Biomagnification in Marine

Ecosystems

By Angela Leemhuis Hansen

Biomagnification• Xenobiotic compounds

– POPs and others

– Properties

– Current events

• Bioaccumulation

– Biomagnification vs.

bioconcentration

– Contaminant load: Effects

• Different foodwebs

• Goerke, et al. 2004 Biomagnification in the

Antarctic Foodwebhttp://www.mpv-sam.com/img/WhereCanITrainFish.gif

Xenobiotic compounds

• From the greek xenos ―stranger‖ and biotic

―related to living beings‖

• A chemical (natural or man-made) which is found

in an organism, but not normally produced or

expected to be there.

– Persistent organic pollutants (POPs)

– Some heavy metals (Hg, Pb, etc.)

– Heavy isotopes (14C, 15N, etc.)

– Natural toxins (phytoplankton toxins)

– Alien hormones (sewage exposure)

Persistent Organic Pollutants• Recalcitrant: Compounds which persist in the

environment and increase in concentrations with time.

• Ubiquitous: Widespread, semi-volatile, found

everywhere.

• Lipophilic: Dissolves in, or has an affinity for lipids.

Higher trophic levels have more lipids. Hydrophobic.

• High fugacity: Ability to move from one compartment

to another, estimated with the octanol-water partition

coefficient (Kow) or air (KOA).

• Toxic: High molecular mass, endocrine disrupters.

Stockholm Convention on POPs• 1995: The Governing Council of the United Nations Environment

Programme (UNEP) called for global action on "chemical substances

that persist in the environment, bio-accumulate through food webs,

and pose a risk of causing adverse effects to human health and the

environment".

• Intergovernmental Forum on Chemical Safety (IFCS) and the

International Programme on Chemical Safety (IPCS) prepared an

assessment of the 12 worst offenders.

• 2001-2004: Negotiations completed on 23 May 2001 in Stockholm.

Came into force on 17 May 2004. Co-signatories agreed to outlaw

nine of the dirty dozen chemicals, limit the use of DDT, and curtail

the production of dioxins and furans.

• 2009: Nine additional POPs were added on 8 May 2009.

―The Dirty Dozen‖

www.epd.gov.hk

Aldrin

Chlordane

DDT

Dieldrin

Endrin

HCB

Heptachlor

Mirex

Toxaphene

PCBs

Dioxins

Furans

The Ocean: The Sink full of Soup

• The ultimate destination for most persistent

anthropogenic substances

• Substances with long residence times can

cause serious harm to biota

• Substances can interact:

– Plastics are known to adsorb

hydrophobic pollutants (Moore, 2008)

Not everything in the ocean belongs there! Plastic bags are particularly troublesome.

Bioaccumulation• The uptake of a xenobiotic compound by an

organism from the abiotic environment and

biotic environments (all sources).

– Bioconcentration is uptake directly from the

abiotic environment (surrounding water), resulting

in a higher concentration in the organism. This is

the most common process for marine organisms up

to and including fish (water breathing) (Gray,2002).

Water breathing animals from phytoplankton to inverts to fish can be affected by contaminants in the water, sediments and in their food.

Bioaccumulation

– Biomagnification is uptake from food to the

consumer, resulting in a higher concentration in

the consumer. This is clearly shown as the only

route for air-breathing marine animals such as

birds and marine mammals (Gray, 2002).

http://farm1.static.flickr.com/118/296212100_f12a51442a.jpg http://neveryetmelted.com/wp-images/LeopardSeal.jpg http://topnews.in/law/files/Whale-Eating-Whale.jpg

Air breathing animals are affected primarily by contaminants in their food.

Contaminant Load

• Determined by:

– Rate of uptake, metabolism and elimination

– Affected by trophic level, environmental

conditions, specie, size/lipid content and life history traits

– Chemical qualities of the contaminant (KOW and KOA).

• Deleterious effects (sub-lethal and lethal):

– Reproduction (impairment, reduced success)

– Development (weakness, endocrine disruption)

– Immune system (stress, infection, cancer, death)

• POPs accumulate in feathers, eggs, milk, liver, kidney

and fat storage/blubber (high lipid content).

http://romepointseals.org/Blubber%20Crop.jpg

More blubber can mean more toxic contaminants stored!

Biomagnification in

Different FoodwebsEcosystems close to POP sources show the

highest environmental levels of POPs and the

highest concentrations in their resident

organisms.

BUT

Due to the semi-volatile, ubiquitous nature of

POPs they are now found EVERYWHERE!

http://www.jazzhostels.com/blog/wp-content/gallery/skyline/new-york-city-skyline.jpg

http://room42.wikispaces.com/file/view/tundra-climate.jpg/33454003/tundra-climate.jpg

South to North Pacific

Tanabe, 2002: Fig. 5. PCBs concentrations in mammals

and birds collected from Japan and nearby seas.

http://i.dailymail.co.uk/i/pix/2009/10/09/article-1219251-06C2AD22000005DC-653_634x381_popup.jpg

Tanabe, 2002:

Fig. 9. Comparison of toxicity equivalents (TEQ) values (pg/g fat weight) of dioxins and related compounds in humans and wildlife.

Location, location, location. You’re not just what you eat but where you eat it too!

Arctic Foodweb

http://www.greenfacts.org/en/arctic-climate-change/figtableboxes/arctic-marine-food-web.htm

Arctic Foodwebs

Kelly, et al. 2007Fig. 1. Relationship between

observed tissue residue

concentrations (ng·g–1 lipid

equivalent) and trophic level

for PCB 153 (a high KOW,

high KOA compound) and

ß-HCH (a low KOW, high

KOA compound) in Arctic

organisms of the piscivorous

(A), terrestrial (B), and

marine mammalian (C) food

webs. Data represent

geometric means ± 1 SD.

Arctic Foodweb

http://www.alaska-in-pictures.com/gray-whale-carcass-with-polar-bears-north-slope-alaska-6728-pictures.htm

Antarctic FoodwebUnique environment:

• Remoteness, proves the persistence and long-

range transport of POPs.

• With the absence of point emissions or of

river input to the Southern Ocean,

contaminants found in fauna reflect global

pollution levels, and recent uses in the

southern hemisphere.

• Few studies done for POPs over a time-series.

Antarctic Foodweb• Goerke, et al. 2004

– Sampled from 1986-2000

– Most recalcitrant POPs: HCB,

p,p'-DDE, Mirex, PCB,

chlordane

– 11 species: 2 inverts (krill and

squid), 6 fish (benthic and

surface), 1 bird (Adelie

penguin), and 2 pinnipeds

(Weddell and elephant seals)

– Samples were normalised to

lipid content.

Temporal trend results

Goerke, et al. 2004

Fig. 2. Concentrations of

organochlorine

compounds in livers of

three Antarctic fish

species from 1987 and

1996. Heavy lines

indicate statistically

significant differences (t-

test, P=0.05). Bars

represent standard errors

of the means.

Concentration

patterns in organisms

Fig. 3. Concentration

patterns of

organochlorine

compounds in Antarctic

species of different

trophic levels. Bars

represent means and

standard deviations.

Bold numbers indicate

biomagnification factors

in relation to krill. (I)

Herbivore, (II) 1st level

carnivore, (III) 2nd level

carnivore.

Antarctic Foodweb

• Results: Goerke, et al. 2004

–Benthic and fish feeding fish had higher

contaminant loads for most POPs than krill

feeders (vertical transport of POPs from the

surface to the benthos accumulating in the

sediments).

– Increase in contaminant load over time

observed (due to redistribution and recent

uses in the southern hemisphere)

–Mirex and chlordane most increasedttp://www.sycelandine.com/log/?m=200904

Antarctic Foodweb• Goerke, et al. 2004

– Biomagnification observed with increasing

strength in mackerel icefish, adelie penguins, and

both pinnipeds.

– The pinnipeds showed high biomagnification for

all POPs except HCB (special metabolic ability

suspected), not seen in cetaceans.

– Biomonitoring should include multiple taxa

– POPs in antarctic fish were 1-2 orders of

magnitude lower than northern hemisphere fish

– POPs rising here...diminishing there.

―Biomagnification occurs when contaminants that don’t easily

degrade increase with each link of a food chain. In seawater,

these persistent molecules stick to small particles and

phytoplankton. Small fish eat the phytoplankton, but the

contaminants can’t be broken down and are absorbed, intact,

by the fish. When small fish are eaten by larger predators, the

process repeats—again and again, up the food chain. Each

subsequent predator receives a higher dose than the previous

one. Animals at the top of the food chain, such as dolphins,

receive the most concentrated dose of these contaminants with

every meal.‖ (Illustration by E. Paul Oberlander, Woods Hole Oceanographic Institution)

Questions?

References

• Chiou, C.T. 1985 Partition coefficients of organic compounds in lipid-water

systems and correlations with fish bioconcentration factors. Environ. Sci. Technol.

19: 57-62.

• Goerke, H., Weber, K., Bornemann, H., Ramdohr, S., Ploetz, J. 2004. Increasing

levels and biomagnification of persistent organic pollutants (POPs) in Antarctic

biota. Marine Pollution Bulletin. 48: 295-302.

• Gray, J.S. 2002. Biomagnification in marine systems: the perspective of an

ecologist. Marine Pollution Bulletin. 45: 46-52

• Kelly, B.C., Ikonomou, M.G., Blair, J.D., Morin, A.E., Gobas, F.A.P.C. 2007. Food

web-specific biomagnification of persistent organic pollutants. Science. 317: 236-

239.

• Moore, C.J. 2008. Synthetic polymers in the marine environment: A rapidly

increasing, long term threat. Environmental Science. 108: 131-139.

• Tanabe, S. 2002. Contamination and toxic effects of persistent endocrine disrupters

in marine mammals and birds. Marine Pollution Bulletin. 45: 69-77.

Notes for presentation

Introduction

Today we will be discussing the biomagnification of compounds in the marine environment, the significance and intricacies of the

process, the effects on biota.

First we will cover the types of compounds that biomagnify, called xenobiotic compounds, their properties and some current events

that have made them of such interest to the scientific community now. Then we will cover the differences of

bioaccumulation, bioconcentration and biomagnifications (yes, they are three different things). We will briefly discuss

contaminant loads and their effect on an organism’s health. Then we will take a look at biomagnifications trends in different

foodwebs. And finally we will take a look at a paper by Helmut Goerke, et al., 2004, Increasing levels and biomagnifications

of persistent organic pollutants in Antarctic biota.

Xenobiotic compounds

The word xenobiotic comes from the greek xeno, meaning stranger or foreigner, and biotic, meaning related to living beings.

Xenobiotic compounds are any chemical or element which is found in an organism, but which is not normally produced by it,

or expected to be there. Xenobiotic compounds include persistent organic pollutants which are anthropogenic (man-made),

some heavy metals such as mercury and lead, heavy isotopes such as 15N and 14C, natural toxins that build-up in a predator

from eating it’s prey such as phytoplankton toxins, and even alien hormones which refers to human hormones found in fish

that live downstream from sewage outlets. We will be focusing on persistent organic pollutants, or POPs.

Persistent organic pollutants

Persistent organic pollutants are recalcitrant, which means that they persist in the environment and increase in concentration

over time. They are ubiquitous, which means they are widespread across the plant and within all the oceans. This is a

function of their persistence in the environment and that many POPs are semi-volatile, which mean they easily evaporate and

move with global air-circulation patterns. They are lipophilic, which means they dissolve in lipids, have an affinity for lipids,

and are hydrophobic, so they won’t dissolve in water. Instead they will stick to other things they come in contact with in the

water column (particulate matter, organisms, etc.). They have a high fugacity, or ability to move from one compartment to

another (across lipid layers), and this is expressed with the octanol-water and octanol-air coefficients. We will see more about

this later. And lastly, due to their unnaturally high molecular masses they are generally very toxic to organisms, and can act

as endocrine disrupters.

Stockholm Convention on POPs

In 1995 the governing council of the United Nations Environment Programme (UNEP) called for global action on "chemical

substances that persist in the environment, bio-accumulate through food webs, and pose a risk of causing adverse effects to

human health and the environment". In response the Intergovernmental Forum on Chemical Safety (IFCS) and the

International Programme on Chemical Safety (IPCS) prepared an assessment of the 12 worst offenders, which we now call

the “dirty dozen”. Negotiations were completed on 23 May 2001 in Stockholm, to come into force on 17 May 2004, and the

co-signatories agreed to outlaw nine of the dirty dozen chemicals, limit the use of DDT, and curtail the production of dioxins

and furans. On May 8, 2009 nine additional POPs were added to the list, and countries are still negotiating over them.

The Dirty Dozen

This is an educational brochure from the government of Hong Kong explaining POPs, the Stockholm convention, and how

Hong Kong is in the forefront when it comes to adhering to the Stockholm Convention and being environmentally friendly. I

found it interesting and amusing.

The Ocean: The sink full of soup

Biomagnification has been observed in the terrestrial environment for much longer than in the marine environment. Actually,

some scientists originally thought biomagnifications would not occur in marine systems because of the dilution of

compounds, and the openness of marine foodwebs. Unfortunately for the ocean this has turned out to not be true. The ocean

is the ultimate sink for just about all man-made compounds, and because we make things to last, they tend to have long

residence times in the ocean. Some even interact. Seabird research has shown a correlation between PCB levels in birds and

the amount of plastic they have in their stomachs. Plastic polymers, which have a very long residence time in the water

column, are now known to adsorb hydrophobic pollutants (POPs) like little sponges. When the plastic is consumed by the

less-picky eaters of the ocean (which is most of them) they are also exposed to the toxins stuck to the plastic.

Bioaccumulation

Bioaccumulation is the uptake of xenobiotic compounds by an organism from all sources in its environment. From the water

directly, as well as from food sources. Bioconcentration is the passive uptake from the surrounding water only, which occurs

readily across respiratory surfaces of water-breathing invertebrates and vertebrates. Elimination also occurs across these

respiratory surfaces, but generally decreases in rate with increasing organism size. The lipid content of the organism is also a

factor in retention.

Biomagnification is the uptake from food only, when the consumer ends up with a higher concentration of the compound than was

found in the prey. This is the only pathway for air-breathing marine animals to accumulate compounds. Here ar some pictures

of air-breathing marine wildlife: a bird eating a fish, a leopard seal eating a penguin, and an orca eating a seal.

Contaminant load

Contaminant load is the over-all concentrations of contaminants, such as POPs, in an organism. It is determined by rates of

uptake, metabolism and elimination of the organism. Also, life history traits such as life-span, size, trophic level, species,

lipid content, and environmental conditions. The chemical properties of the contaminants are also important. The detrimental

effects of contaminants are many. Reproductive health and success are reduced, development can be affected by endocrine

disruption or reduced fitness. Immune impairment is a common side-effect with increased stress levels, disease and infection

incidence, cancer and even death. POPs do not collect evenly within an organism, they tend to gather in lipid rich parts of the

body (blubber/fat deposits, liver, kidney), and are even offloaded (feathers, eggs, milk, offspring).

Biomagnification in different foodwebs

POPs are highest in concentration closest to their sources, but there is not truly pristine environments left. They are found

everywhere now. Observe the trends in the POP concentration data from Tanabe, 2002 off the coast of Japan and nearby seas.

Observe the differences between the piscivorous, terrestrial and marine mammal food webs in the Arctic, by Kelly, et al.

2007. Fin whales, a stork, and polar bears eating.

The Antarctic foodweb is unique because there is no near-by sources of pollution. POPs found here prove the persistence and

long-range transport of them. There are also few studies investigating POP levels in the Antarctic.

Goerke, et al. 2004

The Antarctic foodweb biomagnifications study of eleven different species: krill, squid, six types of fish, the adelie penguin,

weddell seals and elephant seals. Samples were taken from 1986 to 2000, and normalized to lipid content so that the POP

levels found would be comparable. Only the most recalcitrant POPs were tested for: HCB, DDT, Mirex, PCB and chlordanes.

Temporal trends can be seen here, with Mirex, and chlordane metabolites having the most increase with time in these three

fish species.

Different POP concentrations were found in different species: see the trends in HCB and DDT from krill up to weddell seals.

Benthic and fish feeding fish were found to have higher contaminant loads than krill feeder, this probably has to do with the

vertical transport of POPs to the seafloor, where they accumulate in the sediments.

There was an increase in contaminant levels observed over time in Antarctica, demonstrating the increased use of POPs in the

Southern hemisphere and the redistribution of old POPs from other regions. Mirex and chlordane were both the most

increased, and they are known to be in current use in the Southern hemisphere.

Conclusions: Biomagnification was observed in the foodweb. Biomonitoring should include more than one taxa for each

trophic level due to differences in elimination abilities. POP levels in the Antarctic are 1-2 orders of magnitude lower than in

the Northern hemisphere, but they are increasing, while in the Northern hemisphere levels are decreasing.

Conclusion

So, to recap, in simple terms, “Biomagnification occurs when contaminants that don’t easily degrade increase with each link

of a food chain. In seawater, these persistent molecules stick to small particles and phytoplankton. Small fish eat the

phytoplankton, but the contaminants can’t be broken down and are absorbed, intact, by the fish. When small fish are eaten by

larger predators, the process repeats—again and again, up the food chain. Each subsequent predator receives a higher dose

than the previous one. Animals at the top of the food chain, such as dolphins, receive the most concentrated dose of these

contaminants with every meal.” (Woods Hole Oceanographic Institution) Biomagnification is of most significance in

foodwebs with air-breathing constituents; but as we saw from Goerke, it is observed in water-breathing benthic fish as well.

Questions?