.005 (DOI)000277726500034 ()20116150 (PubMedID)
Available from: 2010-04-29 Created: 2010-04-29 Last updated: 2017-12-12Bibliographically approved
2. Slow improvements of metal exposure, health- and breeding conditions of pied flycatchers (Ficedula hypoleuca) after decreased industrial heavy metal emissions
Open this publication in new window or tab >>Slow improvements of metal exposure, health- and breeding conditions of pied flycatchers (Ficedula hypoleuca) after decreased industrial heavy metal emissions
(English)Manuscript (preprint) (Other academic)
Abstract [en]

The environment around metal industries, such as smelters, is often highly contaminated due to continuous deposition of metals. We studied nest box breeding populations of pied flycatchers (Ficedula hypoleuca) in a well-studied pollution gradient from a sulfide ore smelter in Northern Sweden, after reduced aerial metal emissions (by 93 – 99%) from the smelter. The deposition of As, Cd, Cu and Zn (based on moss samples) reflected the reduced emissions fairly well. However, nestling pied flycatchers had similar concentrations of these elements and Hg in tissue (bone, liver and blood) and feces in the 2000s, as in the 1980s, when the emissions were substantially higher. The slow improvement of metal accumulation in birds was explained by a food web transfer of metals mainly from the highly polluted soils, and it was concluded that nestlings reflected the slowly cycling soil pool, rather than the current atmospheric deposition. The exposure to high metal concentrations in the close vicinity of the smelter resulted in inhibited ALAD activities, depressed hemoglobin and hematocrit levels and increased mortality of nestlings. Our results indicate that in metal contaminated environments, the concentration in soils plays an important role for the response of pied flycatchers to reduced atmospheric deposition.

Keyword
Metals, Bird, Reproduction, Health, Blood variable, Recovery, Smelter, Rönnskärsverken, Air pollution
National Category
Pharmacology and Toxicology Biological Sciences
Research subject
Ecotoxicology
Identifiers
urn:nbn:se:umu:diva-33766 (URN)
Available from: 2010-05-05 Created: 2010-05-05 Last updated: 2010-05-07Bibliographically approved
3. Effects of reduced lead deposition on Pied flycatcher (Ficedula hypoleuca): tracing exposure routes using stable lead Isotopes
Open this publication in new window or tab >>Effects of reduced lead deposition on Pied flycatcher (Ficedula hypoleuca): tracing exposure routes using stable lead Isotopes
2009 (English)In: Environmental Science and Technology, ISSN 0013-936X, E-ISSN 1520-5851, Vol. 43, no 1, 208-213 p.Article in journal (Refereed) Published
Abstract [en]

To what extent the lead burden of birds living in strongly contaminated ecosystems is responding to decreased atmospheric lead deposition is not well known. In this study, we measured lead concentrations and stable lead isotope ratios (206Pb/207Pb and 208Pb/207Pb) in liver and feces from pied flycatcher nestlings (Ficedula hypoleuca) along a 90 km pollution gradient from the Rönnskär smelter in northern Sweden. Changes in lead concentration in the birds from 1984 to 2006 were used for assessing the recovery of the environment following reduced lead emissions at the smelter. The 206Pb/207Pb and 208Pb/207Pb ratios were used to identify lead sources to the birds. Lead concentrations in liver and feces have decreased since the 1980s, typically by 9−15% (liver) and 18−40% (feces) as a result of a 98% emission reduction. This relatively weak recovery is explained by a transfer of old lead contaminants accumulated in soil to the birds via their prey, which was evident by a 206Pb/207Pb ratio in liver tissue (1.15 ± 0.01) that overlapped with the ratio in ants (1.16 ± 0.01) and organic soil horizon (1.17 ± 0.01) rather than the current atmospheric lead pollution (1.11 ± 0.01). Our findings suggest that insectivorous birds living around smelters may remain contaminated decades after ceased emissions.

Place, publisher, year, edition, pages
American Chemical Society, 2009
Identifiers
urn:nbn:se:umu:diva-23302 (URN)10.1021/es801723q (DOI)
Available from: 2009-06-09 Created: 2009-06-09 Last updated: 2017-12-13Bibliographically approved
4. Oxidative stress in pied flycatcher (Ficedula hypoleuca) nestlings from metal contaminated environments in northern Sweden
Open this publication in new window or tab >>Oxidative stress in pied flycatcher (Ficedula hypoleuca) nestlings from metal contaminated environments in northern Sweden
2007 (English)In: Environmental Research, ISSN 0013-9351, E-ISSN 1096-0953, Vol. 105, no 3, 330-339 p.Article in journal (Refereed) Published
Abstract [en]

Metals have been shown to induce oxidative stress in animals. One of the most metal polluted terrestrial environments in Sweden is the surroundings of a sulfide ore smelter plant located in the northern part of the country. Pied flycatcher nestlings (Ficedula hypoleuca) that grew up close to the industry had accumulated amounts of arsenic, cadmium, mercury, lead, iron and zinc in their liver tissue. The aim of this study was to investigate if pied flycatcher nestlings in the pollution gradient of the industry were affected by oxidative stress using antioxidant molecules and enzyme activities. The antioxidant assays were also evaluated in search for useful biomarkers in pied flycatchers. This study indicated that nestlings in metal contaminated areas showed signs of oxidative stress evidenced by up regulated hepatic antioxidant defense given as increased glutathione reductase (GR) and catalase (CAT) activities and slightly but not significantly elevated lipid peroxidation and glutathione-S-transferase (GST) activities. Stepwise linear regression indicated that lipid peroxidation and CAT activities were influenced mostly by iron, but iron and lead influenced the CAT activity to a higher degree. Positive relationships were found between GST and lead as well as GR activities and cadmium. We conclude that GR, CAT, GST activities and lipid peroxidation levels may function as useful biomarkers for oxidative stress in free-living pied flycatcher nestlings exposed to metal contaminated environments.

Place, publisher, year, edition, pages
Elsevier, 2007
Keyword
Oxidative stress, Aves, Metals, Biomarker, Environmental assessment
Identifiers
urn:nbn:se:umu:diva-17344 (URN)10.1016/j.envres.2007.06.002 (DOI)
Available from: 2007-11-08 Created: 2007-11-08 Last updated: 2010-05-07Bibliographically approved

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CiteExportLink to record
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