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 Foodweb
http://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‖
Aldrin
Chlordane
DDT
Dieldrin
Endrin
HCB
Heptachlor
Mirex
Toxaphene
PCBs
Dioxins
Furans
www.epd.gov.hk
 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: http://romepointseals.org/Blubber%20Crop.jpg

– Rate of uptake, metabolism and elimination More blubber can mean more
toxic contaminants stored!

– 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).
 Biomagnification in
Different Foodwebs
Ecosystems close to POP sources show the
highest environmental levels of POPs and the
highest concentrations in their resident
organisms.
http://www.jazzhostels.com/blog/wp-content/gallery/skyline/new-york-city-skyline.jpg

BUT
Due to the semi-volatile, ubiquitous nature of
POPs they are now found EVERYWHERE!

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.
 Tanabe, 2002:

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

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

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. 2007
Fig. 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 Foodweb
Unique 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 increased
ttp://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?