United States
Environmental Protection
Agency
Environmental Research
Laboratory
Duluth MN 55804
Research and Development
EPA-600/S3-84-013 Mar. 1984
&EPA Project Summary
Structure and Organization of
Persistent Aquatic Laboratory
Communities Exposed to the
Insecticide Dieldrin
William J. Liss, Becky L McClurken-Lilley, and Douglas S. Lee
Sixteen aquatic communities com-
posed of persistent populations of
guppies (Poeciliareticulata), amphipods
(Gammarus fasciatus), snails (family
Planorbidae), planaria (Dugesia sp.),
and various microinvertebrates were
established under laboratory conditions.
Eight of these communities received
low energy input with low habitat
availability while the remaining eight
communities had high habitat availabil-
ity and received high energy input. At each
level of input, guppy populations in two
systems were exploited at either 0. 10,
20, or 40 percent of the population bio-
mass each month. Macroinvertebrates
were also sampled monthly for popula-
tion counts and biomass measurements.
After each system reached near steady-
state conditions, 1 /ug/l of dieldrin was
introduced into one system of each
treatment. These systems were allowed
to reach new steady-state conditions.
The response of the systems was
dependent upon both the energy input/
habitat and exploitation levels. The low
energy input/habitat systems were
more sensitive to dieldrin particularly at
higher levels of exploitation. The influence
of organization and environment on
population persistence and system
structure is explored theoretically with
isocline models, and the implications
for aquatic ecology and environmental
management strategies are discussed.
This Project Summary was developed
by EPA 's Environmental Research
Laboratory, Duluth, MN. to announce
key findings of the research project that
is fully documented in a separate report
of the same title (see Project Report
ordering information at back).
Introduction
Management of toxic substances
should be based upon good understand-
ing of their effects not only on individual
organisms but also on populations and
communities. The goal of the research sum-
marized here was to advance understand-
ing of the influence of toxicants on the
structure and organization of aquatic com-
munities. Persistent laboratory communi-
ties maintained under differing environ-
mental conditions were exposed to the or-
ganochlorine insecticide dieldrin. The
conditions included differing levels of
invertebrate habitat availability, differing
rates of energy and material input and
differing rates of population exploitation.
In simple communities, structure may be
taken to refer to the kinds of species found in
the system along with their distribution and
abundance in space and time Organization
is taken to be more of a theoretical concept,
in part entailing how species populations and
their level-specific environments are inter-
related and so incorporated into a system as
a whole.
The theoretical perspective employed in
designing the experiments and interpreting
the results entailed the use of multisteady-
state isocline models (Figure 1). In this
perspective, under differing environmental
states, a community will develop differing
steady-state structures and organizations
and can thus be understood as a multistead-
state system. Dynamics or changes in
structure through time of an n-dimensional
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Low Med High I
Low Med High I
Low Med High I
5 I i I \ ?
.1H
\ \ xs:
4 -
25H
3.5H
5H
Figure 1. P/7ase planes and isocline systems modeling the interrelationships between populations in a system.
E - C ~ H ~ P ~ Ft -1
? + + + +
T
wheie C,H,P. and R comprise the system and E, units of harvesting effort, and I, rate of input of plant resources, are factors in the environment of the
system. A toxicant directly affects only the carnivore population On each phase plane predator biomass is plotted on the y-axis and prey biomass is
plotted on the x-axis. The descending lines identified by different rates of plant resource input, I, are prey isoclines Each prey isocline is defined as a set
of biomasses of predator and prey where the rate of change of prey biomass with time is zero. The ascending lines on each phase plane are predator
isoclines. Each predator isocline is defined as a set of biomasses of predator and prey where the rate of change of predator biomass with time is zero.
Each intersection of a predator and prey isocline is a steady-state point where the rate of change of both predator and prey biomass with time is zero.
The positions and forms of the isoclines can be deduced from equations or sets of graphs representing the rates of gain and loss of each of the
populations. The presence of the toxicant lowers the predator isocline at each E on the C-H phase plane, the extent to which it is lowered depending
upon the effect of the particular toxicant concentration on carnivore growth, reproduction and survival. Steady-state system structure at HIGH I, Of, 07"
(circles); HIGH I, 05, 2T (squares); LOW I, 90E, 2T (triangles) is shown. Trajectories of biomasses of carnivore (C), herbivore (H). plant (P), and plant
resource (R) originating at point 0 are shown to converge on each of these steady-states under each particular set of environmental conditions
community can be understood as a
trajectory in constant pursuit of an n-
dimensional steady-state point whose
location in phase space is continually
changing as a result of changes in
environmental conditions. Toxic substances
change the structure and organization of
systems; these changes can be understood
as alterations of the location of the
system steady-state point in phase space.
The response of the system to a toxicant
is jointly determined by its organization
and conditions in its environment. Under
differing sets of environmental conditions,
a system will respond differently to a
given concentration of toxicant.
Description of Research
Sixteen aquatic communities were
established, each composed of persistent
populations of guppies (Poecilia reticulata),
amphipods (Gammarus fasciatus), snails
(family Planorbidae), planaria (Dugesia
sp.), and benthic microinvertebrates
including flagellates, rotifers, nematodes,
gastrotrichs, and protozoans. Habitat and
escape cover for invertebrates were
provided by a substrate of quartzite
gravel. A gelatinous mixture of 60
percent alfalfa and 40 percent Oregon
Test Diet served as the primary source of
energy and materials.
Each laboratory system was maintained
in a fiberglass tank holding 560 liters of
water, which was continuously exchanged
by a 600 milliliter per minute flow of
heated well water. Fluorescent lighting
was placed above each tank, and light
was maintained at a relatively low level to
prevent the formation of blue-green algae
blooms.
Eight laboratory systems were established
with three circular nests of quartzite
gravel covering 20 percent of the bottom
area of each tank. Each system received a
0.6 gram per tank daily alfalfa-OTD
ration. This treatment is identified as low
energy and material input and low habitat
availability, or LOW I.
In the remaining eight systems, gravel
habitat covered 95 percent of the tank
bottom. Each system received 4.0 grams
of alfalfa-OTD ration daily. This treatment
is identified as HIGH I. In four systems at
HIGH I, planaria, which are effective
predators on amphipods and capable of
completely eliminating them from a
system, were abundant. In the remaining
four, planaria were controlled, their
numbers being kept at very low levels.
At each I, guppy populations in two
systems were exploited at one of four
rates, 0, 10, 20, or 40 percent of the
biomass of the population present at the
time of sampling (OE, 10E, 20E, and 40E,
respectively).
Every 28 days the systems were
sampled and the guppy populations were
exploited at their assigned rates. All
macroinvertebrates were removed, counted,
weighed and replaced in the systems.
Number, biomass, and yield of guppies
were determined.
Dieldrm was introduced into four
systems, one at each exploitation rate, at
both LOW I and HIGH I. When these
systems established near steady-states
(NSS), continuous introduction of one ppb
of dieldrin was begun. NSS structure at
each combination of levels of I and E was
assumed when the trajectories of bio-
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masses of the interacting populations
fluctuated in a very restricted region of
phase space relative to previous fluctua-
tions
Additional experiments were conducted
to determine the extent to which simpler
models of complex systems could provide
some understanding and prediction of
toxicant effects in the more complex
laboratory systems. Accordingly, labora-
tory systems composed of only guppies,
only snails, and guppy and snail popula-
tions together were established These
systems, though smaller and simpler
than the complex laboratory systems,
were still capable of exhibiting population
and simple community response. Effects
in these simpler systems were to be
compared to effects in the more complex
systems. Guppy populations were exploited
at three different rates Two levels of
energy and material input in the form of
an alfalfa-OTD ration were maintained.
Protocol for sampling, exploitation, and
toxicant introduction into these systems
was to be the same as in the more
complex systems. The funding period for
the Cooperative Agreement was shortened,
and time was not available during the
period of the agreement to introduce
toxicant into the simpler systems.
Approximately 18 to 24 months were
required for the more complex laboratory
communities to establish NSS. At differ-
ent levels of habitat (I) and exploitation
(E), the systems established different
NSS structures, in conformity with the
expectations of the multisteady-state
perspective Guppies and snails were
competitors for the alfalfa-OTD ration. At
each I there was an inverse relationship
between NSS guppy and snail biomasses.
Increased E brought about a reduction in
NSS guppy biomass, which was accom-
panied by an increase in the NSS biomass
of the snail competitor. Increased I led to
an increase in the NSS biomasses of both
guppies and snails at each E.
The relationship of amphipods to
guppies and snails is rather complex and
not well understood. Amphipods were
apparently a competitor of guppies and
snails as well as prey of guppies At LOW
I, NSS amphipod biomass was inversely
related to guppy biomass. At HIGH I, in
systems in which planaria were controlled,
changes in NSS guppy biomass brought
about by changes in E had no discerned
effect on amphipod biomass. Because of
the large amount of rock substrate
available as an amphipod refugium at
HIGH I and the greater availability of their
preferred food, the alfalfa ration, guppies
may not have preyed as effectively on
amphipods and thus had little direct
effect on their biomasses
At HIGH I in systems where planaria
were not controlled, amphipod popula-
tions were maintained at very low levels
or driven to extinction by planaria
predation. At each E, snail populations
maintained higher NSS biomasses in
these systems than in systems where
planaria were controlled and the amphi-
pod competitor was abundant.
The simpler laboratory systems also
established NSS. The time required for
these systems to come to NSS was nearly
as long as that required by the complex
laboratory systems. The NSS relation-
ships between guppies and their snail
competitors were similar to those observed
in the more complex systems. The
simpler systems aided in clarifying the
role of guppy-snail competition in organ-
izing the more complex systems. Further,
these systems and the more complex
laboratory communities were useful in
illustrating that system productivity,
expressed as energy and material input I,
predation, exploitation, and competition
operate together to determine system
structure.
Results and Conclusions
Dieldrin altered community structure
and organization, nearly all systems
establishing new NSS's during exposure.
Individual organism experiments conducted
at our laboratory indicated that a dieldrin
concentration of one ppb in the laboratory
systems probably directly affected guppy
survival, growth, and reproduction and
only indirectly affected other populations
through reduction in guppy predation
and/or competition intensity resulting
from reduction in guppy biomass.
The response of the laboratory systems
to continuous exposure to one ppb of
dieldrin was dependent upon the levels of
both I and E. At LOW I, system response to
dieldrin ranged from perturbation and
recovery at OE to guppy populations
extinction at 40E. At LOW I, OE, over a
period of about 12 months of continuous
exposure, guppy biomass was reduced
about 30 percent and amphipod biomass
was slightly increased. While dieldrin
was still being introduced, however, the
system began to recover from perturbation
with guppy biomass gradually increasing.
The structure of the recovering system
eventually overlapped the NSS structure
that existed prior to dieldrin introduction.
At LOW I, 10E, and LOW I, 20E, guppy
biomass was reduced about 30 and 50
percent, respectively Amphipod biomass
increased in both systems, presumably as
a result of reduction in predation and/or
competition intensity resulting from the
decrease in guppy biomass. Dieldrin was
continuously introduced into these
systems for over 18 months. Unlike the
system at OE, these communities did not
show any indication of recovery until
dieldrin introduction was terminated.
At LOW I, 40E the guppy population
became extinct following 15 months of
continuous exposure to dieldrin. After
this, amphipod biomass increased consid-
ecably. Evidence indicates that extinction
may have been related to dieldrin
exposure. The NSS density that guppies
maintained prior to dieldrin introduction
was very low. For several months prior to
extinction there was no recruitment to
the population, even though females
carried sufficient eggs to replenish the
adult stock. Perhaps offspring survival
had been reduced as a result of dieldrin
accumulation in eggs. In the community
at LOW I, 40E into which dieldrin was not
introduced, the guppy population persisted
for 65 months until the termination of the
experiment.
The response of the laboratory communi-
ties to dieldrin was dependent upon the
level of I as well as E. At HIGH I, all
systems established new NSS's after
introduction of dieldrin. The alteration of
system structure and organization at
each exploitation rate was much less
than at LOW I. At HIGH I, during dieldrin
introduction, the guppy population at
each E maintained a somewhat lower
NSS biomass than it maintained prior to
dieldrin introduction Amphipod and snail
biomasses were only slightly altered. At
HIGH I, 40E the guppy population
persisted until the experiment was
terminated, a period of nine months
under continuous exposure to the toxicant.
This population maintained substantial
recruitment and a much higher density
than the population at LOW I, 40E and
was apparently in nodanger of extinction.
Changes in community structure and
organization after termination of dieldrin
introduction were examined in the four
systems at LOW I to determine if the
systems would recover structures they
had maintained prior to dieldrin introduc-
tion Recovery was evaluated for nearly
two years. System structures during re-
covery were different from those main-
tained during dieldrin introduction. But
the systems did not return to the struc-
tures they had maintained prior to diel-
drin introduction Inadvertent coloniza-
tion by the amphipod Hyallela azteca,
a competitor of Gammarus, and leeches,
an effective predator on snails, made it
difficult to ascertain whether exposure to
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dieldrin was responsible for the failure
of several of the systems to return to
their original structures.
Responses of the laboratory communi-
ties to exposure to dieldrin are related to
changes in the life history patterns of the
individuals composing the populations.
Individual organisms alter their life
history patterns in response to changes in
their environment. The community provides
the environmental context in which
individuals develop and populations
must be adapted to persist. Changes in
factors such as I and E bring about
changes in community structure and
associated changes in individual organism
life history patterns. For example, at each
I, increased exploitation rate (mortality
rate) reduces length of life and number of
reproductions per life time. But, due to
reduction in density of the exploited
population and an increase in the density
of its food resources, any of the following
"density-dependent" changes in life
histories of individuals in the exploited
population may also occur: faster juvenile
and adult growth, increased size at first
reproduction (or perhaps decreased age
at first reproduction), and increased
fecundity. Some of these kinds of
changes in guppy life history patterns
occurred in response to increase E. Life
history changes of this kind have been
observed in natural populations. Develop-
ment of such life history characteristics
can be understood as adaptations enabling
populations to persist in high mortality
environments.
Toxic substances may so alter life
history patterns of individual organisms
that populations are no longer able to
persist in their environments, or the
populations may persist only at reduced
densities. In the laboratory communities,
dieldrin apparently altered guppy life
history patterns by reducing growth and
fecundity and also, at LOW I, 40E, by
increasing mortality of offspring. At LOW
I, 40E, dieldrin may have contributed to
extinction of the population by effectively
preventing individuals from exhibiting
the life history patterns—more rapid
growth, higher fecundity, increased
offspring survival—that would have
adapted the population to persist at this
high exploitation rate. At HIGH I, greater
food availability brought about more rapid
growth and reproduction, and thus may
have enabled the guppy population to
persist when exposed to dieldrin and
exploited at 40E. But there surely would
have been some exploitation rate higher
than 40E at which a population even at
HIGH I would not have been able to
persist.
Not only changes in the life history
patterns of individual organisms, but also
evolutionary changes in populations—
changes in their genetic organization—
can be brought about by exploitation and
exposure to toxic substances. At LOW I,
the guppy population exploited at OE
was able to adapt developmentally and
perhaps evolutionary to the presence of
dieldrin and so recover from dieldrin
pertubation. Natural selection could have
favored those individuals that had the life
history capacity to survive, grow, and
reproduce most efficiently i n the presence
of dieldrin—the so-called "resistant"
individuals. However, in adapting to the
toxicant, the population at OE may have
lost some of its capacity to adapt to other
kinds of changes in environmental
conditions.
In the laboratory communities at LOW
I, populations exploited at 10E and 20E
did not recover from toxicant pertubation
throughout the time that dieldrin was
being introduced. The unexploited popu-
lation maintained a greater density than
the populations exploited at 10E and 20E.
Perhaps greater population density
increased the probability that "resistant"
genes or sets of genes were present in
the population and so speeded evolution-
ary adaptation and recovery. The popula-
tion exploited at 40E, which maintained a
very low density, was apparently particu-
larly sensitive to dieldrin and was driven
to extinction.
Several workers have argured that, for
genetic reasons alone, reduction in
density, as occurs with increased E, leads
to increased inbreeding and reduction in
genetic variation, especially in isolated
populations in which gene flow is limited.
Life history traits severely affected by
inbreeding are those associated with
survival and reproduction. Inbreeding
and its negative effects on life history
traits would act in opposition to any
adaptive density-dependent increases in
these performances. Toxicants that
themselves reduce growth, survival, and
reproduction would, in effect, reinforce
the negative effects of inbreeding at low
population densities. Further, loss of
genetic variation would amount to
reduction in the capacity of a population
to adapt to changes in environmental
conditions, including toxicant introduction.
Thus, populations in systems of low
productivity that are subjected to high
mortality rates and are maintained at low
densities may be especially sensitive to
toxic substances for life history reasons.
The individuals need to maintain high
growth and reproduction rates for the
population to persist but due to the effects
of both toxicants and inbreeding, the
populations have a severely reduced
adaptive capacity.
At HIGH I, 40E, guppies were able to
survive, grow, and reproduce better than
fish at LOW I, perhaps due to greater food
availability. The density of the population
at HIGH 1,40E was much greater than the
density at LOW I and, thus, perhaps
genetic diversity was also greater. These
factors may have enabled this population
to better withstand toxicant exposure.
William J. Liss, Becky L. McClurken-Lilley, and Douglas S. Lee are with Oregon
State University. Corvallis, OR 97331.
Steven F. Hedtke is the EPA Project Officer (see below).
The complete report, entitled "Structure and Organization of Persistent Aquatic
Laboratory Communities Exposed to the Insecticide Dieldrin," {Order No. PB
84-141 183; Cost: $11.50, subject to change) will be available only from:
National Technical Information Service
5285 Port Royal Road
Springfield. VA 22161
Telephone: 703-487-4650
The EPA Project Officer can be contacted at:
Environmental Research Laboratory
U.S. Environmental Protection Agency
6201 Congdon Blvd.
Duluth, MN 55804
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United States
Environmental Protection
Agency
Center for Environmental Research
Information
Cincinnati OH 45268
Official Business
Penalty for Private Use $300
ir US GOVERNMENT PRINTING OFFICE 1984-759-102/882"
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