Reproductive Failure in UK Harbour Porpoises Phocoena phocoena

Legacy of Pollutant Exposure?

Sinead Murphy*, Jonathan L. Barber, Jennifer A. Learmonth, Fiona L. Read, Robert Deaville, Matthew W. Perkins, Andrew Brownlow, Nick Davison, Rod Penrose, Graham J. Pierce, Robin J. Law, Paul D. Jepson

*Corresponding author for this work

Research output: Contribution to journalArticle

19 Citations (Scopus)
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Abstract

Reproductive failure in mammals due to exposure to polychlorinated biphenyls (PCBs) can occur either through endocrine disrupting effects or via immunosuppression and increased disease risk. To investigate further, full necropsies and determination of summed 25 polychlorinated biphenyls congeners (Sigma PCBs lipid weight) in blubber were undertaken on 329 UK-stranded female harbour porpoises (1990-2012). In sexually mature females, 25/127 (19.7%) showed direct evidence of reproductive failure (foetal death, aborting, dystocia or stillbirth). A further 21/127 (16.5%) had infections of the reproductive tract or tumours of reproductive tract tissues that could contribute to reproductive failure. Resting mature females (non-lactating or non-pregnant) had significantly higher mean Sigma PCBs (18.5 mg/kg) than both lactating (7.5 mg/kg) and pregnant females (6 mg/kg), though not significantly different to sexually immature females (14.0 mg/kg). Using multinomial logistic regression models Sigma PCBs was found to be a significant predictor of mature female reproductive status, adjusting for the effects of confounding variables. Resting females were more likely to have a higher PCB burden. Health status (proxied by "trauma" or "infectious disease" causes of death) was also a significant predictor, with lactating females (i.e. who successfully reproduced) more likely to be in good health status compared to other individuals. Based on contaminant profiles (>11 mg/kg lipid), at least 29/60 (48%) of resting females had not off-loaded their pollutant burden via gestation and primarily lactation. Where data were available, these non-offloading females were previously gravid, which suggests foetal or newborn mortality. Furthermore, a lower pregnancy rate of 50% was estimated for "healthy" females that died of traumatic causes of death, compared to other populations. Whether or not PCBs are part of an underlying mechanism, we used individual PCB burdens to show further evidence of reproductive failure in the North-east Atlantic harbour porpoise population, results that should inform conservation management.

Original languageEnglish
Article number0131085
Number of pages32
JournalPloS ONE
Volume10
Issue number7
Early online date22 Jul 2015
DOIs
Publication statusPublished - 22 Jul 2015

Keywords

  • bottle-nosed dolphins
  • California Sea Lions
  • endocrine-disrupting chemicals
  • persistent organic pollutants
  • St-Lawrence Estuary
  • mink mustela-vison
  • polychlorinated-biphenyls
  • Zalophus-Californianus
  • tursiops-truncatus
  • delphinus-delphis

Cite this

Murphy, S., Barber, J. L., Learmonth, J. A., Read, F. L., Deaville, R., Perkins, M. W., ... Jepson, P. D. (2015). Reproductive Failure in UK Harbour Porpoises Phocoena phocoena: Legacy of Pollutant Exposure? PloS ONE, 10(7), [0131085]. https://doi.org/10.1371/journal.pone.0131085

Reproductive Failure in UK Harbour Porpoises Phocoena phocoena : Legacy of Pollutant Exposure? / Murphy, Sinead; Barber, Jonathan L.; Learmonth, Jennifer A.; Read, Fiona L.; Deaville, Robert; Perkins, Matthew W.; Brownlow, Andrew; Davison, Nick; Penrose, Rod; Pierce, Graham J.; Law, Robin J.; Jepson, Paul D.

In: PloS ONE, Vol. 10, No. 7, 0131085, 22.07.2015.

Research output: Contribution to journalArticle

Murphy, S, Barber, JL, Learmonth, JA, Read, FL, Deaville, R, Perkins, MW, Brownlow, A, Davison, N, Penrose, R, Pierce, GJ, Law, RJ & Jepson, PD 2015, 'Reproductive Failure in UK Harbour Porpoises Phocoena phocoena: Legacy of Pollutant Exposure?', PloS ONE, vol. 10, no. 7, 0131085. https://doi.org/10.1371/journal.pone.0131085
Murphy S, Barber JL, Learmonth JA, Read FL, Deaville R, Perkins MW et al. Reproductive Failure in UK Harbour Porpoises Phocoena phocoena: Legacy of Pollutant Exposure? PloS ONE. 2015 Jul 22;10(7). 0131085. https://doi.org/10.1371/journal.pone.0131085
Murphy, Sinead ; Barber, Jonathan L. ; Learmonth, Jennifer A. ; Read, Fiona L. ; Deaville, Robert ; Perkins, Matthew W. ; Brownlow, Andrew ; Davison, Nick ; Penrose, Rod ; Pierce, Graham J. ; Law, Robin J. ; Jepson, Paul D. / Reproductive Failure in UK Harbour Porpoises Phocoena phocoena : Legacy of Pollutant Exposure?. In: PloS ONE. 2015 ; Vol. 10, No. 7.
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title = "Reproductive Failure in UK Harbour Porpoises Phocoena phocoena: Legacy of Pollutant Exposure?",
abstract = "Reproductive failure in mammals due to exposure to polychlorinated biphenyls (PCBs) can occur either through endocrine disrupting effects or via immunosuppression and increased disease risk. To investigate further, full necropsies and determination of summed 25 polychlorinated biphenyls congeners (Sigma PCBs lipid weight) in blubber were undertaken on 329 UK-stranded female harbour porpoises (1990-2012). In sexually mature females, 25/127 (19.7{\%}) showed direct evidence of reproductive failure (foetal death, aborting, dystocia or stillbirth). A further 21/127 (16.5{\%}) had infections of the reproductive tract or tumours of reproductive tract tissues that could contribute to reproductive failure. Resting mature females (non-lactating or non-pregnant) had significantly higher mean Sigma PCBs (18.5 mg/kg) than both lactating (7.5 mg/kg) and pregnant females (6 mg/kg), though not significantly different to sexually immature females (14.0 mg/kg). Using multinomial logistic regression models Sigma PCBs was found to be a significant predictor of mature female reproductive status, adjusting for the effects of confounding variables. Resting females were more likely to have a higher PCB burden. Health status (proxied by {"}trauma{"} or {"}infectious disease{"} causes of death) was also a significant predictor, with lactating females (i.e. who successfully reproduced) more likely to be in good health status compared to other individuals. Based on contaminant profiles (>11 mg/kg lipid), at least 29/60 (48{\%}) of resting females had not off-loaded their pollutant burden via gestation and primarily lactation. Where data were available, these non-offloading females were previously gravid, which suggests foetal or newborn mortality. Furthermore, a lower pregnancy rate of 50{\%} was estimated for {"}healthy{"} females that died of traumatic causes of death, compared to other populations. Whether or not PCBs are part of an underlying mechanism, we used individual PCB burdens to show further evidence of reproductive failure in the North-east Atlantic harbour porpoise population, results that should inform conservation management.",
keywords = "bottle-nosed dolphins, California Sea Lions, endocrine-disrupting chemicals, persistent organic pollutants, St-Lawrence Estuary, mink mustela-vison, polychlorinated-biphenyls, Zalophus-Californianus, tursiops-truncatus, delphinus-delphis",
author = "Sinead Murphy and Barber, {Jonathan L.} and Learmonth, {Jennifer A.} and Read, {Fiona L.} and Robert Deaville and Perkins, {Matthew W.} and Andrew Brownlow and Nick Davison and Rod Penrose and Pierce, {Graham J.} and Law, {Robin J.} and Jepson, {Paul D.}",
note = "This research was supported by a Marie Curie International Outgoing Fellowship within the Seventh European Community Framework Programme (Project Cetacean-stressors, PIOF-GA-2010-276145 to PDJ and SM). Additional funding was provided through the Agreement on the Conservation of Small Cetaceans of the Baltic, North East Atlantic, Irish and North Seas (ASCOBANS) (Grants SSFA/2008 and SSFA / ASCOBANS / 2010 / 5 to SM). Analysis of Scottish reproductive and teeth samples was funded by the EC-funded BIOCET project (BIOaccumulation of persistent organic pollutants in small CETaceans in European waters: transport pathways and impact on reproduction, grant EVK3-2000-00027 to GJP), and Marine Scotland (GJP). Samples examined in this research were collected under the collaborative Cetacean Strandings Investigation Programme (http://ukstrandings.org/), which is funded by the Department for Environment, Food and Rural Affairs (Defra) and the UK’s Devolved Administrations in Scotland and Wales (http://sciencesearch.defra.gov.uk/Defaul​t.aspx?Menu=Menu&Module=More&Location=No​ne&Completed=0&ProjectID=15331) (grants to PDJ, RD). UK Defra also funded the chemical analysis under a service-level agreement with the Centre for Environment, Fisheries and Aquaculture Science (grants to RJL, JB). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.",
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T2 - Legacy of Pollutant Exposure?

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AU - Read, Fiona L.

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AU - Perkins, Matthew W.

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AU - Davison, Nick

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PY - 2015/7/22

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N2 - Reproductive failure in mammals due to exposure to polychlorinated biphenyls (PCBs) can occur either through endocrine disrupting effects or via immunosuppression and increased disease risk. To investigate further, full necropsies and determination of summed 25 polychlorinated biphenyls congeners (Sigma PCBs lipid weight) in blubber were undertaken on 329 UK-stranded female harbour porpoises (1990-2012). In sexually mature females, 25/127 (19.7%) showed direct evidence of reproductive failure (foetal death, aborting, dystocia or stillbirth). A further 21/127 (16.5%) had infections of the reproductive tract or tumours of reproductive tract tissues that could contribute to reproductive failure. Resting mature females (non-lactating or non-pregnant) had significantly higher mean Sigma PCBs (18.5 mg/kg) than both lactating (7.5 mg/kg) and pregnant females (6 mg/kg), though not significantly different to sexually immature females (14.0 mg/kg). Using multinomial logistic regression models Sigma PCBs was found to be a significant predictor of mature female reproductive status, adjusting for the effects of confounding variables. Resting females were more likely to have a higher PCB burden. Health status (proxied by "trauma" or "infectious disease" causes of death) was also a significant predictor, with lactating females (i.e. who successfully reproduced) more likely to be in good health status compared to other individuals. Based on contaminant profiles (>11 mg/kg lipid), at least 29/60 (48%) of resting females had not off-loaded their pollutant burden via gestation and primarily lactation. Where data were available, these non-offloading females were previously gravid, which suggests foetal or newborn mortality. Furthermore, a lower pregnancy rate of 50% was estimated for "healthy" females that died of traumatic causes of death, compared to other populations. Whether or not PCBs are part of an underlying mechanism, we used individual PCB burdens to show further evidence of reproductive failure in the North-east Atlantic harbour porpoise population, results that should inform conservation management.

AB - Reproductive failure in mammals due to exposure to polychlorinated biphenyls (PCBs) can occur either through endocrine disrupting effects or via immunosuppression and increased disease risk. To investigate further, full necropsies and determination of summed 25 polychlorinated biphenyls congeners (Sigma PCBs lipid weight) in blubber were undertaken on 329 UK-stranded female harbour porpoises (1990-2012). In sexually mature females, 25/127 (19.7%) showed direct evidence of reproductive failure (foetal death, aborting, dystocia or stillbirth). A further 21/127 (16.5%) had infections of the reproductive tract or tumours of reproductive tract tissues that could contribute to reproductive failure. Resting mature females (non-lactating or non-pregnant) had significantly higher mean Sigma PCBs (18.5 mg/kg) than both lactating (7.5 mg/kg) and pregnant females (6 mg/kg), though not significantly different to sexually immature females (14.0 mg/kg). Using multinomial logistic regression models Sigma PCBs was found to be a significant predictor of mature female reproductive status, adjusting for the effects of confounding variables. Resting females were more likely to have a higher PCB burden. Health status (proxied by "trauma" or "infectious disease" causes of death) was also a significant predictor, with lactating females (i.e. who successfully reproduced) more likely to be in good health status compared to other individuals. Based on contaminant profiles (>11 mg/kg lipid), at least 29/60 (48%) of resting females had not off-loaded their pollutant burden via gestation and primarily lactation. Where data were available, these non-offloading females were previously gravid, which suggests foetal or newborn mortality. Furthermore, a lower pregnancy rate of 50% was estimated for "healthy" females that died of traumatic causes of death, compared to other populations. Whether or not PCBs are part of an underlying mechanism, we used individual PCB burdens to show further evidence of reproductive failure in the North-east Atlantic harbour porpoise population, results that should inform conservation management.

KW - bottle-nosed dolphins

KW - California Sea Lions

KW - endocrine-disrupting chemicals

KW - persistent organic pollutants

KW - St-Lawrence Estuary

KW - mink mustela-vison

KW - polychlorinated-biphenyls

KW - Zalophus-Californianus

KW - tursiops-truncatus

KW - delphinus-delphis

U2 - 10.1371/journal.pone.0131085

DO - 10.1371/journal.pone.0131085

M3 - Article

VL - 10

JO - PloS ONE

JF - PloS ONE

SN - 1932-6203

IS - 7

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ER -