Using predatory birds to monitor long term trends
of PBDEs in the UK
John D. Crosse1,2,, Richard F. Shore1, Richard A. Wadsworth1, Kevin C.
Jones2 & M. Glória Pereira1
1. NERC Centre for Ecology & Hydrology, Lancaster Environment Centre, Library Avenue, Bailrigg, Lancaster, LA1 4AP, U.K.
2. Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, U.K.
Overview
• PBDEs
• What they are
• Usage and consumption
• Environmental occurrence
• Why we should care
• Environmental monitoring
• Using apex predators (birds and their eggs)
• Results from two UK birds
 Spatial trends (marine, terrestrial)
 Temporal trends
 Toxicity
PBDEs
• Additive flame retardants
– Not chemically bonded to host matrix
• Disrupt combustion
– Dilute flammable gases
– Scavenge free radicals
• Used in high impact plastics, textiles, furniture foam
• Release to environment from product manufacture, use,
disposal
– Continual release through normal usage
PBDEs
• Structurally and chemically analogous to PCBs
• 209 theoretical congeners
– 28, 47, 99, 100, 153, 154, 183, 196,197, 201, 202, 203, 209
• Technical products utilise a mixture of congeners
– PeBDE (99,47), OBDE (183, 209), DeBDE (209)
Drivers for changes in PBDE usage
• Series of fire disasters in the UK and Ireland
– Summerland 1973, Taunton train fire 1978, Woolworth’s
department store fire 1979, Stardust discotheque fire 1981,
Bradford City football stadium fire 1985, King’s Cross
Underground fire 1987
– Over 150 people died
– Rapid spread of fire, production of toxic smoke
• Furniture and Furnishings Fire Safety Regulations
(FFFSR), 1988
• RoHS, EEC Directive EEC793/93
• EEC proposes ban on penta- and octa-BDEs, 2001
PBDE consumption
Prevedouros et at., 2004
Cycling of PBDEs
Wet & dry
Deposition
Photolysis
Volatile/
particulate
emissions/dust
Production
/incorporation
into
consumables
Commercial
products
Shipping /
Drilling
Agricultural
Soils
Consumption &
metabolism by
plants & animals
Sea
Consumption and
metabolism by
humans
WWTP
Water
courses
Fish
Industrial
effluents
PBDEs are everywhere
• Persistent
• Subject to long range transport
• Lipophilic and bioaccumulative
• Are toxic
• Found in all environmental compartments
• Found in places where they have never been used
• Found in unborn children
• Growing evidence of toxicity
Examples of human toxicity
• Chromosomal damage and genotoxicity at low doses
– (Barber at al., 2006; Llabjani et al., 2011)
• Cytotoxicity
– (He et al., 2008)
• Apoptosis and genotoxicity in a dose dependant manner
– (Song et al., 2009;
• Cellular changes in DNA/RNA reflecting a genotoxic
mechanism – (Llabjani et al., 2011)
• Competitive binding with T4 to plasma thyroid hormonetransporter transthyretin (TTR)
– (Athanasidou et al., 2008; Lacorte & Ikonomou, 2009; Ryden et al., 2012)
Specific examples in predatory birds
• Henny et al., (2009)
– Osprey
– Reduced productivity (concs >1ug/g wwt)
• McKernan et al., (2009)
– American kestrel
– Decreased pipping and hatching success (concs 10-20ug/g)
• Fernie et al., 2005, 2008, 2009 ; Marteinson et al., 2010
– American kestrel - Concs 0.2 – 2.1 ug/g)
– Delayed hatching, reduced pair bonding, shell thinning
• Llabjani et al., 2012
– DNA/RNA effects
– Low doses (10-9, 10-12 M)
Legislation
• Penta and Octa BDE mixtures now ‘banned’
• Inclusion into the Stockholm Convention on POPs
– Tetra, Penta, Hexa, Hepta BDEs
– Annex A (Elimination)
• OC pesticides and PCBs
• Deca BDE now prohibited in EU in electrical goods
– ~80% of usage
– Subject to voluntary phase-outs in the US
• All formulations still in circulation in consumer goods
• Reoccurrence through recycled plastic?
Predatory
Bird Monitoringsampling
Scheme (PBMS)
Environmental
Air
Top predator
Soil
Water
Terrestrial biota
Aquatic biota
• Occupy a high trophic position
• Representative of a whole ecosystem
Predatory Bird Monitoring
PBMS Scheme (PBMS)
• Long term, national scale
• Funded by CEH, NE, EA,
CRRU, RSPB
• Chemical surveillance and
monitoring in sentinel species
• SGARs, POPs, Trace & toxic
metals, PAHs
• Aims: identify hazards, assess risk, quantify environmental
drivers, inform policy, evaluate mitigation, assess risks to high
priority species
• Tissue and egg archive for monitoring and research
Predatory birds as Biomonitoring tools
• Why use predatory birds?
– High trophic position
– Integrated sentinel – more representative of the
ecosystem as a whole
– Sparrowhawks = terrestrial
– Gannets = Marine
• Why use eggs?
– Consistent media
– Easy to collect
– Long running archive ~1970-present
– Good accumulators of lipophilic contaminants
How does the
pbms
How
it work?
works
5
liver concentration (µg/g)
Publication
Sample
archive
PM examination
sparrowhawk
4
3
2
Chemical analysis
1
0
70
75
80
85
90
95
2000 2005
Data
analysis
3
liver concentration (µg/g)
Volunteer
submission
kestrel
2
1
0
1960
1970
1980
1990
2000
Study 1 - Gannets
• Marine sentinels
– Two colonies; Bass Rock and Ailsa
Craig
– Historically contaminated waters
– Eggs from 1977-2007
• Specific aims
– Spatial differences
– Temporal trends
• PBDE concentration
• PBDE congeners
• BDE209 was not analysed as a 209 was
not detected by Leslie et al., 2011 in a
subsample of these eggs
• Toxicity
– Shell thickness
Study 1 - Results
• Congener profile
– PeBDE dominated
• Spatial trends
– No significant spatial trends
– ΣPBDE or congeners
• Temporal trends
– Significant temporal trends
– Rapid increase from 1980s
– Peak in 1994, before declining
– Higher brominated congeners
increase over time
Study 1 - Results
• Toxicity
– Overall concentrations
relatively low
– 12.9 - 66.8 ng/g in eggs
from Bass Rock
– 6.3 to 60.8 ng/g in eggs
from Ailsa Craig
– No effect on eggshell
thickness or volume
Study 1 - Results
Study 1 - Results
75
1200
ΣPBDE
Bass
Ailsa
Consumption
1000
60
ng/gWwt
45
600
30
400
15
200
0
0
1977
1981
1985
1987
1990
1992
1994
1998
2002
2006/7
Consumption (tonnes)
800
Factors affecting consumption in the UK
• Legislative drivers
– For and against
ΣPBDE
Bass
Ailsa
Consumption
1200
Newton
Aycliffe closes
Scrutiny under
RoHS
60
1000
800
45
ng/gWwt
Dumping at
sea banned
600
30
400
15
200
Fire safety law
FFFRS
0
0
1977
1981
1985
1987
1990
1992
1994
1998
2002
• Environmental concentrations respond rapidly
2006/7
Consumption (tonnes)
75
PeBDE &
OBDE banned
Summary
• No spatial differences
– North Sea and Irish Sea exhibit similar
levels of contamination
• Congeners associated with PeBDE
– BDE47 most dominant congener
• Temporal changes
– Marine environmental concentrations
respond rapidly to change
– Increase in higher brominated congeners
over time
• Toxicity
– No significant effect on egg volume or
shell thickness
Study 2 - sparrowhawks
• Terrestrial raptor
• Wide geographic distribution
• Long running archive
– 1985 - 2007
• Specific aims
– Temporal trends
• PBDE concentration
• PBDE congeners
• BDE209 was not analysed for as this
analysis was being conducted by Jacob de
Boer’s group (Leslie et al., 2011)
• Toxicity
– Shell thickness
Sample selection
• Criteria 1
– 1985-2007 (encompassing
major legislation)
– ~5 eggs per year
• Criteria 2
– Smallest geographical area
possible
Results
• Concentrations
– 34 – 2281 ng/g wwt
– Several orders of magnitude higher than the gannets
• Congener profile
– BDE 99 dominant congener
– BDEs 99>47>153>100>154 dominated the
PBDE profile
• Smaller contributions of BDEs 28, 85, 138
– All congeners co-correlated with each other and
with ΣPBDE concentrations (p<0.001)
– Very similar to PeBDE mixture
– Similar profile to that found in prey sp (Van den Steen
et al., 2009)
Results: Congener profile
100%
90%
Relative abundance
80%
70%
Octa
60%
Other
50%
BDE154
40%
BDE100
30%
BDE153
20%
BDE47
10%
BDE99
0%
– No significant decline
1990
1995
2000
2005
2010
-0.3
y = 0.0223x - 44.586
R² = 0.3909
-0.45
6
y = 0.1941x - 383.6
R² = 0.3679
4
2
0
1980
1985
1990
1995
2000
2005
y = 0.1672x - 330.84
R² = 0.2274
2
1985
1990
1995
4
2
1980
1985
1990
1995
2000
2005
2010
BDE153
6
y = 0.1636x - 322.5
R² = 0.2202
4
2
0
1980
1985
1990
1995
2000
2005
2010
8
4
0
1980
y = 0.2562x - 505.48
R² = 0.4636
6
2010
BDE154
6
BDE99
Conc (ng/g - Box-Cox transformed)
BDE100
Conc (ng/g - Box-Cox transformed)
1985
Conc (ng/g - Box-Cox transformed)
– BDE concentrations
remained high from
mid 1990s onwards
8
BDE47
-0.15
Conc (ng/g - Box-Cox transformed)
– Similar pattern for
BDEs 47, 99, 100,
153, 154
0
1980
Conc (ng/g - Box-Cox transformed)
• Linear increase of
ΣPBDE concentrations
until mid 1990s
(R2=0.39, F1,42=17.5,
P<0.001)
Conc (ng/g - Box-Cox transformed)
Temporal trends
2000
2005
2010
ΣPBDE
6
4
2
0
1980
y = 0.1815x - 355.93
R² = 0.3895
1985
1990
1995
2000
2005
2010
6
Conc (ng/g - Box-Cox transformed)
BDE196
BDE197
0
1980
1985
1990
1995
2000
2005
2010
-0.3
3
-0.6
0
1980
-0.9
1985
1990
1995
2000
2005
2010
y = 0.0587x - 116.87
R² = 0.1145
-3
-1.2
BDE202
2
1985
1990
1995
2000
2005
2010
-2
-4
y = 0.1124x - 224.06
R² = 0.4036
0
1985
1990
1995
2000
2005
2010
-2
y = 0.0853x - 170.83
R² = 0.1698
-4
BDE203
Conc (ng/g - BoxCox transformed)
2
Conc (ng/g - BoxCox transformed)
4
0
1980
y = 0.0085x - 17.672
R² = 0.1046
-1.5
BDE201
Conc (ng/g - BoxCox transformed)
• OBDE-associated
BDEs196, 197,
201, 202, 203
increased linearly
over time
(R2≤0.40,
F1,42≤27.75, P<0.05)
Conc (ng/g - Box-Cox transformed)
Temporal trends
2
0
1980
1985
1990
1995
2000
2005
2010
-2
-4
y = 0.0841x - 168.46
R² = 0.3127
Toxicity
• ΣPBDE in sparrowhawk eggs ranged from 0.34-2.28
ug/g wet weight (wwt)
– 0.27-27.4 ug/g (lipid weight)
• Exceed the threshold for shell thinning and reproductive
impairment found in other raptors (Fernie et al., 2009; Henny et al.,
2009; Marteinson et al., 2010)
• No relationship between ΣPBDE nor individual
congeners on sparrowhawk eggshell thickness (p>0.05)
– Shell thickness increasing over time (R2=11.4, F1, 37=5, P<0.05)
• Eggs collected represent failed or abandoned eggs
– May not be associated with PBDEs
Summary
• Concentrations in sparrowhawk eggs represent
environmental concentrations during the breeding season
• PBDE concentrations are not declining in sparrowhawk eggs
– Slow clearance from the terrestrial system
– Stark contrast to the marine system and other studies
• Dominated by PeBDE mix congeners
– BDE99
– Input from OBDE congeners
– Slower clearance of these congeners
• Concentration of heavy BDEs increasing
– BDE209 detected in a subsample of eggs
– Debromination of labile BDE209
Summary (continued)
• Concentrations amongst the highest ever reported in bird
eggs
– Exceed threshold for shell thinning and impaired reproductive
output
– We did not find any effect of PBDEs on shell thinning
– Difficult to relate cause and effect of PBDE concentrations on egg
failures
What’s next?
• DeBDE being phased out in US
– UK following
– New flame retardants already on the market
• PBT, PBEB, HBB, DP, BTBPE, OBIND, TBPAE, TBECH, BATE, DBDPE
– DecaBromoDiphenylEthane
– Replacement for DecaBromoDiphenylEther (DeBDE)
DeBDE (209)
DBDPE
A long way from home…
TBECH
ATE
DBDPE
A long way from home…
Acknowledgements
• NERC & PBMS
–
–
–
–
–
CEH
Natural England
RSPB
EA
CRRU
• Lancaster University (CCM)
• Volunteers who collected the eggs
• Everyone else who helped out
–
–
–
–
Dave Hughes and Lee Walker
Dr Sabino Del Vento
Dr Jasmin Schuster
Dr Gareth Thomas
Thanks for
listening!