ECOTOXICOLOGICAL IMPLICATIONS OF BIOAVAILABILITY

Peter M. Chapman Golder Associates Ltd. North Vancouver, BC, Canada

November 9, 2005, Newark, NY

Two Considerations: First Consideration

BIOAVAILABILITY: WHAT WE WANT TO PROTECT

Human Toxicology: ¾Protect 100% of one species Ecological Toxicology (Ecotoxicology): ¾Protect x% of many species ¾Protect x% of individuals of each

species ¾Protect 100% of endangered species ¾Protect populations / communities, not

individuals

“That depends a good deal on where you want to

get to.”

Second Consideration:

Lewis Carroll: Alice’s Adventures in Wonderland

“Would you tell me please which way I ought to go

from here?”

Key Terms

Bioaccessible: Potentially available for uptakeover the long-term. Fraction that may be available to an organism. Includes portionthat is currently bioavailable + portion(s) thatmay become bioavailable over time

Bioavailable: Immediately available for uptakeby organisms

Bioabsorbed: Actually taken up by anorganism

Bioreactive: Actually able to cause toxicity (thebioabsorbed fraction minus the fraction that is depurated, internally sequestered, or used bythe organism for its own needs)

What is “Bioavailability”? ¾ A substance is bioavailable if it can be

adsorbed or absorbed by an organismwith the potential for distribution,metabolism, elimination andbioaccumulation

¾ Bioavailability simply means that asubstance can be taken up by anorganism; there are no implicationsregarding what may or may not occuronce the substance enters biologicaltissues

¾ Bioavailability is a prerequisite for toxicity

¾ The next question is whether or not abioavailable substance is also bioreactive

What is “Bioreactivity”?

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A substance that is bioavailable to an organism is not necessarily bioreactive once it is within the organism

Bioreactivity refers effectively to bioavailability within an organism

Substances can be sequestered and rendered inert within organisms, which means they are not bioreactive

Bioreactive substances are or can become active within an organism; they are not inert

Bioreactivity is a prerequisite for toxicity

Three Compartment Model

Bioavailability is Affected By:

Chemistry ¾Physico-chemical conditions ¾Environmental compartment Biology ¾

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Route of exposure (e.g., viarespiratory surfaces or viadigestion) Biological interactions (includingbehavior)

BLM: A Conceptual Model Can be any relevant surface on an

organism

BIOAVAILABILITY IS AFFECTED BY MODE OF ENTRY / EXPOSURE

Chemical Contaminationof Ecosystems

1 Terrestrial .,.,. Surface

Water

) " 2 3

'f

Surficial Sediment

Deep Sediment

5 ,,.

Processes

1. Wet or dry deposition (e.g., rain , run-off, dust)

2. Settling/sorption

3. Resuspension (e.g., bioturbation, bioirrigation, scouring, desorption)

4. Burial/mixing

5. Burial

Chemical Contamination of Ecosystems

1 Terrestrial _}I,,.. Surface

Water

) ' 2 3

',. Surficial

Sediment

Deep Sediment

Processes

1. Wet or dry deposition (e.g., rain, run-off, dust)

2. Settling/sorption

3. Resuspension (e.g., bioturbation, bioirrigation, scouring, desorption)

4. Burial/mixing

5. Burial

ROPCs

• Mammals/birds eating aquatic biota

• Fish

• Invertebrates

• Plants

• Algae

1 Terrestrial -"'r

Surface Water

2 ..41'

3,,. Surficial

Sediment

Deep Sediment

Chemical Contamination of Ecosystems Processes

1. Wet or dry deposition (e.g., rain, run-off, dust)

2. Settling/sorption

3. Resuspension (e.'g., bioturbation, bioirrigation, scouring, desorption)

4. Burial/mixing

5. Burial

ROPCs

• Mammals/birds eating aquatic biota

• Fish

• Invertebrates

• Plants

• Algae

Other Stressors

Climate change

Habitat change

Introduced species

Eutrophication

Sediment TransportHydrodynamic Chemical Fate Speciation Bioaccumulation

& Toxicity

Air

Water

Sediment

Hydrodynamics

Suspended solids

Dissolved

Particulate

Dissolved

Particulate

Free

Complexed

Free

Complexed

Environmental Conditions Affect Bioavailability

10

100

1000

96-h

LC

50 (

ug/

l C

u)

Site Lab

10 100 1000

hardness (mg/l as CaCO3)

Sample Determination of a Water-Effect Ratio, WIE.R

Site water LC50 = 350 ~giL copper

Toxicity in site~ water witln added copper. 350 pg/L

W ER = = 3.5 100 ~g/L

Laboratory water LC50 = 100 IJQ/L copper

Tox icity' in IIaboratory water wi t:h added copper.

17

Me

TIEM

PO

Transformación

BIODISPONIBILIDADMe++ Puede ser tóxico

Transformaciónde-mobilización

MENOS BIODISPONIBLE Menos probablede ser tó xico omplejo MeMe

Transformaciónre-solubilización

BIODISPONIBLE Puede stóxico

er

Me++Me++

Transformations Affect Bioavailability EV

ALU

AC

IÓN

DE

RIE

SGO

ID

ENTI

FIC

AC

IÓN

DEL

PEL

IGR

O

C

SUBSTANCIA solubilización

Partitioning and Speciation Affect Bioavailability

Controls on Contaminant “Bioavailability”

¾Chemical state - e.g., paint chips, lead shot, tar balls, metal ore,soot, pitch or coke globules ¾Nature of sediment matrix

- e.g., black carbon, peat, wood chips ¾Biological degradation and

tolerance (acclimation,adaptation) mechanisms,and biota behavior

Bioavailability of Organic Substances

Cornelissen G, Gustafsson O, Bucheli TD, Jonker MTO, van Noort PCM. 2005. Extensive sorption of organic compounds to blackcarbon, coal, and kerogen in sediments and soils: Mechanisms and consequences fordistribution, bioaccumulation and degradation. Environ Sci Technol 39(18): 6881-6895

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Sorption of organic chemicals via “dual-modesorption” – absorption in amorphous organic matter and to carbonaceous materials (e.g., blackcarbon) Solid-phase concentrations “bear little or norelation to actual concentrations in organisms” –reconsider existing sediment / soil criteria Freely dissolved concentrations most important

Organism Behavior Affects Bioavailability

These striking contrasts in behaviour…

vs.

have implications for bioavailability

Plant Roots Affect Bioavailability

Metals ¾Roots exude organic compounds

that complex metals at therhizosphere

Organics ¾Roots influence the distribution of

organochlorine pesticides and probably also other organicsubstances

“Bioavailability” Differs Between Species

ffect

edAt

rcen

eP

1

0.9

0.8

0.7

0.6

0.5

0.4

0.3

0.2

0.1

0

Cladocerans All Invertebrates Crustaceans (Excluding CladoceransInsects

1 10 100 1000 10000 100000 Copper, µg/L

Bioavailability - Environmental Compartment

¾ Are deeper sediments contaminatedand potentially toxic?

and

¾ Are deeper sediments likely to beuncovered under one or more reasonably possible set ofcircumstances?

If so, then contaminants in these sediments are potentiallybioavailable

A7

~-:-=--~---------'~ ~ "··.___~------ ·­.... . -.. .,.,_

·-

-,

...._ ·.,·-.

····-.. '•.

Site

Figur~e 6 : Total Chrom1um 2001, 5-10 em

Legend:

Q Nat Tested

al:ove E~L. he1Q,., E~M (>BZ..:370 rng~Kg)

Figurf: 4: Amphipod Morta1tty 5-10 em

Legend:

Q Na\T~~d

0 0-25'll. comblrl~ M'MI!Iity

“BIOAVAILABILITY”CAN VARY

TEMPORALLY AND BETWEEN ECOSYSTEMS

“BIOAVAILABILITY” CAN VARY

TEMPORALLY AND BETWEEN ECOSYSTEMS

SPECIES SENSITIVITY

DISTRIBUTIONS (SSDs)

SPECIES SENSITIVITY

DISTRIBUTIONS (SSDs)

SPECIES SENSITIVITY

DISTRIBUTIONS (SSDs)

SPECIES SENSITIVITY

DISTRIBUTIONS (SSDs)

HC5 VALUES: 95% CL

HC50 VALUES: 95% CL

Relative Sensitivities (HC50 values)

METAL MOST SENSITIVE

LEAST SENSITIVE

Cu Polar/ Temperate

Tropical

Cd Tropical Polar

Zn Temperate Polar

Pb Temperate Polar

Bioreactivity is affected by:

¾Route of exposure (gut vs gills) ¾Depuration and sequestration

mechanisms ¾Concentrations of that substance

already in the organism (e.g.,spillover effect formetallothionein) ¾Adaptation/acclimation (if not

behavioral, affects bioreactivity, notbioavailability)

Bioreactivity of Metals in Organisms ¾

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1. Detoxified and not bioreactive: metals bound to inducible metal-binding proteins such as metallothionein (MT) or precipitated into insoluble concretions consisting of metal-rich granules (MRG) – virtually unlimited potential for metal absorption for marine invertebrates 2. Metabolically active and bioreactive: metals in metal-sensitive fractions (MSF) such as organelles and heat-sensitive proteins. Species-specific differences in relative proportion of bioreactive metals Trophic transfer of metals to predators: MSF and MT represent tropically available metal (TAM); MRG is not trophically available. Thus “total tissue burdens in prey may not directlyrelate to metal transfer to predators” (Wallaceand Luoma 2003)

Bioreactivity Affected by Uptake Route

Ball AL, Borgmann U, Dixon DG. In review. Toxicity of dietary cadmium to Hyalella azteca. Aquat. Toxicol.

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Growth more sensitive than survival (survival more sensitive for water exposures) No relationship between toxicity and Cd accumulation (relationship established for water exposures)

Biological Strategies – Contaminant Exposure

Inducible Strategies Constitutive Strategies

Changes in behaviour, physiology or biochemistry

Morphological, physiological or biochemical features

Occur only after exposure initiated Persist irrespective of exposure

No performance trade-off Possible fitness disadvantage in absence of stress

Often occur after a measurable time-lag

No time-lag

Example: avoidance (energetically easiest for fish)

Example: metallothionein to detoxify metals

Bioavailability: We Can Get There From Here

“That depends a good deal on where you want to

get to.”

“Would you tell me please which way I ought to go

from here?”

Questions / Discussion?