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Cited by 27Environmental Toxicology and EcotoxicologyMicroplastics and Plastic PollutionHeavy Metal Exposure and Toxicity

Lead Poisoning of Steller’s Sea Eagle (Haliaeetus pelagicus) and White-tailed Eagle (Haliaeetus albicilla) Caused by the Ingestion of Lead Bullets and Slugs, in Hokkaido, Japan

Open access
Saito, Keisuke·2009·Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans
DOI 10.4080/ilsa.2009.0304
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Abstract

The Steller's Sea-Eagle (Haliaeetus pelagicus) and the White-tailed Eagle (H.albicilla) are among the largest eagles.The total population of the Steller's Sea-Eagle is estimated at 5,000 to 6,000 individuals, and these eagles winter in large numbers in northern Japan, on the island of Hokkaido.Lead poisoning of Steller's Sea-Eagles in Japan was first confirmed in 1996.By 2007, 129 Steller's and Whitetailed Eagles had been diagnosed as lead poisoning fatalities.High lead values up to 89 ppm (wet-weight) from livers of eagles available for testing indicate that they died from lead poisoning.Necropsies and radiographs also revealed pieces of lead from rifle bullets and from shotgun slugs to be present in the digestive tracts of poisoned eagles, providing evidence that a source of lead was spent ammunition from leadcontaminated Sika Deer carcasses.Tradition and law in Japan allow hunters to remove the desirable meat from animals and abandon the rest of the carcass in the field.Deer carcasses have now become a major food source for wintering eagles.Reacting to the eagle poisoning issue, Hokkaido authorities have regulated the use of lead rifle bullets since 2000.The Ministry of the Environment mandated use of non-toxic rifle bullets or shotgun slugs beginning the winter of 2001.However, these regulations are limited to the island of Hokkaido, and depend largely on cooperation from hunters.A nationwide ban on the use of lead ammunition for all types of hunting and cooperation from citizens would solve the problem of lead poisoning of eagles.

AI snapshot

Written from the paper’s full text.

TL;DR

Lead poisoning in Steller’s Sea-Eagles and White-tailed Eagles wintering in Hokkaido was caused mainly by ingestion of lead fragments from rifle bullets and shotgun slugs in abandoned Sika Deer carcasses, with 129 eagle lead-poisoning fatalities diagnosed by 2007. Hokkaido and national regulations on lead ammunition began in 2000–2001, but poisoning continued through at least winter 2006–07.

Key findings

  • By 2007, 129 Steller’s and White-tailed Eagles had been diagnosed as lead poisoning fatalities; the paper also reports 92 Steller’s and 37 White-tailed Eagles died since first detection in 1996. Liver lead values of 2.0 to 89 ppm wet-weight indicated death by lead, and necropsies/radiographs found lead pieces from rifle bullets and shotgun slugs in digestive tracts.
  • Reported winter poisoning counts included 21 eagles (18 Steller’s, 3 White-tailed) in 1997–98; 26 (16 Steller’s, 10 White-tailed) in 1998–99; and 10 Steller’s and 4 White-tailed in 1999–2000. In winter 1998–1999, 33 eagle carcasses were found and 78% had lead poisoning.
  • Hokkaido regulated lead rifle bullets for Sika Deer hunting since 2000, and the Ministry of the Environment mandated non-toxic rifle bullets or shotgun slugs beginning winter 2001; regulation for all big game, including Brown Bear, started winter 2004. Despite this, 7 Steller’s and 3 White-tailed Eagles were poisoned in winter 2004–05, 1 Steller’s and 2 White-tailed in 2005–06, and 7 Steller’s in 2006–07.
  • The source was lead-contaminated Sika Deer carcasses from hunting: tradition and law allowed hunters to remove meat and abandon the rest in the field, and deer population control increased remains. Adult eagles dominant at carcasses were at high risk of consuming meat with lead fragments near bullet entry wounds; lead shot from waterfowl hunting was also a source.

Methods

  • Design: descriptive conference paper/review of lead poisoning cases and prevention activities in Hokkaido, combining field investigation, diagnostic case work, and policy review.
  • Data/sample: eagle carcasses and live/dead birds brought to the Kushiro Shitsugen Wildlife Center; preserved eagle specimens; field surveys of wintering eagles and abandoned deer carcasses; deer tissue samples around bullet impact areas; fecal samples and pellets.
  • Main analysis: necropsy, radiography, lead concentration measurement in liver/blood (criteria: hepatic >2 ppm and blood >0.6 ppm = lead poisoning), and lead isotope ratio analysis (208/206 Pb and 207/206 Pb) to identify rifle origin; field counts and observations.

Limitations

  • Stated: the number of lead-poisoned eagles collected is “just a tip of the iceberg”; many carcasses occur midwinter in mountains where no one visits, so actual casualties are far more than found. The demographic impact is difficult to measure because deaths during migration and in the Russian breeding range are unknown.
  • Stated: collection rate varies with the number of people entering mountain areas and snowfall conditions; diagnosing lead poisoning is not easily done in each case and requires special equipment. Regulations are limited to Hokkaido and depend largely on hunter cooperation; the restriction prohibits “using” lead bullets but does not limit sales or ownership, and offenders are difficult to catch red-handed.
  • Evident from the text: findings rely on opportunistic recovery and field observations rather than systematic sampling, so reported counts may underrepresent mortality, and no formal population-level analysis is presented.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.4080/ilsa.2009.0304

Cites

5 of 5 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 7 cited sources checked · 0 supported · 0 flagged

  • Findingreasoning

    Deer carcasses have now become a major food source for wintering eagles.

    “Deer carcasses have now become a major food source for wintering eagles.”
    Quote in the paperSubstantial claim
  • Findingown data

    Necropsies and radiographs revealed pieces of lead from rifle bullets and from shotgun slugs to be present in the digestive tracts of poisoned eagles.

    “Necropsies and radiographs also revealed pieces of lead from rifle bullets and from shotgun slugs to be present in the digestive tracts of poisoned eagles”
    • Also stated in: § LEAD POISONING FROM LEAD AMMUNITION · plain
      “Necropsies and radiographs have revealed pieces of lead from rifle bullets and from shotgun slugs to be present in the digestive tracts of poisoned eagles.”
    Quote in the paperSubstantial claim
  • Findingown data

    Afterwards, the number of eagle lead poisonings decreased slightly (ten Steller's and four White-tailed in 1999-2000).

    “Afterwards, the number of eagle lead poisonings decreased slightly (ten Steller's and four White-tailed in 1999-2000)”
    Quote in the paperNot a substantial claim
  • Findingown data

    Twenty-one eagles (18 Steller's and three White-tailed) were confirmed to have been lead poisoned in the winter of 1997-98.

    “Twenty-one eagles (18 Steller's and three Whitetailed) were confirmed to have been lead poisoned in the winter of 1997-98”
    Quote in the paperSubstantial claim
  • Findingown data

    In the first detected case, a lead shot from waterfowl hunting was found in the ventriculus of the eagle.

    “In this case, a lead shot from waterfowl hunting was found in the ventriculus of the eagle.”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim. 17
  • May combine two claims. 11

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Findingnone given

    White-tailed Eagles now also feed on Sika Deer carcasses.

    “Now they also feed on Sika Deer carcasses.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingreasoning

    Steller's Sea-Eagles found deer as a new food source and are now commonly observed inland.

    “Steller's Sea-Eagles found these deer as a new food source, and now are commonly observed inland.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Findingnone given

    Lead poisoning in sea eagles is characterized by high mortality of adult birds.

    “Lead poisoning in sea eagles is characterized by the high mortality of the adult birds.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In winter 1998-1999, the total number of eagle carcasses found was 33, and 78% had lead poisoning.

    “The total number of eagle carcasses found this winter was 33, and 78% had lead poisoning.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Findingreasoning

    The practice of dumping the carcass has gradually changed.

    “The practice of dumping the carcass has gradually changed.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingnone given

    In the maximum case, 1 ton of deer carcasses was collected at one forest road during one day of cleaning activity.

    “In the maximum case, 1 ton of deer carcasses was collected at one forest road, during one day of cleaning activity.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingnone given

    At the time when lead poisoning of eagles became a serious problem in Hokkaido, the Xbullet was almost impossible to obtain in Japan.

    “At the time when lead poisoning of eagles became a serious problem in Hokkaido, the Xbullet was almost impossible to obtain in Japan.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Steller's Sea-Eagles normally weigh 6 to 8 kg, but individuals killed by lead show severe weight loss.

    “Steller's Sea-Eagles normally weigh 6 to 8 kg but individuals killed by lead show severe weight loss.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingreasoning

    According to field observations, adult eagles are dominant at a carcass and force other birds away, and consequently adult eagles are at high risk of consuming meat that contains a large amount of lead fragments at and near the bullet entry wound.

    “According to field observations, adult eagles are dominant at a carcass and force other birds away, and consequently, adult eagles are at high risk of consuming meat that contains a large amount of lead fragments at and near the bullet entry wound.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based). May combine two claims.

    Interpretationnone given

    A nationwide ban on the use of lead ammunition for all types of hunting and cooperation from citizens would solve the problem of lead poisoning of eagles.

    “A nationwide ban on the use of lead ammunition for all types of hunting and cooperation from citizens would solve the problem of lead poisoning of eagles.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Interpretationreasoning

    As a result of the Sika Deer population increase, deer carcasses resulting from accidents, starvation, or hunting were easily discovered by eagles in the mountains of Hokkaido.

    “As a result, deer carcasses resulting from accidents, starvation, or hunting were easily discovered by eagles in the mountains of Hokkaido.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The population of Sika Deer has dramatically increased.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The principal diet of sea eagles is fish such as salmon and pollack.

    “The principal diet of sea eagles, as their scientific name”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Ueta et al. 1995

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Shiraki 2001 source

  • May combine two claims.

    Interpretationreasoning

    The present restriction is a prohibition of using lead bullets, but it does not limit sales or ownership of lead ammunition, and it is difficult to catch an offender red-handed; these factors will prolong the threat of lead poisoning.

    “The present restriction is a prohibition of”
    • Also stated in: § Activity to Promote the Shift to Nontoxic Bullets.- · plain
      “These factors will prolong the threat of lead poisoning.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Interpretationnone given

    Even if the amount of ingested lead was not fatal, lead can have sub-lethal effects (e.g., neurological) that could contribute to other causes of death, such as being hit by cars.

    “Even if the amount of ingested lead was not fatal, the toxic substance can have sub-lethal effects (e.g., neurological) that could contribute to other causes of death, such as a being hit by cars.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    Therefore, if some hunters wanted to use the copper bullet, it was necessary to make them with an expensive reloading machine.

    “Therefore, if some hunters wanted to use the copper bullet, it was necessary to make them with an expensive reloading machine.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    Lead poisoning of eagles also is caused by ingestion of lead shot used for waterfowl hunting.

    “Moreover, lead poisoning of eagles also is caused by ingestion of lead shot used for waterfowl hunting.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Interpretationnone given

    A nationwide abolishment of all lead ammunition could solve the problem of raptor lead poisoning.

    “A nationwide abolishment of all lead ammunition could solve the problem of raptor lead poisoning.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    As a result of the 1998 Hokkaido deer population control program, the remains of Sika Deer left by hunters increased and wounded deer that died afterwards also greatly increased.

    “As a result, the remains of Sika Deer left by hunters increased and Sika Deer that had been wounded and died afterwards also greatly increased.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: In 1998, Hokkaido government authorities announced a radical deer population control program to reduce feeding damage caused by Sika Deer.
    • Rests on an assumption: The deer population control program would cull the herd in eastern Hokkaido from 200,000 animals to 30,000 within three years.

  • Classified as probably not a substantial claim.

    Interpretationreasoning

    Under the condition of legality outside Hokkaido, it is difficult to verify that all foreign hunters change their bullets to non-toxic ones on Hokkaido Island.

    “Under the condition of legality outside Hokkaido, it is difficult to verify that all”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based). May combine two claims.

    Interpretationreasoning

    If the police come frequently to the hunting field, collect deer tissue samples at bullet entry points, and examine for the presence of lead fragments, they will document the problem, and then the use of lead ammunition will certainly decrease.

    “However, if the police come frequently to the hunting field, collect deer tissue samples at bullet entry points, and examine for the presence of lead fragments, they will document the problem, and then the use of lead ammunition will certainly decrease.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Interpretationreasoning

    Because eagles are accustomed to feeding on carcasses, they are attracted to traffic accident carcasses near roads or railroads and are thus vulnerable to traffic accidents.

    “Now that eagles are accustomed to feeding on carcasses, they are attracted to traffic accident carcasses that occur near the road or railroad and thus are vulnerable to traffic accidents.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing). May combine two claims.

    Interpretationreasoning

    The number of lead poisoned eagles collected is just a tip of the iceberg, and actual casualties by lead poisoning are far more than the number found.

    “Moreover, the number of lead poisoned eagles collected is just a tip of the iceberg.”
    • Also stated in: § LEAD POISONING FROM LEAD AMMUNITION · hedged
      “It is suggested that actual casualties by lead poisoning are far more than the number found.”
    Quote in the paperNot a substantial claim
22 of 22

  • The paper relies on this without support.

    The waterfowl-derived criteria for lead exposure (hepatic >2 ppm, blood >0.6 ppm) are valid for diagnosing lead poisoning in sea eagles.

    “The criteria for assessing lead exposure in raptors have been established by using examples from waterfowl: Hepatic level <0.2 ppm: normal range 0.2-2 ppm: high exposure >2 ppm: lead poisoning Blood level <0.1 ppm: normal range (obstruction of the enzyme level is reported at 0.1 ppm.) 0.1-0.6 ppm: high exposure >0.6 ppm: lead poisoning”

  • The paper relies on this without support.

    The population of Sika Deer has dramatically increased.

    “Around the same time, the population of Sika Deer (Cervus nippon) has dramatically increased.”

  • The paper relies on this without support.

    In 1998, Hokkaido government authorities announced a radical deer population control program to reduce feeding damage caused by Sika Deer.

    “Furthermore, in 1998, Hokkaido government authorities announced a radical deer population control program to reduce the feeding damage caused by Sika Deer.”

  • The paper relies on this without support.

    The deer population control program would cull the herd in eastern Hokkaido from 200,000 animals to 30,000 within three years.

    “This would cull the herd in eastern Hokkaido from the current 200,000 animals to 30,000 within three years.”
4 of 4

Cites

Flagged first, then by citations

Research works printed but not linked: 5

  1. KUROSAWA, N. 2000. Lead poisoning in Steller's Sea Eagles and White-tailed Sea Eagle. Pages 107-109 in First symposium on Steller's and White-tailed Sea eagles in east Asia: Proceed- ings of the International Workshop and Sympo- sium in Tokyo and Hokkaido 9-15 February, 1999. Wild Bird Society of Japan, Tokyo, Japan.
  2. SAITO, K. 1997. Lead Poisoning of Steller's Sea Eagle in Eastern Hokkaido. Proceedings, 3rd Annual Meeting of Japanese Society of Zoo and Wildlife Medicine, Gifu, Japan.
  3. SAITO, K., N. KUROSAWA, AND R. SHIMURA. 2000. Lead Poisoning in White-tailed Eagle (Hali- aeetus albicilla) and Steller's Sea-Eagle (Hali- aeetus pelagicus) in Eastern Hokkaido through ingestion of shot Sika Deer, 2000. Pages 163- 169 in J. T. Lumeij, J. D. Remple, P. T. Redig, M. Lierz, and J. E. Cooper (Eds.). Raptor Bio- medicine III, Zoological Education Network, Inc, Lake Worth, Florida, USA.
  4. UETA, M., E. G. LOBKOV, K. FUKUI, AND K. KATO. 1995. The food resources of Steller's Sea-Eagles in eastern Hokkaido. Pages 37-46 in Survey of the status and habitat conditions of threatened species, 1995. Published by Envi- ronment Agency, Tokyo, Japan.
  5. UETA, M., AND M. J. MCGRADY (EDS.). 2000. First symposium on Steller's and White-tailed Sea eagles in east Asia; Proceedings of the Interna- tional Workshop and Symposium in Tokyo and Hokkaido 9-15 February, 1999. Wild Bird So- ciety of Japan, Tokyo, Japan.

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Authors
Saito, K.
Corresponding author
Saito, Keisuke
ORCID
Saito, Keisuke
Venue
Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans
Publisher
The Peregrine Fund
Published
2009-01
DOI
10.4080/ilsa.2009.0304
OpenAlex
W2327142357
Semantic Scholar
c1c4de273f0ca1792416cdf704c3a4719c436392
Cited by
27
References
5
Citations by year
2024: 1 · 2022: 2 · 2021: 4 · 2020: 4 · 2018: 4 · 2017: 3 · 2014: 3 · 2013: 2 · 2012: 2
FWCI
11.30
Type
conference paper
Language
en
Open access
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
  • Physical Sciences › Environmental Science › Pollution › Microplastics and Plastic Pollution
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Heavy Metal Exposure and Toxicity
Keywords
lead poisoning, Steller's sea eagle, Haliaeetus pelagicus, white-tailed eagle, lead ammunition, Hokkaido, wildlife poisoning

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