Persistent Chemicals in the Marine Ecosystem

Author(s): David Epel and Welton L. Lee

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Persistent Chemicals
In the Marine Ecosystem
DAVIDEPELand WELTONL. LEE,Hopkins Marine Station of Stanford University, Pacific Grove, Calif.

W ho, 50 years ago, could have predicted that man freshwater, estuarine, coastal-oceanic, and open-
would walk on the moon by 1969? Who, 20 years oceanic. Remarkably, the extent of contamination
ago, could have predicted that man would pollute of freshwater, estuarine, and coastal organisms is
the entire globe, including the 71% of it covered by quite similar. Although less marked, the contamina-
the seas, with a single family of chemical com- tion of open-ocean organisms is also highly sig-
pounds? Both have now happened. The zenith and nificant.
nadir of man's activities have resulted in his at- How has this worldwide contamination of organ-
taining the moon and at the same time fouling the isms by DDT occurred? Are these DDT levels suf-
oceans. ficient to cause damage? If so, what kind of damage
In this article we will review the evidence for can we expect to see? To answer these questions,
the pollution of the oceans by persistent chemicals. we must first know something about the chlorinated
As the chlorinated hydrocarbons, especially DDT, hydrocarbons-especially their chemical stability,
are probably the most widely distributed and best- mobility, and solubility properties, and their basic
studied group, we shall here use DDT as a "mod- toxicology.
el" persistent chemical. We shall detail how such Persistence. Because many of the chlorinated
chemical contamination occurs, what these chemi- hydrocarbons are chemically stable, some of the
cals are doing, and what must be done if a viable DDT sprayed in 1945 is still with us in 1970. Al-
oceanic and global ecosystem is to be maintained. though the environmental half-life of DDT is not
accurately known, estimates range between 10 and
Background 20 years. Partial degradation, through such pro-
The recent, highly publicized concern about DDT cesses as ultraviolet radiation (Mosier, Guenzi, and
is not simply an amplificationof Silent Spring but a Miller, 1969) and enzymatic breakdown (O'Brien,
frighteningly accurate and well-documented escala- 1967), results in the removal of one chlorine atom,
tion of many of Rachel Carson's charges regarding yielding the compound DDE. This, however, is not
pesticides. Eight years ago Miss Carson had to base a true "degradation:w"DDE is also toxic, although
a number of her arguments on extrapolations of possibly less so than DDT. Indeed, DDE is the
the then limited scientific literature on pesticides. derivative most commonly encountered in the mar-
Today, however, a solid body of scientific evidence ine environment and (as will be noted later) may
points to the actual pollution of the oceans by DDT be the primary agent responsible for its biologic
and its derivatives and the resultant destruction of effects on marine organisms.
portions of oceanic food webs by this ubiquitous Mobility. DDT does not stay where it is put. This
compound. is an obvious statement (given the global distribu-
The extent of this pollution is indicated in the tion of DDT), but the mechanism of this distribu-
table. This table reports measurements of DDT tion is not so apparent. Recent research, however,
levels in organisms from three different ecosystems: indicates that the bulk of this "redistribution" oc-

207

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 WIND

CODISTILLATION

RAIN _

BIRDS

PHYTOPLANKTON F

1S RIVERS

ZOOPLANKTON jN**

I 1* j E ; .0 . -FOOD CHAIN

I I 1
g \ , ---DEATH-DECAY

I I &l; * * s

. 1L~ 0 ~~~
ACCUMULATION * *
IN SEDIMENTS INFAUNA FILTERFEEDERS

Modes of transfer of DDTfrom land to sea, and transfer of DDT within the oceanic food-webs. Relative concentration of DDT is
indicated by the size of the solid dots in the organisms.

curs (i) during the actual application process, (ii) rectly by wind, in the form of dust storms. For
through "codistillation" of DDT from the treated example, in agricultural areas with extensive dry
areas into the atmosphere, (iii) thro'ugh agricultural seasons, wind storms kicking up the dry topsoil
runoff, and (iv) through aerial transport of agricul- can carry DDT for very long distances. A well-
tural soil. documented instance is the fallout over Ohio of
The major route of DDT into the oceans appears DDT-laden dust originating in a Texas dust storm.
to be atmospheric (Risebrough et al., 1968a). Thus, Concentration of DDT in these particles was 3 to 80
some DDT never reaches the ground during the ppm (Cohen and Pinkerton, 1966).
spraying operation (Terriere et al., 1966). That Solubility. The solubility properties of DDT are
which does can then evaporate with water back into of critical importance in determining the entry of
the atmosphere through the process of codistillation this material and its derivatives into food chains.
(Acree, Beroza, and Bowman, 1959): although DDT DDT is extremely insoluble in water (1.4 parts per
has a very low vapor pressure, it, along with other billion), but it is highly soluble in fat. Because of
chlorinated hydrocarbons, has the peculiar ability this property, DDT essentially partitions between
to evaporate or codistill with water. As water evap- the physical environment and living organisms, both
orates, the DDT evaporates with it, getting into the plant and animal. In effect, the organisms act as if
air and hence becoming available for distribution they were magnets in their attraction for DDT. As
by wind and air currents. such, the levels of free DDT in water are practically
Another means of DDT dispersal is related to its immeasurable, but levels of DDT in plants and ani-
ability to adsorb to dust or soil particles. Movement mals living in the water can be extremely high.
of these DDT-laden particles results in translocation This direct uptake from water, combined with the
of the pesticide. Thus, agricultural drainage pro- amounts acquired from food intake, results in the
cesses and heavy runoff can transport large amounts "biological magnification" of these compounds as
of DDT into the major rivers and thence into the one moves up the food chain (see fig.).
oceans. Toxicity. Here, of course, is the major reason for
Finally, DDT in soil can also be transported di- our concern. That DDT is toxic to most insects is,

208 THE AMERICANBIOLOGYTEACHER,APRIL 1970

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 of course, obvious; but it is also true that DDT is times in four hours from levels of 0.11 to 0.35 parts
highly toxic to other forms of life as well. Presum- per billion (Sutton, 1969).
ably one would expect that the localized application This direct uptake, however, appears to be only
of the pesticide only to agricultural areas would part of the story. Organisms low in food chains,
assure safety to nontarget organisms. But we have such as zooplankton, contain low levels of DDT
seen that DDT does not stay where it is put: as and the organisms higher in food chains, such as
indicated in the table, it is getting into nontarget fish and birds, contain much higher levels. Here,
organisms. "biological magnification" is taking effect (Wood-
The major problem is that the levels in these well, 1967). Because DDT is only slowly degraded
organisms are sufficiently high to yield both acute and is stored in fat, most of the DDT consumed
and chronic effects. For example, in the case of in the diet by an organism remains with that or-
robins feeding on insects around DDT-treated elm ganism. Because of what might be called "biological
trees, the accumulation of DDT is rapid enough to economics" the food chain amplifies the extremely
yield acute toxicity and death (Wurster, Wurster, small environmental levels into the very large
and Strickland, 1965). Although accumulation of amounts found in the organisms. Thus, at the tops
DDT is much slower in oceanic organisms, small of food chains, fish and birds can contain DDT at
amounts accumulated over a lifetime can also build levels of tens or hundreds of parts per million.
up to toxic levels. Such toxic doses, normally stored
in the fat and hence not available to assert their Effects on Nontarget Organisms
toxicity, can be released into the bloodstream during Birds. The most critical aspect of this problem
periods of starvation, migration, or other instances is the effects of DDT on birds, fish, and other ma-
of fat mobilization. At such times acute toxicity rine organisms. There is evidence for both acute
and death may ensue (Hunt et al., 1969).
and chronic toxicity in seabirds. Last spring we
The symptoms of acute toxicity are obvious, and
observed large numbers of cormorants and murres
if large numbers of deaths from DDT-poisoning
dead or dying on California beaches. Those that we
were occurring we would all be well aware of it
saw dying had nervous tremors similar to those
and would be doing something about it. The critical
associated with DDT poisoning. Analyses of these
problem, however, appears to be chronic toxicity. birds revealed extremely high levels of DDT in the
Because the symptoms can be difficult to observe,
liver and other organs (Mascovich, 1969). These
recognition of the problem often requires extensive birds were emaciated: it is possible that the incle-
scientific investigation. Such investigations indicate
ment weather and difficulty in feeding had resulted
that chronic poisoning is occurring and is of the in mobilization of fat, release of stored DDT into
gravest import, since it now appears to be affecting the bloodstream, and a resultant acute DDT toxic-
a good part of marine food chains. ity.
More insidious and perhaps more important is
Accumulation in the Ocean . . . the chronic toxicity that has also been found in
Knowing the properties of DDT, we can now birds. Chronic toxicity is most evident in its effect
ask how DDT gets into the oceans and oceanic or- on reproduction. For reasons not yet completely
ganisms and what its effects might be. The figure understood, high DDT levels tend to cause birds
diagrammatically depicts the modes by which DDT to produce thin eggshells. This relationship has now
is transferred from land to sea: release into the been directly tested in kestrels (Porter and Wie-
wind during direct spraying, coevaporation from meyer, 1969). Birds fed low levels of DDT in their
soil into the air, and transport from river and diet possessed eggshells that were significantly thin-
drainage systems. Although the inputs from rivers ner than those of the controls. In most cases these
are significant, evidence indicates that the major thin eggshells are either crushed by the weight of
source of DDT is atmospheric. Carried around the the parent or else desiccation occurs, bringing about
earth in the same pattern as radioactive fallout, the death of the embryo. This thin-eggshell syn-
this DDT comes down in dust-fall or rainfall drome has now been found in most birds high
(Wheatley and Hardman, 1965). in the food chain, such as birds of prey and fish-
eating birds. Thus, many populations of the pere-
. . .and in Marine Organisms grine falcon, bald eagle, osprey, and brown pelican
have been found to have significantly thinner egg-
Given the fact that DDT accumulates in the shells and to be suffering from reproductive failure
oceans, how does it then get into oceanic organisms? (Ratcliffe, 1967; Hickey, and Anderson, 1968; Rise-
Initially, direct uptake from the seawater is in- brough, 1969). A tragic example is the pelican rook-
volved. In experiments conducted last spring at the ery on Anacapa Island, off Santa Barbara: in a
Hopkins Marine Station, it was found that copepods survey of the 300 birds nesting this past spring,
could concentrate DDT 10,000 times from levels of Risebrough found only 12 intact eggs; and of these,
one part per billion in the seawater (Baumgartel, only three hatched. Most of the pelicans were
1969). Similarly, fish liver concentrated DDT 240 either sitting on damaged eggs or had already given

PERSISTENTCHEMICALSIN THE MARINEECOSYSTEM 209

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DDT Levels in Freshwater, Estuarine, and Oceanic Organisms up nesting. In the latter cases the remnants of
Reference numerous thin-shelled eggs were found near the
DDT (see nests.
fppm) footnotes)
Freshwater fishes (flesh) Thin eggshells result from interference with cal-
Largemouth bass (Calif.) 1.97 1 cium deposition through the effects of DDT on
Channel catfish (Calif.) 4.02 1 estrogen metabolism (Welch, Levin, and Conney,
White catfish (Calif.) 1.01 1 1969) or on thyroid metabolism (Jefferies and
Yellow Perch (Calif.) 0.07 1
Rainbow trout (Calif.) 0.17 1 French, 1969), or by inhibition of the enzyme car-
Coho salmon (Lake Michigan) 10 2 bonic anhydrase by DDT (Keller, 1952). The latter
Atlantic coast estuary treated with DDT enzyme is involved in deposition of the calcium
for mosquito control (DDT values for carbonate of the eggshell (Van Goor, 1947).
whole organism)
Zooplankton 0.04 3 Fish. It is well known that low concentrations of
Shrimp 0.16 3 DDT can result in the acute poisoning and death of
Mud-snail 0.26 3 many species of fish. Such acute poisoning,however,
3-spine stickleback 0.26 3
0.94 3 may not be critical in the oceans. What may be
Sheepshead minnow
Summer flounder 1.28 3 critical, though, is chronic toxicity-especially as it
Atlantic needlefish 2.07 3 relates to reproduction. For example, in lake trout
Common tern 3.15-5.17 3 low DDT levels (0.5 to 2.9 ppm) in ova can affect
Herring gull 3.52-18.5 3
4.75-6.40 3 development (Burdick et al., 1964). Here, as in many
Least tern
Pacific Ocean, coastal (levels for whole fish, embryonic nourishment is obtained from the
animal unless stated otherwise) yolk. The bulk of the DDT originally present in the
Mytilus californianus egg also remains in this lipid-rich sac. Thus, as the
(common mussel) 0.019-0.120 4,5 yolk is utilized the DDT concentration of the re-
Pisaster ochraceus
(common starfish) 0.020 4 maining yolk becomes higher and higher. Finally,
Thais emarginata as the yolk is completely absorbed, there occurs a
(short-spired purple snail) 0.094-0.163 4 large amount of DDT release into the larvae. At
Loligo opalescens (squid) 0.028 4 this point, if the DDT level is too great, death will
Sand crab 0.080-0.220 6
Rock crab (eggs) 0.491-0.500 7 occur. Burdick and co-workers found this critical
Northern anchovy level to be 2.9 ppm in larvae from upper New York
San Francisco 0.59 1 state; but in Alberta, Canada, a similar study
Monterey 0.90 1 showed the critical level to be between 0.3 and
Morro Bay 3.04 1
Los Angeles 14.00 1 0.6 ppm (Currier, Keith, and Stone, 1967). It is also
English sole possible that even if the fish survives this critical
San Francisco 0.55 8 period, behavioral alterations will occur; for exam-
Monterey 0.76 8 ple, temperature-selection ability of salmon is im-
Shiner perch (San Francisco) 1.17 8
Jack mackerel (Santa Barbara) 0.56 8 paired if salmon are exposed to very low DDT
Bluefin tuna (Baja California) 0.56 8 levels (Ogilvie and Anderson, 1965).
Western gull 9.20 9 Other Organisms. Farther down the food chain
Western gull (liver), dead bird 800 10 are the zooplankton-important as a major link
Cassin's auklet 1.0-15.4 4
Brandt's cormorant 4.4 4 between phytoplankton and the larger animals.
Brown pelican (breast muscle) 84.4 4 Most of the zooplankton are arthropods; therefore
Pacific Ocean, open seas they, like insects, may be prime targets for DDT
Yellowfin tuna effects. Here, too, there may also be chronic ef-
Galapagos 0.07 8
Central America (90?W, 8?N) 0.62 8 fects on reproduction. A study by the California
Skipjack tuna Department of Fish and Game (reported in the
Hawaii 0.057 8 San Francisco Chronicle, May 3, 1969) showed that
Galapagos 0.056 8 the large decrease in the crab fishery of San Fran-
Ecuador 0.029 8
1.0 4
cisco Bay may have resulted from embryonic mor-
Red phalarope
Fulmar 1.9 4 tality due to DDT in the crab eggs.
Sooty shearwater 8.4 4 One step lower in the food chain are the phyto-
Slender-billed shearwater 32.0 4 plankton. These organisms, fortunately, contain the
See in references: lowest levels of DDT at the moment. We say "for-
1. Keith and Hunt, 1966. tunately" because it has been found that DDT in-
2. Johnson, 1969.
3. Woodwell, Wurster, and Isaacson, 1967. hibits photosynthesis of phytoplankton.Further ex-
4. Risebrough et al., 1967. periments, made last spring at the Hopkins Marine
5. Davis, 1969. Station, showed that DDE also inhibits photosyn-
6. King, 1969. thesis and that the inhibition was three times greater
7. Hansen, 1969.
8. Risebrough, 1969. than with DDT (Bailey, 1969). If DDT levels con-
9. Risebrough et al., 1968. tinue to increase there could be serious trouble.
10. Mascovich. 1969. Besides the fact that marine phytoplankton supply

210 THE AMERICANBIOLOGYTEACHER,APRIL 1970

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some 70% of the world's oxygen productionby pho- The lessons from the DDT episode are clear.
tosynthesis, any decrease in productivity of this base First, any chemicals with the properties of DDT
of most oceanic food chains could have drastic ef- will end up in the ocean and be concentrated by its
fects on the entire marine system. organisms. Second, emphasis on acute toxicity is a
woefully inadequate criterion of safety: chronic ef-
Prospects fects can be more dangerous but more difficult to
The elimination of the use of DDT in U.S. agri- observe. Unless we want a dead ocean, steps must
culture by 1971, announced in November by the be taken to limit or eliminate thb use and release
Secretary of Health, Education, and Welfare, is an of persistent chemicals.
important step in decreasing the contamination of
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Scientific American 216(3):24-31. When disposing of larger quantities of pesticides,
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concentration of a persistent insecticide. Science 156:821- McDaniel. The service may accept pesticides and
824. bury them in an area remote from water. Do not
WURSTER,C. F., D. H. WURSTER, and W. N. STRICKLAND.1965. remove the chemical from its container. Wrap the
Bird mortality after spraying for Dutch elm disease with container in several layers of newspapers and put
DDT. Science 148:90-91.
it in a tightly covered garbagecan.
Where proper dump facilities are not available
you may be able to bury these chemicals safely
Alaska Featuredin Booklet by following certain procedures. Select a dry area
which has a low water table and is away from wells.
Alaska's turbulent and colorful history, its na-
Clay soils are usually much safer than lighter, sandy
tive people, its mineral wealth and wildlife, its
soils for burying pesticides. Dig a hole large enough
water and power resources, and its natural beauty
for the container as well as the pesticide in a single
are set forth in the 76 pages of Natural Resources
layer of soil. This layer should be at least 18 inches
of Alaska, the most recent booklet in the Depart-
below the surface. You will also need some calcium
ment of the Interior's series on the natural re-
hydroxide (hydrated lime) equal in volume to the
sources of the states.
pesticide. Pour one-half of the lime into the bottom
Many people think of Alaska as a wilderness of
of the hole. Place the pesticide and container on
snow and ice. There are world-famous glaciers, but
top of the lime-making sure the container is open
they cover only 3% of the "Great Land." There are
-and cover it with the remaining lime. Then fill the
also luxuriant forests of hemlock and Sitka spruce.
hole with dirt, making a mound on top so that
Parts of Alaska are as modern as tomorrow. In
water will run off to the sides.
Anchorage, for example, commuters fighting traffic
snarls are aided by helicopter radio broadcasts, as When handling pesticides, always use the same
are their counterparts/in many large cities in the precautionsthat would be taken if spraying, McDan-
"Lower 48." Still the "Cheechako" (newcomer) of- iel stresses. Follow the directions on the label. Glass
ten expects to find everyone traveling by dogsled, and metal containers should be rinsed at least twice
living in igloos, and eating whale blubber. with water when emptied at spraying. The rinse
Prepared with the help of the Forest Service, water should be run through the sprayer. This will
the Soil Conservation Service, and the Army Corps remove most of the pesticide remaining in the con-
of Engineers, the amply illustrated booklet may be tainer and it is one of the safest means of disposal.
purchased for 65? from the Superintendent of Docu- Puncture and destroy your metal containers, if
ments, U.S. Government Printing Office, Washing- possible. But do not puncture or burn pressurized
ton, D.C. 20402. Previously published booklets on cans. Also, pesticide containers should never be
Washington, Colorado, Montana, Oregon, New Mex- reused for other purposes. When properly rinsed,
ico, and Idaho (each 50?), Arizona, Massachusetts, punctured, or broken, the glass and metal con-
Ohio, West Virginia, Nevada, Utah, and Texas (each tainers should not create a problem if left for regular
45?), and California (60?) are also available. garbage pickup.

212 THE AMERICANBIOLOGYTEACHER,APRIL 1970

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