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. 2016 Jan 14;6:18573.
doi: 10.1038/srep18573.

PCB Pollution Continues to Impact Populations of Orcas and Other Dolphins in European Waters

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PCB Pollution Continues to Impact Populations of Orcas and Other Dolphins in European Waters

Paul D Jepson et al. Sci Rep. .
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Abstract

Organochlorine (OC) pesticides and the more persistent polychlorinated biphenyls (PCBs) have well-established dose-dependent toxicities to birds, fish and mammals in experimental studies, but the actual impact of OC pollutants on European marine top predators remains unknown. Here we show that several cetacean species have very high mean blubber PCB concentrations likely to cause population declines and suppress population recovery. In a large pan-European meta-analysis of stranded (n = 929) or biopsied (n = 152) cetaceans, three out of four species:- striped dolphins (SDs), bottlenose dolphins (BNDs) and killer whales (KWs) had mean PCB levels that markedly exceeded all known marine mammal PCB toxicity thresholds. Some locations (e.g. western Mediterranean Sea, south-west Iberian Peninsula) are global PCB "hotspots" for marine mammals. Blubber PCB concentrations initially declined following a mid-1980s EU ban, but have since stabilised in UK harbour porpoises and SDs in the western Mediterranean Sea. Some small or declining populations of BNDs and KWs in the NE Atlantic were associated with low recruitment, consistent with PCB-induced reproductive toxicity. Despite regulations and mitigation measures to reduce PCB pollution, their biomagnification in marine food webs continues to cause severe impacts among cetacean top predators in European seas.

Figures

Figure 1
Figure 1. Temporal trends in ∑PCBs in UK-stranded harbour porpoise (Phocoena phocoena) and striped dolphins (Stenella coeruleoalba) in the western Mediterranean Sea.
To assess the ∑PCBs trend we have fitted a Generalised Additive Model (GAM) to the data using the R (R Development Core Team, 2013) package mgcv. We used thin plate regression splines to do the smoothing and the degree of smoothing was determined by generalised cross validation. (A) Ln ∑PCBs (sum 18–25CB) mg/kg lipid concentrations in UK harbour porpoise blubber against date for all data for 1990–2012 (n = 706). The continuous line represents the smoothed trend from a Generalized Additive Model fitted to the data. The trend is statistically significant (p < 0.001, F = 11.76, residual df = 701.97, trend df = 3.03) against the null hypothesis of no trend. The dashed lines represent the 95% bootstrapped Confidence Intervals. The yellow line represents ln ∑PCBs equivalent to 20.0 mg/kg lipid and the red line 40 mg/kg lipid. (B) Ln ∑PCBs (sum 18–25CB) lipid concentrations in biopsied striped dolphin blubber from the Mediterranean Sea against date for all data for 1990–2009 (n = 220). Figure shows the natural logs (ln) of the whole data set plotted against the date found. The continuous line represents the smoothed trend from a Generalized Additive Model fitted to the data. The trend is statistically significant (p < 0.001, F = 55.45, residual df = 212.03, trend df = 6.97) against the null hypothesis of no trend. The dashed lines represent the 95% bootstrapped Confidence Intervals. The yellow line represents ln ∑PCBs equivalent to 20.0 mg/kg lipid and the red line 40 mg/kg lipid.
Figure 2
Figure 2. Mean ∑PCBs concentrations in male and female cetaceans (four species; all ages) The blue bars are males and the grey bars are females.
The lower line is the equivalent ∑PCBs concentrations threshold (9.0 mg/kg lipid) for onset of physiological effects in experimental marine mammal studies. The upper line is the equivalent ∑PCBs concentrations threshold (41.0 mg/kg lipid) for the highest PCB toxicity threshold published for marine mammals based on marked reproductive impairment in ringed seals in the Baltic Sea. Mean ∑PCBs concentrations in male (n = 388) and female (n = 318) UK-stranded harbour porpoises (HPs) in 1990–2012. Mean blubber ∑PCBs (mg/kg lipid) concentrations in subsets of male (n = 201) and female (n = 144) UK-stranded HPs that died of acute physical trauma and male (n = 120) and female (n = 132) HPs that died of infectious disease from the same 1990–2012 period. Mean blubber ∑PCBs (mg/kg lipid) concentrations (1990–2012) shown for stranded/biopsied male (n = 29) and female (n = 17) bottlenose dolphins (BNDs) from UK and Ireland; male (n = 28) and female (n = 24) BNDs from Atlantic coast of Spain and Portugal and male (n = 9) and female (n = 11) BNDs from western Mediterranean Sea. Male (n = 50) and female (n = 39) striped dolphins from western Mediterranean Sea (1991–2009) and male (n = 5) and female (n = 19) KWs from NE Atlantic (1994–2012). Error bars = 1Standard Error of the Mean (SEM).
Figure 3
Figure 3. Mean ∑PCBs concentrations in male and female cetaceans (four species; adults only).
The blue bars are adult males and the grey bars are adult females. The lower line is the equivalent ∑PCBs concentrations threshold (9.0 mg/kg lipid) for onset of physiological effects in experimental marine mammal studies. The upper line is the equivalent ∑PCBs concentrations threshold (41.0 mg/kg lipid) for the highest PCB toxicity threshold published for marine mammals based on marked reproductive impairment in ringed seals in the Baltic Sea. Mean ∑PCBs concentrations (mg/kg lipid) in adult male (n = 146) and female (n = 134) UK-stranded harbour porpoises in 1990–2012. Mean blubber ∑PCBs (mg/kg lipid) concentrations (1990–2012) shown for stranded/biopsied adult male (n = 20) and female (n = 14) bottlenose dolphins from UK and Ireland and the Atlantic coast of Spain and Portugal (NE Atlantic). Mean blubber ∑PCBs (mg/kg lipid) concentrations shown for adult male (n = 8) and female (n = 14) striped dolphins from the western Mediterranean Sea (1991–2009). Finally, mean blubber ∑PCBs (mg/kg lipid) concentrations shown for adult male (n = 3) and female (n = 18) killer whales from the NE Atlantic (1994–2012). Error bars = 1SEM.
Figure 4
Figure 4. Mean ∑PCBs concentrations in male and female cetaceans (four species; juveniles only).
The blue bars are juvenile males and the grey bars are juvenile females. The lower line is the equivalent ∑PCBs concentrations threshold (9.0 mg/kg lipid) for onset of physiological effects in experimental marine mammal studies. The upper line is the equivalent ∑PCBs concentrations threshold (41.0 mg/kg lipid) for the highest PCB toxicity threshold published for marine mammals based on marked reproductive impairment in ringed seals in the Baltic Sea. Mean ∑PCBs concentrations (mg/kg lipid) in juvenile male (n = 233) and female (n = 180) UK-stranded harbour porpoises (HPs) in 1990–2012. Mean blubber ∑PCBs (mg/kg lipid) concentrations (1990–2012) shown for stranded/biopsied juvenile male (n = 20) and female (n = 14) bottlenose dolphins from UK and Ireland and the Atlantic coast of Spain and Portugal (NE Atlantic). Mean blubber ∑PCBs (mg/kg lipid) concentrations shown for juvenile male (n = 17) and female (n = 15) striped dolphins from western Mediterranean Sea (1991–2009). Finally, mean blubber ∑PCBs (mg/kg lipid) concentrations shown for juvenile male (n = 2) and female (n = 0) killer whales from NE Atlantic (1994–2012). Error bars = 1SEM.
Figure 5
Figure 5. Mean ∑PCBs concentrations in male and female cetaceans (three species; sexual maturity unknown).
The blue bars are males and the grey bars are females. The lower line is the equivalent ∑PCBs concentrations threshold (9.0 mg/kg lipid) for onset of physiological effects in experimental marine mammal studies. The upper line is the equivalent ∑PCBs concentrations threshold (41.0 mg/kg lipid) for the highest PCB toxicity threshold published for marine mammals based on marked reproductive impairment in ringed seals in the Baltic Sea. Mean ∑PCBs concentrations (mg/kg lipid) in male (n = 9) and female (n = 4) UK-stranded harbour porpoises of unknown sexual maturity (1990–2012). Mean blubber ∑PCBs (mg/kg lipid) concentrations (1990–2012) shown for stranded/biopsied male (n = 16) and female (n = 13) bottlenose dolphins (BNDs) from the Atlantic coast of Spain and Portugal and male (n = 8) and female (n = 11) BNDs from the western Mediterranean Sea (all sexual maturity unknown). Mean blubber ∑PCBs (mg/kg lipid) concentrations shown for male (n = 25) and female (n = 10) striped dolphins from western Mediterranean Sea (1991–2009) (sexual maturity unknown). Error bars = 1SEM.
Figure 6
Figure 6
(A–D) Distribution map (smooth mean density kernel plots) of ∑PCBs data points in Europe – all cetacean species (all ages) from 1996–2012. (A) – HPs (n = 548); (B) – BNDs (n = 110); (C) – SDs (n = 71) and (D) – KWs (n = 21). Spatial distribution of ∑PCB lipid concentrations produced in Esri ArcMap 10.1 (www.esri.com). Maps are displayed in the WGS84 co-ordinate system. Data points are shown along with local averages. These averages were calculated by kernel smoothing using a polynomial order 5 kernel with power = 0, ridge parameter = 50 and bandwidth based on the spatial distribution of the observations for each species: bottlenose dolphin 0.75 degrees; harbour porpoise 0.5 degrees; killer whale 1.2 degrees; striped dolphin 0.5 degrees. Both the data points and the local averages are displayed in three colours: yellow (∑PCB concentration =  < 20 mg/kg); orange (∑PCB concentration = 20–40 mg/kg lw); and red (∑PCB concentration =  > 40 mg/kg lw).
Figure 7
Figure 7. Mean ∑PCB concentrations in stranded and biopsied BNDs (1990–2012), SDs (1991–2009) and KWs (1994–2012) – all cetacean species (all ages).
The blue bars are males and the grey bars are females. The lower line is the equivalent ∑PCBs concentrations threshold (9.0 mg/kg lipid) for onset of physiological effects in experimental marine mammal studies. The upper line is the equivalent ∑PCBs concentrations threshold (41.0 mg/kg lipid) for the highest PCB toxicity threshold published for marine mammals based on marked reproductive impairment in ringed seals in the Baltic Sea. Error bars = 1SEM.
Figure 8
Figure 8
(A–D) Box and whisker plots for male (M) v female (F) v unknown sex (U) were generated for ∑PCB and ln ∑PCB concentrations for (A) all stranded HPs (1990–2012); (B) stranded or biopsied SDs (1990–2008); (C) stranded or biopsied BNDs (1990–2012); and (D) stranded or biopsied KWs (1994–2012). The lower line (blue) is the lower PCB toxicity threshold (=9.0 mg/kg lipid, as ∑PCB) for onset of physiological effects in experimental marine mammal studies. The upper line is the highest PCB toxicity threshold (=41.0 mg/kg lipid, as ∑PCB) published for marine mammals based on marked reproductive impairment in ringed seals in the Baltic Sea.

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