Jennifer McIntyre (NOAA): influence of water chemistry on copper ...
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SWASSW | Jenifer McIntyre | Dec. 4 2013
David Baldwin, Nat Scholz - NOAA-Fisheries, NWFSC
The influence of water chemistry on copper neurotoxicity in fish
Ph
oto
by
Mo
rgan
Bo
nd
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Copper is neurotoxic
Peripheral sensory system
Mechanosensation (lateral line)
Olfaction (smell)
Gustation (taste)
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Olfaction begins at olfactory rosettes
Kuhlia sandvicensis
Anguilla anguilla
Lepisosteus platostomus Eleotris sandwicensis
Hansen &
Zielinski. 2005. J.Neurocytol. 34
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Olfactory Sensory Neurons
Microvillous
Ciliated Non-
sensory
Hansen & Zielinski. 2005. J.Neurocytol. 34
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Cross-Species Cu Toxicity
All sensitive to olfactory toxicity at
low ppb dissolved Cu
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Bioavailability
Is copper in PNW salmon streams bioavailable to the salmon nose?
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• Biotic Ligand Model (BLM) = classic metals toxicity in fish
Cu+
Cations
Anions
DOM Na+ transporter
Gill
• Water chemistry determines bioavailability
water tissue
Copper Bioavailability - Fish Gill
• Metals compete with cations at the ‘biotic ligand’
• Metals complex with anions & DOM
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Copper Bioavailability – Fish Nose
Odour Receptor Golf
AC
Cation channel
Cl-
Odour molecules
2+
Na+ K+
Do ions & DOM ‘protect’ nose against Cu ?
? Cu+
Cations
Anions
DOM
Nose
ATP
Cl channel
water tissue
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0.2 mM Ca 0.2 mM HCO3 0 mg/L DOM
Dissolved Organic Matter Hardness
[Ca] 0.4 0.8 1.6
Alkalinity
[HCO3] 0.8 1.6 3.2
[Fulvic Acid] 2.5 5
10
[Natural Organic Matter]
10 Hi pH Low pH
Low-ion Control
+
One of 3 increases
Copper Bioavailability in Different Waters
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• pre-exposure to artificial test water (24-h)
Odour exposure •L-serine, TCA: 10 s each •Alternating odour pulses every 2.5 min.
Fish placed on ‘rig’
• Test water over nose • Measure electrical
response to odours • 15 min acclimation • 30 min Cu exposure
(20 μg/L)
Bioavailability Study Design
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Water Quality on Copper Neurotoxicity
•20 μg/L Cu (30 min) significantly inhibits
olfaction of L-ser (and TCA)
•Olfaction improves with ↑ calcium,
bicarbonate, and DOC
•DOC has strongest effect
[Calcium] mM0.0 0.4 0.8 1.2 1.6
020406080
100120 Hardness
[HCO3-] mM0 1 2 3
020406080
100120 Alkalinity
Normal pHLow pH
[DOC] mg/L0 2 4 6
020406080
100120 Dissolved Organic Carbon
Fulvic AcidNOM
% R
elat
ive
Olfa
ctor
y R
espo
nse
No-copper control 95% L.C.L. control
McIntyre et al. 2008. ES&T. 42
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Fathead minnow corroboration
0 0.1
10 0.1
ppb Cu mM Ca
10 0.5
10 1.0
1.2 1.0 0.8 0.6 0.4 0.2
0
Green et al. 2010. ES&T 44
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Hardness & Alkalinity in PNW Streams
Only 1 stream sample (<1%) had enough bicarbonate for 50% protection
No streams contain enough calcium for even 50% protection
Puget Sound
Cal
cium
(mM
)
0
1
2
3
4
5SacramentoYakimaWillamette
Puget Sound
Bic
arbo
nate
(mM
)
0
2
4
6
8
10
12
14
95% SER
50% SER
Willamette Yakima Sacramento
Copper toxicity reduced 50%
Copper nontoxic
Copper toxicity reduced 50%
Copper nontoxic
McIntyre et al. 2008. ES&T. 42
HC
O3- (
mM
)
C
alci
um (m
M)
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DOC in PNW Streams
Puget Sound
DO
C (m
g/L)
0
2
4
6
8
10
12Willamette Yakima Sacramento
DOC should be measured along with dissolved copper concentrations in streams of concern
Copper toxicity reduced 50%
Copper nontoxic
19% of samples
6% of samples
McIntyre et al. 2008. ES&T. 42
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DOC protective at: • Fish gill Less protective at: • Nose
Hardness effect similar at: • Gill • Nose
Little protection at: • Nose
Alkalinity • Very protective at fish gill
Water Chemistry Comparison: Gill vs Nose
McIntyre et al. 2008. EST 42
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A
B
C
Copper Toxicity to Lateral Line
Linbo et al. 2006. ET&C
Control Fish Copper-exposed
Danio rerio larva
Hair cells
No hair cells
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Copper Toxicity to Lateral Line
1. Hardness • CaCl2 • MgSO4 • CaCl2:MgSO4 2. Sodium • NaCl • NaHCO3
3. Dissolved organic matter (DOC)
?
Linbo et al. 2009. ETC
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DOC protective at: • Fish gill Less protective at: • Nose
Hardness effect similar at: • Gill • Nose
Little protection at: • Nose
Alkalinity • Very protective at fish gill
Chemistry Comparison
• Lateral line
• Lateral line (Na effect)
• Lateral line McIntyre et al. 2008. EST 42
Mg
Ca
Linb
o et
al.
2009
. ETC
28
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Freshwater Cu Bioavailability
Cu+ DOC
Alkalinity
DOC
Alkalinity
Cu+
Cu Toxicity at Fish Gill Cu Toxicity at Fish Nose (and LL)
Hardness Hardness
Important to measure DOC and alkalinity in receiving waters
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Fresh vs Seawater Cu Bioavailability
Does saltwater protect against copper sensory toxicity?
DOC Cu+
Saltwater Cu Toxicity
CO32- OH-
HCO3- SO4
2-
Ca2+ Mg2+
DOC Cu+
Freshwater Cu Toxicity
CO32- OH-
HCO3- SO4
2-
Ca2+ Mg2+
Na+ Hardness
Alkalinity
Na+
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Important uncertainties relative to toxicity in freshwater
• Salinity - changes in copper complexation, etc.
• DOC influence - changes in copper/DOC interaction
• Physiology - changes in fish upon smolting
Seawater Cu Bioavailability
Olfactory toxicity of copper to seawater-phase salmon
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No olfactory toxicity up to 100 ppb in seawater (35 ppt)
Seawater Cu Bioavailability Baldwin et al. Unpublished results.
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Linbo et al. 2009. ETC 28
Sodium protective against Cu?
436 mM
Copper toxicity to lateral line neurons
EC50 >500 ppb
Cop
per t
oxic
ity (E
C50
ppb
) (NaCl, NaHCO3)
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Measuring Olfactory Response: EOG & EEG
Electro-olfactogram (EOG)
Perfusion Recording electrode
EEG measured at olfactory bulb
Measures changed in electrical current at olfactory epithelium in perfusion water
Measures changed in electrical current at olfactory bulb – no water chemistry interference with recording
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Olfaction important to salmon behaviors Cu Reproductiv
e priming & behaviour
Cu
And/or fry emergence
Olfactory predation cues can alter egg hatch timing
Cu
May interfere with imprinting Cu
Copper may be developmentally neurotoxic Cu
Olfaction required for natal stream
Cu homing
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Cu Sensory Toxicity: Research Needs
• What are current water chemistry conditions (esp. DOC)? • What changes in water chemistry are predicted? • Is olfactory toxicity in adult salmon similar to juveniles? • Species specific measurements for SOC (e.g. sockeye) • Consequences of Cu toxicity to other olfactory behaviors
– Homing – Reproductive priming and behaviors
• Better understanding of mechanosensory toxicity – Testing in salmonids – Functional impairment vs cell death – Survival consequences of mechanosensory impairment
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Acknowledgements
Technical & Field Assistance James Meador (NOAA Fisheries - Montlake) Julann Spromberg NOAA Fisheries – Montlake) Dave Rose (University of Washington) Gordy George (University of Washington) Matt Gilman (WA Dept. Fish & Wildlife) Chris Tatara (NOAA Fisheries - Manchester) Barry Berejikian (NOAA Fisheries - Manchester) Sarah McCarthy (King County – DNR) Evan Malczyk (King County Environmental Lab)
Funding Sources:
NOAA Coastal Storms Program
EPA S.T.A.R. Graduate Fellowship
NOAA Oceans & Human Health
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Olfactory Neuroanatomy
ciliated microvillous crypt
Olfactory Sensory Neuron Types
Bile salts Amino acids Steroids Stimulated By:
Feeding Reproductive Alarm Behaviours:
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4 hr
(Hansen et al. 1999. E
TC 18)
Num
ber o
lfact
ory
neur
ons
Copper impacts olfactory receptors
Epithelium
Copper can destroy olfactory receptors
Rosette
Dendrites with odour receptors
Axon reaching olfactory bulb
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Inhibition of olfaction: • Dose-dependent • Short exposures • Low concentrations
30 min in 10 μg/L Cu
Bal
dwin
et a
l. 20
03.
ET&
C. 2
2:22
66
San
dahl
et a
l. 20
07. E
S&
T
Copper inhibits olfaction Recording electrode
70% inhibition Relative EOG = 0.3
Electro-olfactogram (EOG)