Organiz'ution and Adaptation of Aquatic
Laboratory Ecosystems Exposed to tne
Pesticide Dieldrin
Oregon
Corvaiiis
Prepared t"-'r
Rnviromne ri! al Researcn Lab
Duiutn, M!
May
U.S.
Najional Technical information Service
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TECHNICAL REPORT DATA
(Please read Instructions on the reverse before completing
I. REPORT NO.
EPA-600/3-82-050
ORD Report
3. RECIPIENTS ACCESSION NO.
PB82- 21912 2
4. TITLE AND SUBTITLE
Organization and Adaptation of Aquatic Laboratory
Ecosystems Exposed to the Pesticide Dieldrin
5. REPORT DATE
May 1982
6. PERFORMING ORGANIZATION CODE
7, AL)THOR(S)
W. J. Liss, D. M- Woltering, S. E. Finger, M- L.
Kulbicki, and B. McClurken
8. PERFORMING ORGANIZATION REPORT NO.
9, PERFORMING ORGANIZATION NAME AND ADDRESS
Oak Creek Laboratory of Biology
Department of Fisheries and Wildlife
Oregon State University
Corvallis, Oregon 97331
10. PROGRAM ELEMENT NO.
11. CONTRACT/GRANT NO.
12. SPONSORING AGENCY NAME AND ADDRESS
U.S. Environmental Protection Agency
Environmental Research Laboratory-Duluth
6201 Congdon Boulevard
Duluth, Minnesota 55804
13. TYPE OF REPORT AND PERIOD COVERED
4. SPONSORING AGENCY CODE
15. SUPPLEMENTARY NOTES
16. ABSTRACT
A tiyalen of generalizations pertaining lo the organization, development ami
persistence, adaptation, arH productivity of ecological ayatems and their response to toxic
substances was formula tr-d - Laboratory ecosystems composed of persistent populations of
puppies, nmphlpods, snails and various mlcroluvertebrates were used In examining the systere
of generalizations for their utility and conformity with observation, (.'uppy populations In
thp ecosystems were exploited at different rates to simulate flBhlnp,, and tlit systems were
provided with illlfcrcnt levels of habitat availability and enemy Input rates.
The Inbor.itory coinmunltles developed different steady-stare structures at different
guppy exploitation rates nnrl different levels of habitat availability and energy Input.
Cupples, amphlpoHs, and anal Is were competitors for a common fooJ resource, organic natter
derived In part from tlie primary energy source, an nlfilfa ration. Amphl.->ods were also a
prey of the gupples. ChnnRns In ouplo I ta t Ion rate, and habitat availability and energy Input
brought sbout clianges In the densities of all these Interacting populal Inns.
Arguarlum experIcrents Intended to "valuate the effects of dl»ldrln on r,"Ppy 'If" history
patterns were conducted In conjunction with the laboratory ei-osystcm studies. Tills provided
the opportunity for examining some of the relationships between effects observed In
experiments more like simple toxlclty tests and effects observed In laboratory ecosystems.
In the aquarium experiments, concentrations of dleldrln similar to those us"d In the
laboratory ecosystems had effects on life history patterns similar to effectn on life
history patterns observed In the ecosysteas. It Is leett evident ho» the diversity of
effects en guppy populations observed In the ecosystems— ranging fron pertirbatlon and
recovery to extinction—could have been predicted froo the anuarlua experiments-
17.
a.
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UNCLASSIFIED
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EPA Form 2220-1 (R«v.
pstviou! eoi-riON is OBSOLETE
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EPA-600/3-82-050
May 1982
ORGANIZATION AND ADAPTATION
OF AQUATIC LABORATORY ECOSYSTEMS
EXPOSED TO THE PESTICIDE DIELDRIN
by
William J. Liss, Daniel M. Weltering, Susan E- Finger,
Michael L. Kulbicki, and Becky McClurken
Oak Creek Laboratory of Biology
Department of Fisheries and Wildlife
Oregon State University
Corvallis, Oregon 97331
Grant No. R804622
Project Officer
John G. Eaton
Environmental Research Laboratory-Duluth
U.S. Environmental Protection Agency
Duluth, Minnesota 55804
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ABSTRACT
A system of generalizations pertaining to the organization, development
and persistence, adaptation, and productivity of ecological systems and their
response to tonic substances was formulated. Laboratory ecosystems coaposed
of persistent populations of guppies amphipods, snails, and various micro-
invertebrates were used in examining the system of generalizations for their
utility and conformity with observational experience. The guppy populations
were exploited at different rates to simulate fishing and the systems were
provided with different levels of habitat availability and energy input r-a.es.
The laboratory communities developed different steady-stivee structures
at different guppy exploitation rates and different levels of .aabitat availa-
bility and energy input. Guppies, amphipods, and snails were conpetitors
for a common food resource, organic matter derived from the primary energy
energy source, an alfalfa ration. Amphipods were also a prey of the guppies.
Changes in exploitation rate and habitat availability and energy input brought
about changes in the densities of all of these interacting populations.
One part per billion of dieldrin was continuously introduced into ::our
ecosystems, one at each guppy exploitation rate, at the low level of habitat
availability and energy input. It was determined in ancillary experiments
that 1 ppb of dieldrin prob*My directly affected only the guppy populations.
The response of the systems to dieldrir was influenced by exploitation rate.
They ranged from reduction in biomass and subsequent recovery of the unex-
ploited guppy population to extinction of the most heavily exploited popu-
lations. Amphipod populations increased as a result of reduction in guppy
biomasses.
Guppies exhibited different life history patterns at different community
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structures, which were generated by different rates of exploitation and levels
of habitat availability and energy input. As exploitation rate increased,
guppies exhibited increased size-specific growth and reproduction. These
changes in life history pattern were interpreted as adaptations enabling the
populations to per ist at high exploitation (mortality) rates where length of
life and consequently, number of reproductions per lifetime was reduced.
Dieldrin altered life history pattern by reducing survival, growth, and re-
production. Thus, the toxicant may have caused extinction of the heavily
exploited population by effectively preventing it from exhibiting the life
history patterns that adapted the population to persist at high exploitation
rates.
Aquarium experiments intended to evaluate the effects of dieldrin on
guppy life history patterns were conducted in conjunction with the labora-
tory ecosystem studies. This provided the opportunity fer examining some of
the possible relationships between effects observed in experiments more liks
simple toxicity tests and effects observed in laboratory ecosystems. In the
aquarium experiments, concentrations of dieldrin similar to those used in the
laboratory ecosystems had effects on life history patterns similar to effects
on life history patterns observed in the ecosystems. It is less evident how
the diversity of effects on populations observed in the ecosystems — ranginrg
from perturbation and recovery to extinction -- could have been predicted
from these individual organism experiments.
11
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CONTENTS
Abstract - • • • - i
Figures - iv
Tables ...... v
Introduction 1
Conclusions and Recommendations . 16
Materials and Methods 20
Laboratory Ecosystem Experiments 20
. .Biological and Physical Systea ....-'. 20
Experimental Design (Phase I) 21
Experimental Design (Phase II) 21
Sampling Procedures 24
Methods Used to Determine Effects of Dieldrin on Guppy Life
History Patterns Determined in Separate Aquarium Experiments 26
Results and Interpretation 51
Trophic Organisation of the Laboratory Ecosystem 31
Organismic System 31
Environmental System 34
Dynamic and Near Steady-State Structure of
the Laboratory Ecosystem 36
Predation, Competition, and System Organisation at
Different Levels of Habitat Availability, Energy
Input Rates, and Exploitation Rates , 41
System Response to Toxicant Introduction 48
Guppy Population Structure and Organizstion
Near Steady-State 36
Guppy Population Biomass, Production, and Yield
Near Steady-State ...... 56
Guppy Size-Specific Growth and Fecundity Near
Steady-State. . ;. 59
Cohort Size-Specific Biomass, Production, and Yield
Near Steady State 68
Effects of Dieldrin OR Guppy Life History Patterns
Determined in Aquarium Experiments 74
Discussion 86
References . . . 108
iii
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FIGURES
Number
1 Phase planes and isoclina systems representing the
interrelationships between populations in_a system
represented as E*-*C^*H-^^P^^R*-*-*-I,
where C,H,P, and R comprise the system and E,
exploitation rate, and I, rate of energy or plant
resource input, are factors in the environment
of the system. . .
Phase planes and isocline systems illustrating a
possible effect of different concentrations of a
toxicant (7) on the structure of a simple community. . 8
Impact of a toxicant T on the magnitude of carnivore
steady-state production and yield curves at high and
low energy input rates 13
Kinetic diagram representing inferred trophic
interrelations in the laboratory ecosystems 32
Guppy-amphipod phase planes showing near steady-
state and ncnsteady-state behavior at four guppy
exploitation rates at high and low levels of
habitat availability and energy input rate 37
Histograms showing steady-state biomasses of
guppies, snails, amphipods, and organic
sediment at the low level of habitat availability
and energy input rate prior to and after intro-
duction of dieldrin and at the high level of
habitat availability 39
Phase plane representation of near steady-state
guppy and amphipod population biomasses at low
habitat availability and energy input rate 43
.Phase plane representation of near steady-state
guppy and snail population biomasses at low
habitat availability and energy input (solid
symbols), and at low energy input after intro-
duction of deildrin (open symbols). 44
Phase plane representation of near steady-state
guppy and amphipod population biomasses at high
habitat availability and energy input rate 45
IV
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Phase plane representation of near steady-state
guppy and snail population biomasses ax high
habitat availability and energy input. 46
11 Phase plane representation of near steady state
guppy and organic sediment biomasses and low (open
* symbols) and high (solid symbols) level of habitat
availability and energy input rate . 49
12 Phase plane representation of dynamic and near
steady-state guppy and amphipod population biomasses
at low habitat availability and energy input prior
to (open symbols) and after (solid symbols) con-
tinuous exposure to 1.0 ppb dieldrin. . 51
13 Mean guppy population biomasses near steady-state
as a function of the mean exploitation rate 58
14 Mean near steady-state guppy population production
(upper axis) and yield (lower axis) as a function
of mean near steady-st?.te population biomass . 60
IS Guppy mean relative growth rate near steady-state
for the systems at the low level of habitat availa-
bility and energy input before (open symbols) and.
after (solid symbols) introduction of dieldrin. .62
16 Guppy mean relative growth rats near steady-state as
a function of near steady-scate population biomass at
the low level of habitat availability and energy input 63
*
17 Guppy fecundity (mean number of eggs and i-abryos carried
by an exploited female of given sire) near steady-state
for laboratory ecosystems at the low level of habitat
availability energy input 64
18. Guppy fecundity (mean number of eggs and embryos carried
by an exploited female of a given size) near stsady-state
at low (open symbols and high (solid symbols) levels of
habitat availability and energy input 66
19 Guppy fecundity (mern number of eggs and embryos carried
by an exploited female of given size) in ecosystems at
the low level of habitat availability and energy input
before (open symbols) and after (solid symbols) dieldrin
introduction at 10,20, ana 40 percent exploitation
rates (system 2-40E, system 4-20E, system 14-10E) 67
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Number v
2C Guppy size class mean bionasses near steady-state
.for the four low habitat availability and energy
. '.• input, systems ( -0, -10, 20, and -40 percent
guppy exploitation) before (open symbols) and after
. ' (solid symbols) dieldrin introduction. •. ............. 69
21 Guppy size class mean production r.ear steady-state
as a function of near steady-state population bio-
mass for four low habitat availability and energy
input systems (O-O,
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TABLES
Number Page
1 Experimental design and chronological order
of experimental manipulacions. 22
2 Experimental design showing the number of
juvenile, adult female, and F-l generation
juveniles at each treatment 23
3 Summary of the reproductive performances of
feaaJe parental fish 79-80
4 Some possible predator life history patterns
at low and high exploitation rates 101
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INTRODUCTION
The introduction to this report is an attempt to formulate a system
of generalizations pertaining to the organization, development and per-
sistence, adaptation, and productivity of ecological systems and their
response to toxic substances. We believe it is the development and ulti-
mately use of systems of generalizations like these, and not any particular
empirical results or methodologies, that will be of most importance in
understanding and managing toxic substances. These generalizations are
derived from a conceptual framework (Warren et al., 1979) pertaining to
the nature of biological systems and frcm ecological theory. .Mssy, if
not most, of the statements are implicit in extant ecological theory
although perhaps they have not been stated and organized in just this way.
Th.a generalizations certainly do not encompass all of ecological knowledge.
We view them as an attempt at achieving some sort of synthesis and thus,
at this point, as a dynamic structure subject to extension, revision, and
clarification.
Much of this report deals with long-term research conducted on the
effect: of a toxicant on the organization and adaptation of laboratory
ecosystems. The laboratory ecosystems are composed of persistent popu-
lations of guppies, snails, amphipods, and various microinvertebrates.
The guppy populations ars exploited at different rates to simulate fish-
ing and the systems are provided with different levels of habitat availa-
bility and energy input rates. The laboratory ecosystem research is
useful for examining the system of generalizations as to their utility
and conformity v/ith observational experience.
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Our conceptual and theoretical views of the nature of biological
systems determines the approaches we take in understanding the effects of
toxic'substances on then. The performances of individual organisms, popu-
lations, and-communities are in continuous chsnge. Any performance of
these organismic systems, such as structure, development, replication,
and persistence, can be understood as being determined by the system's
capacity and its environment at a particular time (Warren et al., 1979).
The capacities of organisnie systems depend on their organization, which
entails incorporation of organismic subsystems whose capacities and per-
formances are concordant with the capacities and performances of their
level specific environments. Systems with a given capacity will exhibit
different performances under different sets of environmental conditions.
Development and evolution alter the capacities of organismic systems and
thus also lead to different performances. Any organismic system can be
understood to have a unique realised capacity at each developmental -
evolutionary state, this realized capacity being a partial expression of
the potential capacity of the system in interaction with its coextensive
environmental system.
Adaptation entails the maintenance of present and probable future
concordance of the capacities and psrforaances of an organismic system
with the capacities and performances of its environmental system CWarren
and Liss, in press). The word concordance implies the existence of
harmonious and apparently rule-governed relations between the organlrmic
system and its environmental system. The adaptive capacities and per-
formances of organismic systems depend upon their organization. Competition,
predation, human exploitation, and toxic substances alter the organization
and thus the adaptive capacities of populations and communities.
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A population adapts to changes in its environment through life history
adaptation and through evolutionary adaptation (Warren and Liss, in press).
Individual organisms have life history capacities that enable them to de-
velopmentally alter their life history patterns in accordance with changes
in their environmental systems. This is life history adaptation. But, as
environmental conditions fluctuate from generation to generation, natural
selection brings about a change in the kinds of individual organism life
history capacities composing the population. The population thus becomes
made up of life history capacities that are best adapted — most concor-
dant -- with the environmental system. This is evolutionary adaptation.
Human exploitation and management of an ecological resource entails
the exploitation of life history and evolutionary adaptive capacity of a
particular population, whereby developmental adaptation and evolutionary
adaptation tend to favor its persistence in the face of exploitation and
increased mortality. Not only changes in exploitation but the presence
of toxic substances can alter life history patterns, bring about evolu-
tionary changes, and so alter the adaptive capacities of populations and
communities. And often now, populations must adapt to both exploitation
and toxic substances as well as to other factors in their environments.
Thus explanation and understanding of the adaptive capacities of indivi-
dual organisms, populations, and communities becomes not only of such
ecological interest but of much practical importance as well.
The levels and kinds of energy and materials available to an eco-
logical system, patterns of climatic conditions, colonisation opportunities,
species interactions including predation, competition, mutualism, and the
spaciotemporal distribution of primary physical habitat types are joint
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determinants of the brganizaton of systems of populations or communities.
Thus these determine whatever performances including structure and per-
sistence, populations and communities may exhibit. Too often in ecological
theory, and observation, these determinants have been treated separately
in hypotheses intended to account for differences in the diversity or
communities, as may be observed along latitudinal gradients (Pianka, 1966).
In recent years, some ecologists have attempted to use two or more of these
hypotheses together to account for observations onn community structure
and diversity (Coimell, 197S; Menge and Sutherland, 1976), For clarity,
these hypotheses may be stated separately, but it is as a system of general-
izations that they should be employed in explanation and understanding of
community organization and any of its manifestations.
The productivity hypothesis states that total energy available to a
community is the primary determinant of the diversity and abundance of
organisms (Connell and Orias, 1964). The tita-stability hypothesis asserts
that climatic constancy and length of time for species colonisation are the
primary determinants of community diversity (Sanders 1969). The spacial
heterogeneity hypothesis states that the structural complexity of habitat
is the primary determinant of species diversity (Menge and Sutherland 1976).
The competition hypothesis maintains that competition among species popu-
lations for trophic and habitat resources arrayed in space and time primarily
determines community composition (MacArthur 1972, and Diamond 1975). And
the predation hypothesis asserts that "key" predators allow for coexistence
of some competitors and thus maintain community diversity (Paine 1966, and
Connell 1975).
Booty (1976) developed a model that explicitly couples the dynamics of -
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interactions populations with one another and with prevailing rystem en-
vironmental conditions. The interactions are represented with systems of
isoclines on phase planes. As will become .apparent throughout this report,
such a graphical representation allows us to bring together li::e history
patterns, system productivity, and population system outcomes of predation,
competition, resource utilisation, and the presence of toxic substances,
together with the production and yield of exploited populations, aspects
that have not generally been unified in ecological or toxicological theory.
In a system of populations, or in a community, abundances, and distri-
butions of the interacting populations — the structure cf the system of
populations — is in continuous developmental and evolutionary change.
Even so, systems of populations can be ideally understood as beiag oilti-
steady-state systems. The way that a system is organized deteraunec its
capacity to exhibit different steady-state structures.
For each set of environmental conditions, there exists a single
steady-state point on each phase plane, each of these points being a two-
dimensional projection of a single, multidimensional system, steady-state
point in phase space (Figure 1). The set of these points defines the
steady-state structure of the system for a given set of environmental
conditions. Changing conditions in the system's environment, such as
exploitation rate or rate of input of energy, brings about a change in
the steady-state structure of the system.
On each phase plane, trajectories represent the changes through
tiae in biomasses of the populations composing the system. If environ-
mental conditions are fixed, trajectories on each phase plane will
converge upon the steady-state points locating the steady-state structure
of the system under those conditions (Figure 2). In natural systems,
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Figure 1. Phase planes and isocline systems representing the inter-
relationshics between populations in a system represented
as E^tC^tH'tP^tR^t*!, where C,H,P, and R
comprise the system and E, exploitation rate, and I, rate
of energy or plant resource input, are factors in the
environment of the system. Predator biomass is plotted on
the y-axis of each phase plane and prey biomass is plotted
on the x-axis. On each phase plane, 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 bioraass with time is zero. _/The positions
and forms of the isoclines can be deduced from response
functions representing the rates of gain and loss of each
of the populations (Booty, 1976; Liss, 1977)'. At a particular
level of I and E, a single ateady-scaCc point exists on
each phiise plane, the set of these points defining-the steady-
state biomasses of C,H,P, and R. The points that define the
steady-state biomasses of C,H,P,R at Med I and OE (circles),
30E (squares), 90E (triangles) and 1SOE (hexagons) are shown-
In this sinple system, at each energy input rate, increased
E brings about reduction in steady-state biomass of C,
increases in H, reductions in P, and increases in R. Increases
in I shift the steady-state relationships between predator
and prey to the right on each phase plane, essentially in-
creasing the biomasses of C,H,P, and R. After Liss and Warren
(1980).
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Figure 1.
CARNIVORE BIOUASS (C)
<• O
5 m
HERBIVORE BIOMASS (H)
88
O
f
PLANT 8JOMASS (P)
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Figure 2. Phase planes and isocline systems illustrating a possible
effect of different concentrations of a toxicant (7") on
the structure of a simple community. In this example the
toxicant directly affects only the carnivore population.
Steady-state structure at OE, OT (circles); OE, 2T (squares);
90E, 2T (triangles) is shown. Trajectories of bi.omasses of
carnivore (C), herbivore (H), plant (P), and plant resource
(R) converging on each of these steady-states are shown.
Introduction of toxicant at a concentration .of 2T reduced
carnivore biomass, increased herbivore biomass, reduced
plant biomass and increased plant resource at high I, OE
(compare circles and squares on all phase planes). At
low I, in the absence of toxicant (OT), the carnivore is
able to persist at S0£ (prey isocline identified by low I
intersects predator isocline identified by 90E, OT). But,
at a concentration of 2T, the carnivore population is
driven to extinction at 90E (prey isocline identified by
low I does not intersect predator isocline identified by
90E, 2T) At higher I, the carnivore is able to peisist at
90E, 2T. Response of systems to toxicants may be affected
by conditions in their environments such as rate 01" exploi-
tation (mortality) of their populations or rate of mergy
and plant resource input. After Warren and Liss (1977).
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Figure 2.
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environmental conditions are rarely constant for long enough periods of
tine to permit systems to reach steady-states. Thus, under changing
environmental conditions, systems are in continuous pursuit of an ever-
shifting steady-state point. .
Individual species populations form the subsystems that are incorpo-
rated into a system of populations. The position and form of isoclines
on phase planes and thus the location of steady-state points in phase
space is determined by the characteristics of the interacting popu-
lations. A complete set of isoclines on all phase planes provides at
least a partial view of the organization of a system of populations in-
sofar as it represents harmonious relations between the steady-state
performances of interacting popv-lations under different environmental
conditions and thus at least partially represents concordance of the
capacities of interacting populations. Predation, competition, mutualism,
and omnivory are classes of kinds of concordant relations between the
capacities of interacting populations and are determinants of the organi-
sation of systems of populations. Systems widi somewhat core complex
organization than that shown in Figure 1 can also be represented with
systems of isoclines on phase planes.
Introduction of toxic substances car, alter the structure and organi-
zation of systems of populations (Figure 2). The response of systems to
toxic substances is affected by conditions in their environments such as
rate of energy input a&d level of exploitation of their populations
(Warren and Liss, 1977). In Figure 2, the carnivore population is able
to persist at a low rate of energy input (low I) when it is heavily
exploited (90E) if a toxic substance (T) is not present (the predator
isocline identified by 90E, 07 intersects the prey isocline identified by
10
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lew I). But, under these same environmental conditions at a toxicant
concentration of 2T, the carnivore population is driven to extinction
(C trajectory). The carnivore is able to persist, although at reduced
biomass, at a toxicant concentration of 2T at low I when the carnivore
is unexploited (OE), or at medium and high I when C is heavily exploited
(90E). But toxicant at a concentration of 2T so altered carnivore
adaptive capacity that it was no longer adapted to persist whi;n heavily
exploited at low I.
If a toxicant brings about a reduction in population density and
change in system structure, the effect may be corrected by banning the
toxicant and allowing the system to return to its original structure. Cut
it is just as probable that changes in the capacity of the population or
its community induced by the toxicant will make return to its a iginal
structure impossible (cf. Rolling, 1973, 1978),
Individual organisms have life history capacities to exhibit different
life history patterns under different sets of environmental corditions.
Through such developmental alteration in the life history patterns of these
individuals and through coevolutionary changes, populations and systems of
populations maintain concordance with their environments. Each steady-state
structure of a system cf populations achieved under a given set of system
environmental conditions (Figure 1) represents a particular developmental
environment for individual organisms. Individuals maintain concordance with
systems of populations by developing different life history patterns at
different steady-state system structures (Kulbicki, 1979; Weltering, 1980).
This generalization allows us to aore closely couple life history patterns,
populations, and systems of populations and to better understand system
organization. Furthermore, through relationships of life history patterns
11
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to population density and community structure, the relevance of toxicant
effects on life histories observed in simple toxicity tests to possible
effects on populations and systems of populations say be better understood
and their interpretation facilitated.
In a community, a single or a few populations, because of their
economic or aesthetic importance, may be of special interest to society.
Understanding the productivity of systems for particular populations of
interest is an important practical as well as scientific goal.
The organizaton of a system of populations and levels and kinds of
energy and materials available to the system determine the productivity
of the system for each of its populations. Productivity- was distinguished
by Ivlev (1945) from production or the particular density-dependent rate
of tissue elaboration ior a population (Warren, 1971). Production can
be calculated as the product of relative growth rate and bioaass. So
long as food is limiting, relative growth rate of individuals declines
with increasing population bicmass. A curve of production plotted against
biomass is dome-shaped. Such a curve defines a level of productivity.
Steady-state carnivore production and yield curves can be derived
from the relationship between steady-state carnivore and herbivore bio-
masses defined by the prey isoclines on the C-H phase plane, together
with a relationship between carnivore relative growth rate and herbivore
biomass (Booty, 1975; LLss, 1977). Changes in rate of energy input I
change the productivity of the system for the carnivore population and
thus alter the magnitudes of the production and yield curves (Figure 3).
Furthermore, diversion of energy and material anywhere along the trophic
pathways leading to a population can alter the productivity of a system
12
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i
o
o
a
cc
o.
HIGH I. NO TOX
*- - -
" "~ ~~ HIGH I.
LOW I, TOX
LOW I, No TOX
TOX
HIGH I, NO TOX
2 3
C
Figure 3. Impact of a toxicant T on the magnitude of carnivore steady-state
production and yield curves at high and low energy input rates.
Symbols indicate steady-state carnivore biomass, production, and
yield at different exploitation rates ( 0-OE, 3-30E, A-90E, «>150E),
13
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for that product. This includes competition with the carnivore or
competition on lower trophic levels. Production and yield, a fate.of
prodtiction of much importance to man, is determined not only by the life
history capacities of the individuals coaposihg the population, but also
by the organization of the system. As such, production and yield are as
much performances of the system as they are of the population of interest.
Toxic substances can alter productivity for a population of interest
by affecting system organization or by altering the life history patterns
of individuals composing the population, these kinds of alterations in
productivity reduce the magnitudes of production and yield curves (Figure 3).
The goal of this research is to advance understanding of the adaptive
and other capacities and performances of individual organisms, populations,
and systems of populations exposed to the insecticide dieldrin. The
objectives of the research include:
1. Determine and explain, under different sets of environmental
conditions, the impact of dieldrin on the persistence, structure,
arid organization of laboratory ecosystems in terms of concordance
of the capacities and performances of the incorporated populations.
Environmental conditions include different levels of habitat
availability and rates of input of an energy resource and differ-
ent rates of exploitation of one of the populations.
2. Determine and explain the impact cc dieldrin on the adaptive capacity,
life history patterns, production, and yield, as well as density of
the exploited population and relate these to community structure
and organization and environmental conditions.
3. In ?2parate aquariuaexperiment somewhat like toxicity tests,
determine and explain the impact of dieldrin on maturation and age-
and size specific growth and reproduction of individuals of the
14
-------
exploited population and relats these results to effects on life history
patterns and population density of_the exploited population and on system
structure and organization observed in the laboratory communities.
IS
-------
CONCLUSIONS'AND RECOMMENDATIONS
1. The systems of generalisations presented in the Introduction at least
•. broadly .conforas with observational experience derived from laboratory
ecosystems. Ecological systems can be thought of as multisteady-sta^e
systems with steady-state structure being determined by the system1s
potential capacity and conditions in the system's developmental
environment. Laboratory communities composed of persistent populations
of guppies, snails, amphipods, and various kinds of microinvertebrates
established near steady- states. Conditions in the environments of the
communities such as rate of axploitation of their populations, level of
habitat availability and energy input, and exposure to the insecticide
dieldrin in part determined the steady-state structure that the systems
developed.
2. The capacities of ecological systems dspend upon the way they are organ-
ized. Trophic organization of communities entails intaractions between
populations such as competition, predaticn, mutualism, and commensalism.
Population interactions can be represented on phase planes. In the labora-
tory ecosystems, populations of guppies, snails, and amphipods competed
for a common food resource, the organic sediment. Amphipods were also
prey o* guppies, As a consequence of this organisation, increases in
exploitation rate resulted in reductions in near steady-state guppy
biomass and increases in the near steady-state biomasses of their snuil
competitor and amphipod competitor/prtiy.. Increases in habitat availa-
bility and energy input increased the biomasses of guppies, amphipods,
and snails at each exploitation rate.
16
-------
3. One ppb of dieldrin continuously introduced into the laboratory eco-
systems at the low level of habitat availability and energy input
directly affected only the exploited guppy populations. Other popu-
lations in the systems were affected only indirectly as a result of
changes in guppy biomass. The response of the systems to dieldrin
was affected by environmental conditions including rate of exploi-
tation of the guppy population and level of habitat availability and
energy input. Response to dieldrin ranged from reduction of biomass
and subsequent recovery of the unexploited guppy population to ex-
tinction of the heavily exploited guppy population. It was suggested
that the heavily exploited population driven to »xtinction at the !ov
level of habitat availability and energy input would have been able to
persist at a higher level of habitat and energy input. This is
currently being evaluated experinentally. Aaphipcis, a competitor and
prey of guppies, increased in biomass as a result of toxicant induced
reduction of guppy biomass. Indirect effects on snails were unable to
be determined since monitoring of snail density began after introduction
of dieldrin.
4. Different near steady-state community structures vere generated by
different rates of exploitation and levels of habitat availability and
energy input. Guppies developed different near steady-state life '.
history patterns at different exploitation rates and levels of habitat
and energy- input. Thus, there was a correspondence between guppy life
history pattern and community structure. At each level of habitat
availability and energy input rate, increased exploitation rate reduced
guppy population density and induced the following changes in life
history pattern: reduced lifespan, reduced number of clutches per
17
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life-tine, increased size-specific growth, increased size at first
reproduction, increased fecundity. Increases in size-specific growth
and reproduction of individuals can be interpreted as life history
adaptations enabling the population to persist at high levels of
exploitation (or mortality), where longevity and clutch number are
reduced. Guppy production and yield bear dona-shaped relationships
to population biomass. Increases in habitat - availability increase the
i
magnitude of these curves.
5. ' • bieldria altereu guppy life history pattarnS by reducing survival and
size-specific growth and fecundity. These alterations in guppy life
history patterns resulted in reductions in the magnitude of guppy pro-
duction and yield curves. At the 40 percent exploitation rate, dieldrin
may have caused population extinction by effectively preventing the indi-
viduals from exhibiting life history patterns — more rapid growth, higher
fecundity, increased offspring survival -- that adapt the population to
persist at high exploitation rates. Such heavily exploited populations,
where rapid growth, high fecundity, and good juvenile survival are essen-
tial for persistence, may be more "sensitive" to reductions in growth,
fecundity, and survival caused by toxicants than populations exploited at
lower rates. The density of the unexploited guppy population was reduced
by exposure to dieldrin but recovered to pre-dieldrin levels while toxi-
cant was still being introduced. This population was apparently able to
adapt evolutionarily to the pesticide, with natural selection favoring
individuals with more "resistant" life histories. The "recovered" popu-
lation may have been composed of individuals with quite different life
history capacities than the population prior to dieldrin introduction.
6. Separate aquarium experiments more like simple toxicity tests were con-
ducted to evaluate the effects of dieldrin on guppy life history patterns
18
-------
1
at different food rations. Dieldrin concentrations in thess experiments
were similar to the concentration to which the laboratory ecosystems
were exposed. Guppy life history patterns observed at differenr 'cod
rations were broadly similar to near steady-state life history patterns
observed at different exploitation rates and community strictures in the
laboratory ecosystems. Thus, different food rations in aquarium experi-
ments generated life history patterns similar to those occurring at
different exploitation rates. Perhaps life history patterns observed in
these simple experiments can be thought of, in the broadest sense, as
steady-state life history patterns that would exist at some steady-state
community structure generated by some fixed set of environmental con-
ditions. Thus, using ecological theory, perhaps meaning can be "written
onto" the results of such simple experiments. Effects of die:drin on
life history patterns observed in aquarium experiments resembled effects
observed in the laboratory ecosystesm -- reduced juvenile survival and
decreased size-specific growth and reproduction. However, it is not as
evidant how the diversity of effects on population abundance, ranging
from perturbation and recovery at zero percent exploitation to ex-
tinction at 40 percent exploitation, could have been predicted from
these simple aquarium experiments. Perhaps, with appropriate theory,
such effects would have become apparent. Interpretation of simple
aquarium experiments is not a matter of direct extrapolation to complex
systems. Ecological theory should be used as a "vehicle" of extrapola-
tion, and it is in the context of such theory that results of simple
aquarium experiments can be given meaning.
19
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MATERIALS AND METHODS
Laboratory Ecosystem Experinents
Biological and Physical System
Sixteen aquatic ecosystems were established at the Oak Creek
Laboratory of Biology. Each was a nsiltispecies system composed of per-
sistent populations of guppies (Poecilia reticulata), amphipods (Ganicarus_
fasciatus), snails (fanily Planorbidae), planaria (Dugesia sp.), and
benthic sicroinvertebrates including flagellates, rotifers, nenatodes,
gastrotrichs, and protozoans. Green and blue-green algae and diatoms were
present. In addition, each laboratory system had fifty grams of the aquatic
plant Ceratonhyllun deaersum maintained as cover for the newborns of the
cannibalistic adult guppies. Habitat and escape cover for invertebrates were
provided by a substrate of 1.5 cm quartsite gravei four centimeters deep. A
gelatinous mixture of 60 percent alfalfa and 40 percent Oregon Test Diet
(Sinnhuber et al. 1977) served as the primary energy input in the laboratory
ecosystem.
Each laboratory system was maintained in a fiberglass tank measuring
1.2m x l.lm x 0.4m and holding 360 liters of water. This was continuously
exchanged by a. 600 nLlliliter per minute flow of heated well water. Water
temperature (21 ±1'C), dissolved oxygen (8.2 t 0.5 ppm), and pH (7.8 - 0.1)
were maintained at nearly constant levels. Fluorescent lights above each
tank provided an average intensity of about 20 footcandles at the water
surface. Photoperiod was controlled by a timer set for 14 hours light and
10 hours darkness.
20
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Experimental Design (Phase I)
Initially all 16 laboratory ecosystems had a similar experimental
design (identified as low energy input and low habitat availability) in
which there were three circular nests of gravel covering 20 percent of the
bottom area of each tank, and a 0.6 gram per tank daily alfalfa ration was
provided. In April 1975, 200 amphipods were stocked in each system.
Sediment accumulation and development of a benthic microflora and microfauna
ensued. Sn?.ils were introduced with the aquatic plants and persisted at low
densities.
By November 1976, guppies were stocked into all systems and a monthly
sampling program was initiated. Monthly exploitation rates for the guppies
were set at 0, 10, 20, or 40 percent of the poulation biomass, four systems
being exploited at each level (Table 1).
Experimental Design (Phase II)
In March 1978, eight of the laboratory ecosystems (two at each guppy ex-
ploitation level) were modified to establish a higher level of energy input
and habitat availability. The gravel habitat and escape cover was increased
to cover 95 percent of each tank bottom. Energy input was increased to 4-0
grams of alfalfa ration daily. The monthly sampling procedure was continued
unchanged.
In April 1978, the organochlorina insecticide dieldrin was introduced so
as to maintain a concentration of 1 part per billion (ppb) in four of the low
energy and habitat systems (one at each guppy exploitation level).
21
-------
Table 1. Experimental design and chronological order of experimental
manipulations. Sixteen laboratory ecosystems were established
in April 1975 at the low level of habitat availability and
energy input rate. Guppies were introduced and a 28-day
sampling-exploitation schedule was begun in November 1976.
Four systems were continuously exposed to 1 ppb dieldrin in
April 1978, At the sane time, eight systems were shifted
to the high level of habitat availability and energy input.
Dieldrin introduction into the four .systems at low habitat
and energy input was terminated in September 1979.
-------
t-t
(/I
Guppy Eaplollollon Roles
(percent per monlhl
Loborolory System No.
Low Energy Input and llobllal
Avallabllily Level
(0.6 g olfalia/day. 2O% gravel
cover)
Toxicant Perturbation (Tl
High Energy Input and llobilat
Avallabllily Level
(4Og allalfa/day, 95% grovel
cover)
Planar la Removal ( ^)
Toxicant Oemovol (0)
16 Laboratory Ecosysli
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/
3 1
r c
0
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%
\
5 1
j •
: <
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1 l<
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i ;
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1 1
' £
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20
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sms
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11/76
4/78
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10/75
l
10/79
7/eo
-------
Sampling Procedures
Organisms in each laboratory ecosystem were censused and its guppy
population exploited every 28 days. Extreme care was taken to perturb the
systems as little as possible during sample. Guppies were netted from the
tanks -. Individual length and weight measurements were taken for immature
guppies (standard length of 10 to 14 millimeters) and for mature females
(standard length greater than 14 millimeters). Total number and weight
were recorded for nature aales and for newboms (standard length less
than 10 millimeters).
The method of exploitation was similar to that employed by Liss (1974).
A systesatic exploitation schedule was developed for each exploitation rate.
The schedule provided for the removal of a proportion of the population
corresponding to the exploitation rate. At each exploitation rate, all
sizes of fish were exploited with the same intensity.
Total population and size-class biomssses (i.e. the combined weight
of individuals) and yields (i.e., the weight of the catch at a given
sampling date) were calculated for each guppy population. Total population
and size-class production (i.e., the amount of tissue elaborated by the
population or size-class between sampling dates) were estimated using che
difference between the initial and final biomasses of the population and
size-class over the 28-day intervals (Chspman 1968). Final biomasses were
adjusted for any known mortalities and for fish changing size classes over
the interval. Production includes somatic and reproductive (eggs and embryos)
tissue elaboration. Density and size composition of the population, growth
and survival of individuals, and fecundity of exploited females were also
determined and related to environmental factors and to exoloitation.
24
-------
The gravel substrate, contained by wire screen, and the C.eratophyllum
were removed from the tanks and rinsed to dislodge invertebrates. Anphipods,
snails, planaria, and sediments plus associated micororganism^ were then
removed by a siphon and a net. Individuals in each macroinvej-tebrate popu-
lation were sized, counted, and then weighed as a group. The Ceratophyllum
was weighed and restocked as necessary to maintain 50 grams iit each system.
Three one-percent subsamples of the sediment from each system were obtained
with a sample splitting device. Dry weight and organic matter content were
determined. The samples were dried at 70 *C for 72 hours and then ashed for
three hours at SOO'C- Organic nitrogen conte.it.was determined by standard
microkjeldahl technique (Berg and Gardner, 1978). Microorganisms were identi-
fied and their densities estimated with the aid of a Sedgwich Rafter Cell
(APHA 1971). All amphipods, snails, remaining sediments with microorganisms,
and unexploited fish were returned to the tanks.
The insecticide dilution and delivery system was similar to the
continuous flow dilution apparatus described by Chadwick et al. (1972). A
solution raving a constant toxicant concentration was produced by passing
water through a column of 1.5 cm quartzite gravel coated with technical grade
dieldxin. Concentrations of dieldrin were determined weekly in laboratory
ecosystem water samples and periodically in tissue samples of guppies, snails,
plants, and sediments. Following standard extraction procedures, analysis
was dona using a Varian-areograph 2000 gas chromatograph equipped with an
electron capture detector.
-------
Methods Used to Determine Effects of Dieldrin on Giropy Life History
Patterns Determined in Separate Aquariun Experiments
Aquarium experiments were conducted to evaluate the effects of
dieldrin on guppy life history patterns. These experiments were similar
to many kinds of toxicity tests on individual organisms. The purpose of
these experiments was to gain some understanding of the relationship of
effects observed on life history patterns in relatively simple tests to
effects on life history patterns, populations, and communities in the more
complex laboratory ecosystems. Soma insight into the relevance of such
simple tests in understanding and predicting effects in more complex
systems may thus be obtained.
Seven hundred newborn guppies (approximately 5 mm in length) were
collected over a period of one week and divided into two groups of 350
fish each. Fish were fed live tubificid woras (Tubifex SB.). Each group
received a different food ration. Food ration levels for individuals in
each group represent a fixed proportion of the mn^trnm daily food con-
sumption rate per individual. The high ration (HR) represents 0.66 of
the riff-""*™™ daily food consumption rate and the low food ration (L?.) re-
presents 0.53 of the Bp-Hmmg daily food consumption rate. Since mariircim
daily food consumption rite is dependent upon body weight, all food rations
are expressed as a decimal fraction of body weight:
1) fj • 0.33 M for the low ration and
2} fj • 0.66 M for the high ration
fi • daily food ration per individual as a
proportion of body weight
M » iprEffl"" daily food consumption rate per
individual as a proportion of body weight
26
-------
In fish, maximum daily food consumption rate, as a fraction of body
weight, declines as body weight increases. Preliminary experiments were
conducted to determine the maximum daily consumption rate per individual
for different size classes of both male and female guppies (Kulhicki, 1980).
From ths results, daily food rations, as a fraction of body weight, were
determined from equations 1 and 2. Total daily food ration per individual
is given by:
3) Fi * fiw
where W is body weight. As the fish grew, their ration was adjusted in
accordance with changes in their maximum daily food consumption rate and
body weight. All fish were weighed weekly and their food rations were
adjusted accordingly. Fish were fed once a day.
Both groups of newborn guppies were held in control water and fed
control food, at the appropriate ration levels, until sexual maturity was
reached. Mature males were identified by the presence of a gonopodium.
Fish 16 mm and over without a gonopodium wer? considered to be females.
When sexual maturity was reached, 30 females from each group were selected.
Each of these females was placed in a seven liter aquarium. At each ration
level, ten females received control food and control water, ten females
were continuously exposed to 1 ppb of dieldrin in the water and 2 ppm of
dieldrin in the food (low dieldrin or LD), and ten females were exposed
to two ppb in the water and four ppm in their food Oiigh dieldrin or HD).
The experimental design is shown in Table 2. A pesticide dilution system
similar in design and principle to the continuous flow dilution apparatus
described by Chadwick et_ aJU (1973) was used to introduce the appropriate
concentrations of dieldrin into the experimental chambers. Dieldrin con-
centrations 2 and 4 ppm in the food were obtained by holding the tubificid
27
-------
Table 2. Experimental design showing tl>e number cf juvenile, aduit female, and F- I generation
juveniles at each treatment. All F-I generation Hah were from the second clutch of
parental females.
K>
CO
Parental
Fioh
Juveniles
Adult Females
F- 1 Generation
Juveniles
Control
350
10
5
Clutches
High Ration
Low
Dieldrin
0
10
5
Clutches
High
Dieldrin
0
10
5
Clutches
Control
350
10
5
Clutches
Low Ration
Low
Dieldrin
0
10
5
Clutches
High
Dieldrin
0
10
5
Clutches
-------
worms for 24 hours in flowing water containing, respectively, 5 ppb and 10
ppb of dieldrin.
One male was put with each female for a period of 24 hours each week
to ensure fertilization. Since guppies are cannibilistic on their young,
plants (Ceratoghylua deaersum) were placed in each tank to provide cover
for the newborn. Newborn fish were collected every morning (birth almost
always occurs at night), and their number and weight were recorded along
with the age and weight of the mother. Age- and size-specific growth, age
and size at first reproduction, and age- and size-specific production of
offspring of parental were determined from birth through four reproductions.
Newborn fish from the second clutch produced by each of five females
from each treatment were raised as the F-l generation= Each of these
groups of newborn fish were raised at the same food ration and dieldrin
concentration as their parents. Juvenile survival and growth, sex ratio
at maturity, and body composition were recorded.
The intrinsic rc.te of increase, r, is a convenient parameter for sum-
marizing the possible population effects of changes in individ""1 ".."-vival
and fecundity and was determined for parental fish at each treatment.
Lotka (1925) showed that if the age schedules of survival (1^) and
reproduction (n^) remain constant, a population will develop a stable
age distribution and population number, N, will change according to the
equation:
dN/dt » rN
where r is the intrinsic rate of increase. The age schedule of survival
and reproduction will remain constant only if environmental conditions
remain constant and birth and death rates are not affected by changes in
population density. Furthermore, as Birch (1948) illustrated in his
29
-------
examination of the effects of temperature and moisture on the intrinsic
rate of increase of grain beetles, a particular value of r exists fcr
each.particular set of environmental conditions. Thus, r has meaning
only in the ccntext of the environmental conditions under which it was
determined. In natural systems, environmental conditions are continuously
changing, and birth and death rates are density-dependent, making direct
applicability of laboratory determinations of r to natural systems tenuous.
The.concept of intrinsic rate of increase direcrs our attention to life
history characteristics of the individual that may be important in popu-
lation growth, and provides a means of evaluating how population growth
and persistence cculd be affected by changes in life history character-
istics of the individual induced by changes in environmental conditions
or the presence of toxic substances.
The calculation of r was based upon the arithmetic approximation
given by Birch (1948) f 01 •:
I^M
1 m e"**- i
A ^W
X*0
Given the 1 and m^ schedule, the intrinsic rate of increase r was found
by substituting trial values of r in the equation until the equation
had a value of approximately one.
50
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RESULTS AND INTERPRETATION
Trophic Organization of the Laboratory Ecosystems
Trophic organization entails that aspect of community organization
based on interactions between species populations for rood resources.
Other aspects of community organization include life history and habitat
organization. Figure 4 represents the inferred trophic interrelations
in the laboratory ecosystems. This synthesized view can be taken to be
an organismic system and environmental system which together form an
ecological system in space and time.
Organismic System
The organismic system is a system of populations that includes
predatcr, prey, and competitor populations. Organic sediments including
the alfalfa ration and microorganisms were the common prey for the three
major populations: guppies, amphipods, and snails. Copepods were
inadvertently introduced with amphipods but died out early in the study.
Alfalfa ration, feces, decomposed plants and animals, and benthic micro-
organisms made up the 60 to 80 percent of sediments that were organic.
The iiean organic nitrogen content of the sediments was 3.0± 0.5 percent
for the 16 systems over 34 months. The microorganism component included
nematodes, flagellates, rotifers, gastrotriclis, and protozoans (Finger,
1980). An apparent link between this benthic subsystem and the major
predators was a protozoan - nsmatode - g**ppy trophic chain. Alfalfa
input, 0.6 or 4.0 grass per day, was the major source of sediment
differences between tanks at low and high energy input levels.
31
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EXPLOITATION
PLANARIA
-^- DIELDRIN
T» SNAILS
ORGANIC SEDIMENTS AND
ASSOCIATED MICROORGANISMS
ALFALFA RATION
ATTACHED
ALGAE
LIGHT ENERGY
Figure 4. Kinetic diagram representing inferred trophic interrelations
in the laboratory ecosystems. Population interactions are
designated as predation (p) or conroetition (c). Exploitation,
dieldrin, alfalfa ration, and light energy are variable
environaental factors.
52
-------
Guppies are omnivorous, live-bearing, cannibalistic fish. Adult
females (up to 42 mm and 2.0 grass) and mature males (up to 20 nn and 0.1
grams) were observed consuming the alfalfa ration, sedirents, and aophi-
pods. Stomach samples showed the presence of materials and nicroorganisms
identified in the sediments, plus amphipod parts. Newborn guppies were
observed eating alfalfa and picking through the sediments.
The amphipods in these laboratory systems were herbivorous crusta-
ceans that ranged in size from 0.5 to 15.0 ixLllioeters (4 x 10" to 4
x 10" graas). They were observed feeding in the sediments and on the
alfalfa ration. Amphipods moved freely throughout the tank and were found
among the rocks, on the plants, and on the sides of the tanks vr.en guppies
were absent or at low densities. Their movement was usually limited to
among the rocks and the sediment when guppies were present. ABB/ ipods were
prey of the guppy populations as well as competitors for the alfalfa ration.
Later in the experiment, planaria ware inadvertently introduced and
were more effective predators on amphipods than were guppies, the amphi-
pods being unable to escape from planaria in the rock substrate
habitat. Planaria were observed in all systems at low densities (i.e., 1
to 30 individuals) as early as October 1977. Following the increase in
alfalfa input and substrate cover in eight systems, amphipod populations
increased up to 15 times in biomass. Planaria populations increased
following the increase in amphipods, and this led to drastic declines in
amphipod populations. Complete elimination of planaria by exploiting
them in four high productivity systems allowed the amphipods to again
increase. Planaria were not exploited in the remaining four systems at
high productivity and they eventually eliminated all the amphipods.
33
-------
Snails were introduced as eggs attached to the aquatic plant
Ceratgphyllum. Snails were observed eatirj attached algae on the sides
and bottom of the tanks as well as reeding in the sediments. They were
competitors of both guppy and snail populations for the alfalfa ration.
High alfalfa input brought about draaatic increases in snail bionasses.
Censusing of snail populations in both high and low productivity systems
was initiated about this tioe. Losses of snails to parasitism, predaticn
on eggs, and other mortality was unaccounted for in these systems.
Attached algae included a mixture of blue-green and green algae and
diatoms. These algae and associated microorganisms were a food resource
for snails and other species ia the laboratory syrtsss. Algal density
varied between tanks from essentially macroscopically non-visable levels
to a solid green-brown mac. Differences in algal density and sediaent
accumulation patterns had apparent effects on resulting structure ami
organization of the systems. More detailed evaluation of the structure
of the algal system and its role in the community is presently being
undertaken.
Environmental System
The manipulated environmental components of the laboratory ecosystems
included habitat availability, energy and material input, guppy removal by.
exploitation, and introduction of the toxicant dieldrin. Alfalfa was the
major energy source, as was made apparent by increases in population bio-
masses corresponding to the change froa 0.6 to 4.0 grams per day of alfalf?.
ration. The organic nitrogen content of the alfalfa ration was 3.0 percent.
Light levels were kept relatively low to prevent blue-green algae blooms.
i
Intensities ranged from IS 'to 23 foot-candles at the surface of the water
and were directly correlated to location of the tanks in the laboratory.
-------
Monthly exploitation of the gupp/ populations simulated the impact
of fishing. Heavy exploitation resulted in si:e distributions occasion-
ally having up to 80 percent of & population's biomass residing in one
large, female. More or less than the intended percentage of bicmass was
thus often exploited in any one month. This led to some fluctuations in
population biomass; over many months, however, mean exploitation rates
were near the intended percentages.
The environmentally stable insecticids uieidrin was introduced at a
concentration of 1 ppb to evaluate the response of the laboratory eco-
systems to toxicant at different rates of input and exploitation. Means
and standard deviations of lieldrin concentrations in weekly water samples
were: system No. 1, 0.95 _+_ 0.09 ppb; system No. 3, 0.98 +_ 0.08 ppb; and
systems No. 4 and 14, 0.96 *_ 0.08 ppb dieldrin.
Through food and water, the lipophilic dieldrin accumulated in tissues
of the organisms and in the sediments. To obtain enough tissue to perform
analysis, juvenile, male, and smaller female guppies had to be combined in-
to a single sample. The mean tissue concentration of such combined samples
was 11.2 ppm. Very large females (28 aa to 58 mm in length) provided enough
tissue to be analyzed individually. Tissue concentrations of these fish
ranged from 29.0 to 45.0 ppm. These high tissue concentrations probably
result in part from accumulation of dieldrin in eggs and developing embryos
being carried by the females. The mean concentration of dieldrin in the
tissues of snails (including shells) was 0.87 ppm and the concentration in
sedLaents was 7.5 ppa.
In nature, populations persist through interactions and adaptations
in complex and fluctuating environments. Figure 4 begins to account for
somo of the major trophic interactions including predation, competition,
35
-------
and ooaivery in the laboratory systems. These interactions along with
prevailing environmental conditions resulted in changes in connmnity
structure. The pattern of organization inferred for the laboratory systeas
will be used to explain observed dynamic and near steady-state conmmity
structure.
ic and Near Steady-State Structure of thJ Laboratory Ecosystems
Co-occurring biomasses of two interacting populations can be plotted
on coordinate axes forming a phase plane. This graphical procedure
explicitly couples the dynamics of interacting populations to one another.
Dynamic structure is represented by the trajectories connecting the points.
Under constant environmental conditions, the trajectory of coordinate bio-
masses may track toward a steady-state point on the phase plane; -.hanging
environmental conditions alter the direction of the trajectory toward
another steady state. Near steady-state structure for the laboratory
systems for each set of environmental conditions was assumed whim popu-
lations fluctuated in a very restricted area of phase space relative to
previous and succeeding fluctuations.
A phase plane representation of near steady-state relative to non-
steady-state behavior of guppy and amphipod populations for four of the
laboratory systems, one at each level of guppy exploitation, at low energy
input and at high energy input, is shown in Figure 5. Guppy and amphipod
populations achieved near steady states at low energy input, with near
steady-stats biomasses being determined by guppy exploitation rate as well
as energy input rate. Increased energy input rate resulted in establish-
ment of new near steady-states. At each exploitation rate, the near
-------
56
32
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20%
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04 08 12 16
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AMI'IIIPOO OIOMASS (giomi/lonK)
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Figure 5. Guppy-onpliipod phase planes showing near steady-state and nonstendy-stntc behavior nt four
gappy exploitation rates at high and low levels of hrbitat availability and energy input
rate. Open symbols designate behavior at low. and solid symbols behavior at high hnbitnt
anil energy input. Dashed trajectories designate nonstcndy-state bchnvior and solid
trajectories ore taken to be ncnr steady-state behavior.
-------
steady-state biomasses of both populations were .greater at the high rate
of energy input than at the low rate. These and other results sake it
apparent that the laboratory communities were nilti-steady state systems,
(See also Figure 1). We take the steady-stats system structure to be de-
termined by system capacity ar-d conditions in the system's environment.
The effect of energy input rate, exploitation rate, and dieldrin on
the near steady-state structure of the laboratory ecosystems is shown in
Figure 6. Structure is represented as the nean biomasses of the populations
when they were near steady-states. Guppies and snails were the dominant
organisms in the communities. Amphipods were also present but at such
lowar densities. Also present in the communities but not represented in
Figure 6 is the zicrocrguusm component composed of populations of
euglenoid flagellates, protozoans, ciliates, amoebas, nematodes, rotifers,
and gastrotrichs.
Changes in exploitation rate, habitat availability, and energy input
rate, and exposure to dieldrin brought about changes in community structure
4
and orgonizaton. At each level of habitat and energy input, increased
exploitation rate reduced guppy biomass and increased the biomass of
amphipods and snails. At the low level of habitat availability and
energy input, organic sediaent densities appeared to be little affected
by changes in exploitation rate.
Increased habitat availability and energy input rate brought about
increases in the biooasses of all populations and, thus, in total
coamnnity biomass. The systems shown in Figure 6 are those from which
planaria wore removed. In tho systems in which planaria were not removed,
aaphipods,•one of their principal prey, became extinct. These systems
have not yet established near steady-states.
IB
-------
Figure 6. Histogram? showing steady-state bionasses of guppies, snails,
anphipods, and organic sediment at the low level of habitat
availability and energy input rate prior to and after intro-
duction of dieldrin and at the high level of habitat availa-
bility and energy input.
39
-------
Figure 6-
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[SEDIMENT ^GUPPIES QAMPHIPODS
40
-------
: At the lov level of habitat availability and energy input, proto-
zoans, nematodes, and rotifers were :he predominant microinvertebrates.
Ciliates and euglenoid flagellates wvre present at low densities. At the
high level of habitat availability and energy input, amoebas, nematodes,
rotifers, and gastrotrichs occur infrequently in these systems.
Exposure to dieldrin altered connunity structure, but not to the
same degree as did changes in habitat and energy input. The predoninant
effect was reduction in guppy biomass, with the guppy population ex-
ploited at 40 percent being driven to extinction.
Phase planes and isocline systems will be used to explicate the
organization of these systems, including species interactions such as
predation, competition, and omnivery, to account for and so explain
changes in the structure of the laboratory ecosystems.
Predation, Competition, and System Organization at Different Levels of
Habitar Availability, Energy Input Rates, and Exploitation Rates
Near steady-state system structure was determined by the interactions
between the population composing the system and conditions in the system's
environment. At each level of habitat availability and energy input rate,
changes in rate of exploitation of the guppy populations influenced near
sready-state system strucrare by affecting not only guppy biomass but the
biomasses of the guppies' prey and competitors as well.
At the low level cf habitat availability and energy input, increased
exploitation rate brought about reductions in near steady-state guppy
biomass and increases in near steady-state .imphipod and snail biomasses.
As exploitation rate was increased from sero to forty percent, near
41
-------
steady-state guppy biomass decreased from approximately 9.0 to 1.0 grains
(Figure 7). Apparently because of reduction in intensity of predation and
competition, near steady-state biomasses' of anphipods tended to increase
as guppy biomass declined.
Prior to introduction of guppies into the laboratory ecosystems,
smphipod populations did not establish near steady-states and reached
narrmim biomasses of 1.5 grams, the range at the time of guppy intro-
duction being 0.1 to 1.0 grams. Introduction of guppies resulted in es-
tablishment o£ near steady-state amphipod biomasses that were much lower
m
than the bioaasses that existed prior to guppy introduction.
Snail populations were censused monthly beginning in October 1978.
Consequently, in the four systems at the low level of habitat availability
and energy input that were exposed to dieldrin, snail biomasses px.or to
dieldrin introduction were not determined. Represented in Figure 8 for
the low level of habitat availability and energy input, is the relation-
ship between near steady-state guppy and snail biomasses. An inverse
relationship existed between near steady-state guppy and snail biomaises.
Near steady-state snail biomass increased as a result of reduction in
biomass of their guppy competitor brought about by increased exploitation.
Habitat availability and energy input rate were increased in eight of
the laboratory ecosystems. In four of these systems planaria were system-
atically removed. In these systems, increased habitat and energy input
shifted the near steady-state relationships between populations upward and
to the right on each phase plane (Figures 9 and 10, see also Figure 1),
this resulting in increased near steady-state biomasses of organic sediments,
guppies, asphipods, and snails at each exploitation rate.
In systems where planaria were uot removed, amphipod populations were
driven to extinction by planaria prriation (Finger, 1980; Woltering, 1980).
42
-------
Figure 7- Phase plane representation of near steady-state guppy and amphipod population biotnnsses at
low habitat availability and energy input rate. Cuppy exploitation rates are indicated as
O- 0, O- 10, A- 20, and D- 40 percent. Populations were censused, and co-occurring
population hioaiassi
04
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8e
CO
O
to
Q K)
3
-------
t
0
0
6 8 10 12
SNAIL BIOMASS (grams/tank)
16
Figure 8. Phase plane representation of near steady-stcte guppy and snail population boraasses at low
habitat availability and energy input (solid symbols), and at low energy input after intro-
duction of dicldrin (open symbols). Snail populations were censused beginning in October
1978. Cuppy exploitation rate is indicated as O-0, O-1C, A-20, and O-40 percent. Time'
the phnso plnne begins lit the system-numbered point. After Weltering (1981).
on
-------
36
29
a
en 20
in
<
2
O
C3 16
I
« 12
0 a4 0.8 1.2 1,6
AMPHIPOO BIOMASS (grcms/fonK)
Figure 9. Phase plane representation of near steady-state guppy
population biomasses at high habitat availability and energy input
rate. Hatched area indicates relative position of the systess at
low energy input (see Figure 7). The trajectories between low and
high energy input (Figure 5) have been reaoved to facilitate
comparisons. Guppy exploitation rate is indicated as O* 0, O" 1
A- 20, and O - 40 percent.
45
-------
40r
so
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SNAIL BIOMASS (grams/tank)
60
70
Figure 10, Phase plane representation of near steady-state guppy and snail
population bioaasses at high habitat availability and energy
input. Hatched area indicates relative position of guppy and
snail co-occurring bioaasses at low energy input (see Figure 3).
Guppy exploitation rate is indicated as\/- 0, O- 10, A-20,
and C- 40 percent. 'After Weltering (1980).
-------
These systems have not yet established near steady-states and consequently
will not be discussed in detail in this report. Presently gappy biomasses
in these systems are not substantially different from those in systems where
planaria were removed. Snail abiomasses in the systems with j.>lanaria at
present appear to be somewhat greater than near steady-state mail biomasses
in systems where planaria removal was instituted. Snails may be able to
attain higher biomasses in systems with planaria because of the absence of
their amphipod competitors (Woltering, 1980).
At thy high level of habitat availability and energy input rate in
systems where planaria were removed, increased exploitation rate resulted
in reduction in ner steady-state guppy biomasses. Near steady-state
amphipod biomasses appeared to be unaffected by changes in guppy biomass
resulting from exploitation (Figure 9). The reasons for this aye not yet
well understood. Because of the large amount of rock substrate available
as an ssphipod refugium at the high habitat level, guppies may not have
been able co effectively prey upon aaphipcds and thus had little direct
impact cm the population bioxasses. But possible effects of competition
with guppies and snails on anphipod abundances still need to be taken in-
to account in explaining near steady-state biomasses.
As occurred at the low level of habitat availability and energy input
rate, reductions in near steady-state guppy biomass brought about increases
in the near steady-state biomass of thair snail competitor (Figure 10).
Thus, although their relative abundances varied, the dominant organisms in
the laboratory ecosysteos coexisted as competitors over a range of environ-
mental conditions. Thr relative abundances of the competing populations
were determined by rate of exploitation of the guppy population and level
of habitat availability and energy input rate. At a particular habitat
47
-------
level and energy input rate, increased mortality of the guppy as a result
of exploitation reduced its near steady-state bionass and enabled the
snail to increase in near steady-state abundance, apparently because of
reduced competition.
Organic sediment was taken to be representative of the food resource
for which guppy, snail, and amphipod populations apparently cosseted. At
the high level of habitat availability and energy input, organic sedisents
like asphipod biomass appeared to bear a slight inverse relationship to
guppy bioaass (Figure 11). At the low level of habitat availability and
energy input rate, organic sediment biomass did not vary with changes in
guppy, snail, and asphipod bionasses brought about changing exploitation
nte (Figure 11). Apparently, organic sediment loss to predation and
decomposition was approximately the sane at all exploitation rates.
Perhaps the amount of sediment consumed by a particular population varied
according to the biomass of that population, which was indirectly deter-
mined by guppy exploitation rata. Increased exploitation rate caused a
reduction in guppy bionass and probably consumption of sediments by guppies.
But increases in snail and amphipod bionasses and perhaps increases in
consumption of sediments by these populations occurred ir. accordance with
reductions in guppy biomass and consumption. Thus, the outcome of tha in-
verse relationship between guppy biomass and the biomasses of asphipods smd
snails was to maintain total consumption of organic sediments and sediment
biomass relatively constant (Weltering 1980).
System Response to Toxicant Introduction
AC the low level of habitat availability and energy input, four sys-
tems, one at each exploitation rate, with the tightest near steady-state
48
-------
,.
ORGANIC SEDIMENT (groms/fonkJ
Figure 11. Phase plane representation of nsar steady-state guppy and organic
sediment bionasses and the low (open synods) and high (solid
symbols) level of habitat availability and energy input rate.
Guppy exploitation rates are indicated asO- &- 20,
and D- 40 percent.
49
-------
patterns of guppy and amphipod biomasses (systems 1,5,4,14) were selected
for exposure to dieldrin. The four remaining systems (5,6,7, aid 12), one
at each exploitation rate, were kept unchanged at low energfy input, la the
system exposed to dieldrin, near steady-state guppy biomass wss inversely
related to near steady-state anphipod biomass prior to introduction of
dieldria (Figures 12 and 7). Near steady-state saail biomasses in these
four systems, recorded after the introduction of dieldrin, was inversely
related to near steady-state guppy biomass (Figure 8).
Experiments were conducted at our laboratory on the effects of
dieldrin on individual organisms of the species present in the laboratory
ecosystems to enable us to better explain the effects observed in the
ecosystems. The 96 hour LC50 of newborn guppies was about 5 ppb and that
of adult females about 20 ppb. Dieldrin concentrations of 1 ppb and 2 ppb
affected age-specific growth, survival, and reproduction of gupp:.es. The
experiments on the effects of dieldrin on guppy life histories will be
considered in more detail later in this report. The 96 hour LCSO for
aophipods was about 50 ppb. Sublethal effects on amphipods cou-d not be
reliably determined, because of difficulties in maintaining individuals
and populations in aquarium studies outside the laboratory ecosystems.
Benthic aicroorganism populations when exposed co ISO ppb exhibited
densities that were similar to those exhibited in the absence of dieldrin.
Thus, A dieldrin concentration of 1 ppb in the laboratory ecosystems
probably directly affected guppy survival, growth, and reproduction, as
will be shown later in this report, and only indirectly affected other
population;) through its effects on guppies.
In general, the responses of the laboratory ecosystems to continuous
exposure to dieldrin broadly conformed to the responses outlined in the
Introduction (Figure 2). Responses were characteriied by alterations in
SO
-------
Figure 12- Phase plane representation of dynamic and near steady-state
guppy and aaphipod population biomasses at low habitat
availability and energy input.prior to (open syabols) and
after (solid symbols) continuous exposure to 1.0 ppb dieldrin.
Guppy exploitation rates are indicated as <>• °t O- 10,
A- 20, and O- 40 percent guppy exploitation. At :ero
percent exploitation (system 3), guppy steady-state biomass
was reduced by exposure to dieldrin but subsequently re-
covered to pre-dieldrin levels. At 10 percent exploitation
(system 14), guppy biomass was reduced and aaphipod bioaass
increased as a result of exposure to dieldrin. The system
did not establish a near steady-state after dieldrin
introduction. At 20 percent exploitation (system 4), guppies
and aophipods established a new near steady-state after
exposure to dieldrin. Guopy biomass was reduced and anphipod
biomass was increased. At 40 percent exploitation (system 1),
the guppy population went extinct after exposure to dieldrin.
After Weltering (1981).
51
-------
0
0.56
O.I 0.2 0.3 0.4
AMPHIPOD BIOMASS (grams/lank)
E
u.
-------
systea structure and organisation and were dependent upon exploitation
rate. The effects ranged from perturbation and recovery at ze:.*o exploi-
tation to extinction of the guppy population at 440 percent exploitation
(Figure 12).
In he laboratory ecosystem at zero exploitation rate (System 3),
after introduction of dieldrin there was ait immediate and draaatic de-
crease in guppy biomass. Aaphipod populations increased slightly as a
result of the decrease in biomass of their guppy i-.-edator and competitor.
Numerous male and adult female guppies died in the first few months after
exposure. Such mortality was not apparent in the other three systems re-
ceiving dieldrin. At zero exploitation rate prior to dieldrin introduction,
the guppy population maintained a relatively high density and apparently
there was less food available per individual and slower individual growth
than at higher exploitation rates (Figure 16). Thus, th« fish vere in
relatively poorer condition and apparently were highly susceptable to
dieldrin intoxication.
After the introduction of dioldrin, the system uppeard to establish
a new steady-state at a guppy biomass of about five grams and an amphipod
biomass of about 0.4 grass (Figure 12, see also Figure 2). The system
maintained this structure for about eight months. Although dieldrin was
still being introduced, the system began to recover from toxicant pertur-
bation, with guppy biomass gradually increasing and anphipod biomass de-
creasing. The structure of the recovered systea eventually overlapped
the near steady-state structure that existed prior to dieldrin introduction.
Evidently, the guppy population at :ero exploitation was able to adapt
evolutionarily to the presence of dieldrin and so recover from dieldrin
perturbation. Natural selection could have altered the adaptive capacity
-------
• of the populations by favoring those individuals that had the life history
capacity to survive, grow, and reproduce nost efficiently in the presence
of dieldrin — the so-called "resistant" individuals. These individuals
exhibit life history patterns that are well adapted to the presence of
dieldrin, thus enabling the population to increase in biomasa while still
being exposed to dieldrin.
In the laboratory ecosystea at 10 percent exploitation rate
(system 14), exposure to Dieldrin brcught about a decrease in guppy bio-
mass and an increase in amphipod bioaass. However, the bioxasse? of both
guppies and amphipods were highly variable and, after 23 months of con-
tinuous exposure to the pesticide, the systea had failed to establish a
near steady-state.
At the 20 percent exploitation rate (systea 4), the system established
a new near steady-state structure in the presence of dieldrin with near
steady-state biomass of guppies about 46 percent lower and amphipod bioaass
about SO percent higher than their near steady-state biomass prior to
dieldrin introduction.
I* *«e laboratory ecosystea at the 40 percent exploitation rate (system
1), gup-, populations went extinct after IS months of continuous exposure to
dieldrin (see also Figure 2), For the first eight months'after introduction
of dieldrin, there were no obvious changes in the structure of the systea.
Guppy populations exploited at 40 pe-.rcent maintained relatively low densities
and often had size distributions with over 70 percent of the biosass in one
large female. This sometimes resulted in significantly sore or less than
the prescribed 40 percent of the bicaass being exploit?" in any given month.
Over many months, however, mean exploitation rate was near 40 percent.
Systea 1 had been exploited by 77 and 82 percent in two of the It
-------
months prior to dieldrin introduction. In. several months, the population
recovered owing to density dependent increases in growth and reproduction
of individual fish. After ten nonths .of continuous exposure to dieldrin.
system 1 was again "overexploited" at 75 percent (a one gran female). The
population did not recover in the following five months and went extinct
with the removal of a 0.2 and 0.5 gram female. The two fish carried a total
of 42 eggs and embryos. For seven months prior to extinction, the number
of newborn fish was at least 70 percent lower "Jian the number of newborns
present prior to dieldrin introduction. Thee had been no newborn fish
present in the tank for three months prior to extinction. This suggest? that
not only changes in age structure of adults but also reduced survival of off-
spring accounted for reduction in offspring number. Offspring survival may
have been reduced due to accumulation of dieldrin in eggs.
Over a one month period prior to extinction of the guppy population,
aaphipod biomass in system 1 was recuced from 0.33 to 0.12 grams as a result
of planaria predation. Flanaria were then removed from the system. Zt is
unlikely that this lower anphipod biomass was influential in the decline of
guppy biomass since, because of their low densities, asphipods are probably
not a major prey of guppies.
In the laboratory ecosystem at the 40 percent exploitation rate into
which disldrin was not introduced (system 6), the guppy population has
persisted for 47 months, up to the present time. Guppies in 'his system
are also subjected to occasional "overh&svest," this further supporting
the conclusion that guppy population extinction in system 1 resulted from
exposure to dieldrin.
After extinction of guppies, asphipod bLomass increased, reaching
levels that the populations had not attained since guppies were introduced.
In addition, behavioral changes occurred, the asphipods moving more freely
55
-------
throughout the tank rather than restricting their movement primarily to the
rock nests. Since snail populations were not censuscd prior tr dieldrin
introduction, effects on snail biooass could not be determined,,
Guppy Population Structure and Organisation Near Steady State
Guppy populations play an integral role in the organization of the
laboratory systems, functioning as a dominant predator and competitor and
being subjected to exploitation simulating fishing. At each level of
habitat availability and energy input, changes in guppy biooass resulting
from exploitation apparently brought about major changes in the biomass
of ether populations composing the cormunities. Guppy populations were
directly affected by dieldrin, their response co the pesticide b*ing
dependent upon the rate at which they wore exploited.
Oranges in guppy population bioaass can be operationally explained in
terms of population biomass gains from production (grovth and reproduction)
and losses to mortality including yield to exploitation. Survival, growth,
and reproduction are integral parts of ths life history patterns of indivi-
dual organisms. Individuals develop different life History par:eras under
different sets of environmental conditions, -,hn* maintaining concordance with
these conditions. Developmental as well AS evolutionary changes in life
history adapt populations to persist and underlie changes in population pro-
duction, yield, and biomass brought about by el-mages in exploitation rate,
habitat and energy level, and dieldrin.
Guppy Population Biovass, Production, and Yield Near Steady-State
Mean near steady-state guppy biosasses corresponding directly to a
near steady-state guppy trajectory patterns ur. predation and competition
56
-------
phase planes, (Figure 6-12) are shown in Figure 13. At each level of
habitat availability and energy input, mean guppy biomass decreased
as the level of exploitation increased. Dieldrin led to a decrease
in mean guppy biomass of approximately 24 percent at zero exploit&ton
(followed by an eventual recovery), 32 percent at ten percent exploi-
tation, 46 percent at twenty percent exploitation, and 100 percent
(eliminating the guppy population) at forty percent exploitation.
Increased level of energy input and habitat aval.!ability resulted
in an increase in mean guppy biomass.
To maintain guppy population biomass near steady-state, production,
or the rate of elaboration of tissue through growth and reproduction,
must equal the rate of loss of tissue to yield and natural oortality.
At the low level of habitat availability and energy input, very little
natural mortality occurred in populations exploited at 10, 20, and <»0
percent, and consequently near steady-state production is approximately
equal to near steady-state yield in each population. At the 0 percent
exploitation rate, since yield was zero, near steady-state natural
mortality rate must equal near steady-state production. Observed near
steady-state natural mortality of fish above the newborn size in the four
systems that received dieldrin were, before and after dieldrin intro-
duction, 0.17 and 0.31 grams per month for zero exploitation, 0.01 and
0.00 for 10 percent, 0.0 and 0.08 for 20 percent, and O.OC and 0.00 for
40 percent exploitation.
Changes in the magnitudes of production and yield curves represent
changes in the productivity of the system f&r guppies. Increasing habitat
avail ability and energy input rate increased system productivity, while
exposure to dieldrin reduced the productivity of the systems for guppies
57
-------
- y"^>v?
!«£«» "^-x^
-Lneui
-------
(Figure 14); see also Figure 3). Guppy production at high habitat availa-
bility and energy input was not deterained. The relative position that
such a curve would occupy is shovn.
Increasing exploitation rate resulted in reduction in guppy biomas:
and essentially shifted production and yield values from right to left
along the dose-shaped curves. Increased habitat and energy input in-
creased guppy food resources, this resulting in increased guppy biomass,
production, and yield at each exploitation rate. Shift to the right in
the relationships between suppy biomass and the biom&ss of their food •
(Figures 9 and 10) characterised the increase in productivity caking
possible the increased magnitude of guppy production and yield curves.
AC low habitat and energy input, exposure to dieldrin reduced tho
magnitude of guppy production and yield curves. Dieldrin directly
affected only the guppy populations and, as will become apparent, altered
life history patterns by reducing size-specific growth and reproduction,
as well as survival, this accounting for decreased guppy biosass and
reduced magnitude of production and yield curves,
Guppy Size-Specific Growth and Fecundity Near Steady State
The life histories of individual organisms include 'Jie patterns of
growth and reproduction they manifest when exposed to different sets of
environmental conditions. Guppy sire-specific relative growth rate near
steady-state was affected by exploitation rate, exposure to dieldrin, and
level of habitat availability and energy input. Changes in these environ;
mental conditions altered not only life history patterns but also popu-
lation density and cosounity structure. Growth was deterained u change
in body weight per unit of body weight per month. Elaboration of somatic
tissue was not separated froa elaboration of reproductive products in nature
-------
4.0 r
0 c -
£ § ?-4
O.S1
Z 0.8
\
t i
J L
8
16
20 24 23 32 36
4.0 r
\2 16 20 24 23 32
MEAN GUPPY SiCMASS (grams)
36
Figuro 14.
Mean nenr 5teady-state guppy population production (upper axis) and
yiald (lower axis) as a function of Bean noar steady-state population
bioaaas- Guppy exploitation rises are indicated asO- 0, O- 10
^ 2^'.*nl C" 40 PeTCOTlt P«T aonth. Open symbols are production
and yield for low energy input systeas; the four circled open
fyabols are low energy input systmu into which dieldrin was
introduced. The lowest curves represent near steady-state
production and yield after introduction of dieldrin at the low level
of habitat availability and energr input. The highest curves
represent production and yield at the high level of habitat availa-
bility and energy input. Produc':ioa at high habitat and energy
input was not able to bo dettrained, but the relative position
that such a curve would occupy is shown by the dashed line.
60
-------
Elaboration of reproductive products occurs continuously in nature guppies.
Male guppies reached sexual maturity near 15 millimeters and their growth
after that was often negligible.
Due to the ouch greater densities of fish at the high level of habitat
and energy input, individual guppies could not be realiably followed from
month to month. Consequently, sire-specific relative grovth rates and
production could not be determined.
At each exploitation rate, relative growth rate decreased as the fish
grew larger (Figure IS). Growth rates of iamature (newborn, 10-14 am) and
mature fish of a given sire was density-dependent, or related to population
biomass and consequently to exploitation rate (Figures 15 and 16). The
highest growth rates occurred at 40 percent exploitation where population
biosass was lowest, one' the lowest growth rates occurred at :ero fezploi-
tation where population biooass was greatest.
In general, at both the high and low level of habitat availability
and energy input, sire-specific fecundity appeared to be density-dependent,
the highest fecundity occurring at 40 percent exploitation and the lowest
*
fecundity occurring at 10 percent exploitation (Figures 17 and 18).
Fecundity determinations were made on exploited females end, therefore,
fecundity estimates are not available for females in populations exploited
at zero percent. Similar density-dependent effects on fecundity in exploited
guppy populations were found by Liss (1974).
At the low level of habitat availability and energy input rate
(Figure 17), there was overlap in fecundity relationships between systems
exploited r.t different rates, making interpretation of fecundity data
rather tenuous. Average fecundity data for the four systems at each
exploitation rate suggested that sire-specific fecundity was related to
exploitation rate ami population density. At each exploitation rate, si:e
61
-------
Low Efiirgy Input
Low Efltrqy Input
with Oitldrm
~oo* o.'2 C.Z7 03* 0.91
MEAN SIZE OP A GUPPY tN OESfCNATEO SIZE CLASS
Figure IS. Guppy aeon relative growth rate near steady-state for the systems
at the low level of habitat availability and energy input before
(open symbols:) and-after (solid symbols) introduction of dieldrin. Cupoy
exploitation, rate is indicated aso-0, c-10, a-20, and O--40 percent.". Fish
sire is expressed as length (tra) and as cean weight (grass) for
each si:e class. The population exploited at 10 percent did not
establish a steady-state after introduction of dieldrin and, con-
sequently, growth rates of individuals from this population are not
shown. Th« population exploited at 40 percent went extinct after
dieldrin introduction and growth rates are zero. After Kolcertr$
(1980). .
62
-------
* zoe
a IOE
o OC
S O.»r
3 ~ *)•»*«"•»
S
0«-
5
1
Figure 16. Guppy mean relative growth rate near steady-state as a function
of near steady-state population biooass at the low level of habitat
availability and energy input. Cuppv exploitation rare is indi-
cated as O- 0. O 10, A- 20, and &- 40 percent. Open svabols
represent growth rate .prior to introduction of dieldrin and solid
syabols represent growth rate after exposure to dieldrin. The copu-
lation exploited at 10 percent did not establish a steady-state'
after introduction of dleidrin and consequently growth rates of
i^iXHlS13 ^ thi* o0""1"*0" «re not shown. The ooouiation
exploited at 40 percent went extinct after dieldrin introduction
«d growth rates are :ero. No-, all populations had tish in the
35-39 m size class. Curves were fit by eye.
63
-------
«0r
o
*
IU
u.
0.
0.1 O2 0.4 to L4
MEAN SJ2£ MATURE F&MALS
FigU70 17. Guppy fecundity (scan nuaber of epgs and embryos carried by an
exploited female of given si:e) near steady-state for laboratory
ecosysteas At the low level of habitat availability energy input.
Guppy exploitation rate is indicated as O- 10, £ - 20, and £7-40
percent. Inset shows average fecundity of the fours systeas at
ecch exploitation rate. A linear regression was fit to the data
for each systea; r values were between 0.8S and 0.99. After
Weltering (1931).
64
-------
specific fecundity was greater in fish at the high level of habitat availa-
bility and energy input than in fish at low habitat and energy input
(Figure 18), this probably reflecting the greater availability of food.
Information on near steady-state relative growth rates and fecundities
of fish exposed to dieldrin is liaited to those exploited at 0 and 20 per-
cent. The guppy population exploited at 10 percent never established a well-
defined near steady-state after exposure to dieldrin. The steady-state
of the population exploited at 40 percent after exposure to dieldrin was
extinction. Thus, the effect of dieldrin on the relationship between relative
growth rate and population biomaas is only suggestive and is inferred from
information on populations exploited at 0 and 20 percent.
Dieldrin apparently reduced the relative growth rates of juvenile fish
and small nature females up to 24 ma in length ^Figure 16). For each of
these size classes, the relationship between relative growth rate and popu-
lation bionass was shifted downward, indicating that fish in populations
of a given bionass grow sore slowly after exposure to dieldrin. Since so
few fish reached the larger site groups, it is possible that effects of
dieldrin on growth of larger fish was undetected.
Dieldrin reduced sire-specific fecundity of nature female guppies,
this contributing to reduction in relative growth rate (Figure 19). Since
growth rate of immature fish 10-14 na in length was decreased, dieldrin
evidently decreased somatic growth as well as elaboration of reproductive
products.
The relationship doveloped at 40 percent exploitation rate after ex-
posure to dieldrin is a non-steady-state relationship that was fit to
fecundity information collected during the six aonths prior to extinction
65
-------
100 r
in
Q
90
80
2 70
-------
60r
IOE
42mm
f$J^^m .^^.„^p«^__L_u__
0-1 0'.2 ' 0'.4 LO 1.4 2.0 g
MEAN SIZE MATURE FEMALE GUPPY
Figure 19- Guppy fecuncity (sean number of eggs and embryos carried by an
exploited fecale of given sire) in ecosystems at the low level
of habitat availability and energy input before (open synbols)
and after (solid symbols) dieldrin introduction at 10, 20, and
40 percent exploitation rates (system 2-40E, systea 4-20E. •
systso 14-1CE). A linear regression was fit to the data for
each systen; r values were between 0.85 and 0.99. All relation-
ships except that .it 40 percent exploitation after dieldrin
introduction were determined when the systems wero near steady-state.
The guppy population exploited at 40 percent we;tt extinct after
exposure to dieldrin. The fecundity relationship shown here
was constructed froa size-fecundity information obtained over the
seven oonths just prior to extinction (see Figure 12). After
Weltering (1981).
67
-------
when population biosass was declining (see Figure 12). It indicates that
reduced fecundity as well as poor survival of newborn fish and probably
also reduced growth were all responsible for bringing about population
extinction.
Changes in conditions in the environments of the laboratory ccasani-
ties such as exploitation rate, habitat availability and energy input, and
exposure to a toxicant brought about changes in guppy life history pattern,
population density, and consunity structure. That particular guppy life
history patterns can be associated with particular cosaunity structures is
evidenced at least at low habitat and energy input levels. Increasing
exploitation rate resulted in reduction in length of life (as a result of
increased fishing aortality) snd apparent density-dependent increases in
size-specific growth rate and fecundity. Exposure to dieldrin altered
lifj history patterns in that it reduced newborn survival, size-specific
growth rates, and fecundity. SOBS of these kinds «£ effects on guppy life
history patterns were also observed in separate aquarium expeviaents aore
like sisple toxicity tests.
Cohort Size-Specific Biooass, Production, and Yield Near Steady-State
Mean near steady-state bicsass of each size class of guppies at the
low level habitat availability and energy input is shown in Figure 20. So
long as the population is at steady-state, the pattern of change of size
class biosass froa newborn to the largest feaale can be taken to describe
changes in biooass of a cohort as it aoves through size classes. The SUB of
the roan near steady-state bioaasses of all size classes equals asan near
steady-state population biooass.
68
-------
20,-
MEAN NO. OF FISH:
29 4.4 OB Ql O2 05 O Contiol O
40%
14 09 1.3 09 Ci >ol 05
16 09 or oe ' tMim o
2O%
136070 00
16 1338 IS
RID
o%
o»
i«i nnd aftfr fin Mr! Kvnlmlsl tllelflrln introduction. Site is expressed both as
-------
At each exploitation rate, changes in cohort bioaass are
by the rate that a cohort elaborates biosass through production and the
rate that it looses bioaass as yield and natural aortality. Wlten pro-
duction is greater than yield and natural aortality. cohort bicumass
increases and when production is less than yield and natural nortality
the bicsass of the cohort declines. If the cohort is exploited at the
sane rate at all ages, TnariTrmin yield is obtained from the cohort when its
bioaass is greatest.
At all exploitation rates. size clav; bioaass decreased somewhat
between the newborn and 10-14 aa (0.12gJ size class probably as a result
of high asrtality of young, at least in part rac-lting froa cannibalise,
Size class tiomass was greatest ir, the 20-34 aa sire class, except at :ero
exploitation where high density and relatively slow growth resolved in few
guppies reaching larger sizes.
Production of fish in each size cltss can be determined as the product
of relative growth rate (Figure 16) aoc* bioaass (Figure 20} of the size
class. Size class production is represented in Figure 21 as a function of
czean near steady-state population bioaass. The yield of each size class as
a function of population bioaass is shown in Figure 22. At each exploitation
rate, the sua of the aean near steady-state production and yi«ld values of
all sire classes equals neon near steady-state population production and
yield, respectively. Production and yield relationships for each size
class, as well as total population production and yield (Figure 14). are
dome-shaped curve:!. Families of production and yield curves exist for
each sin class, with exposure to toxicants altering the sagnitudes of
these curves.
70
-------
a JOE
A 23 E
o we
« oc
N8
lO-t4
ZS'SSnvn
. 39.39 am
Z«*802««
MCAM CUPfY POSMUATION 8IOMAS3 (g)
Figure 21. Guppy sire class mean production near steady-state aj a function
of near steady-state population bionass fur four low habitat
availability and snergy input systems (O- 0, O- 10, A- 20,
and Q- 40 percent) before (open symbols) and after (solid symbols)
dieldrin introduction. The population exploited at 10 percent did
not establish a steady-state after introduction of di*l<«rin and
site cltss production from this population is not shovn.. The
population exploited at 40 percent went extinct after dieldr't
introduction and size class production is zero. Curves wen ;it
^ by eye. Af?:c.r Weltering (1981).
71
-------
Figure 22. Guppy size class nean yield noar steady state as a function of
near steady-state population bioaass for four low habitat availa-
bility and energy input system* ( O- 0, O-"lO, £ - 20, O - 40
percent) before (open synbols) and after tsolid iyebols) dieldrin
introduction. The population exploited at 10 percent did not
establish a steady-state afver introduction of" dieldrin an-i sire
cl«s yield from this population is no- shown. Th« population
exploitsd at 40 percent went extinct after dieldrin introduction
and sire class yield is :ero. Curves were fit b" eye. After
Weltering (1981).
72
-------
Size class production is greatest in the scalier si:e classes where
organ! sos ore growing oost rapidly (Figures IS and 16). Although si:e
class biomass is large in the older size classes (Figure 20} . growth rare
has been so reduced that production, the product of growth rate and bio-
mass, is low. Size class yield is greatest in the larger si:e classes
where size class bicaass reaches a
Thus, a pattern of guppy cohort dynamics becoses apparent. When a
cohort passes through the smaller size classes, individual relative growth
rate and cohort production are high and yield and other losses to natural
aortal ity, after the newborn stage, are relatively lower end, in general,
cohort bioaass increases. As the cohort passas through successively
larger sizer classes, relative growth rate and production decline and
yield increases, the cohort reaching its eaxisua bioaasa whoro cohofi
production equals cohort yield (and other aortal ity). At this point
cohort yield is ppxima- In the largest size classes, cohort yield is
greater than cohort production and cohort bioaass declines. Even though
cohort production nay differ from cohort yield (and other losses) in a
particular size group, total production of the cohort throughout its
lifetime must equal total cohort losses to yield and natural aortal ity
to aaintain the population at steady-state.
It is just such dyna&ic patterns of cohort, bioa&ss, production,
and yield that underlie steady-state population bioaass. production, and
yield and represent on is^ortar.t aspect of population structure and
organization. And it U the life history patterns — dynanic development
patterns — of individual organisms — that vaderlie and determine dynanic
patterns of cohort bioaass, production, end yield under different sets of
environ&ontal .^nditisns.
At the low level of habitat availability and energy input rats,
-------
dieldria reduced the magnitude of guppy population production and yield
(Figure 14). This decrease can be accounted for trriaarily through
reduction in production sad yield of isnarure and ssall nature fesales
(Figures 21 and 22). These reductions resulted £rca decreases in both
the. bicaaases sod relative growth ratss of these sire classes (Figures
16 and 20).
Effects of Oieldrin en (torpy Life History Patterns
Deterained in Aquariua Experiments
* ' *
; The ispact of dieldria on the life history patterns of guppies was
determined in aquarium experiments core like staple toxicity tests. The
latent was to relate the results of these «xperi3ents to effects ca guppy
life history patterns, population dynamics, and cosssunity structure and
organization observed in the laboratory ecosystecs a&i t? begin ta
evaluate the extent to which these relatively sisole experinonts con-
tribute to understanding and prediction of toxicant effects in zore
coaplex syrtecs. The aspects of the Ufa history patterns of cohorts of
guppies that were exaained include juve&ile and adult growth and survival,
age and sire at first reproduction, clutch sire cr number of offspring
produced at eich reproduction, and intrinsic rate of increase (Kulbicki.
1980).
As juveniles, parental fish receiving a high ration (HR) grew signi-
ficantly faster than parental fish receiving a low ration (LR). At each
ration level, F-l fish exposed to both conseatrations of dieidrln grew
significantly less than control fish, but: there were not significant
differences between growth of fish exposed to high dieidrin concentration
(KD; I ppb la water, 4 ppa in food) and these exposed to low dieldria
concentrations (LO; 1 ppb iA water, 2 ppa in food) (Figure 23).
74
-------
o>
160
160
140
120
_ iOO
.S* 80
-------
Parental fish were first exposed to dieldrin when they reached sexual
maturity. At siailar dieldrin treataents, nature fish receiving the HR
grew faster and attained a larger weight at each age than fish receiving
the LR (Figure 24). At each ration level mature control fish had greater
growth rates and attained larger weights at each .age than fish exposed to
dieldrin. At HR, fish exposed to HD grew sore slowly than fish exposed
to LD.
Cumulative juvenile aortality curves of parents and their f-l progeny
are shown in Figure 25. Same parental fish, especially at LR, were
affected by disease which resulted in higher juvenile aortality of parental
fish than F-l generation control fish. In general, increased dieldrin
concentration resulted in decreased juvenile survival. At LR, however,
fish exposed to HD suffered less aortality than those exposed to LO. No
effect of ration level or dialdrin on survival of mature fish was observed.
Age at first reproduction is an apparently isportant reproductive para-
aster, since it has a large influence on the intrinsic rate cf increase, a
decreasing age at first reproduction tending to increase r. Ration level
had no apparent effect on age at first reproduction (Table 3). At HD, fish
receiving HR first reproduced at a soaswhat younger age than control fish
while fish receiving LR reproduced at an older age than controls.
During their juvenile stage, fish at HR grew faster and attained a
larger weight at first reproduction than fish receiving the LR (Table 5).
In addition, at high ration, there was a significant reduction in si:e at
first reproduction as a consequence of exposure to dieldrin, *hilt at LR a
slight but nonsignificant reduction was observed.
'Jusber of offspring produced by fesale* is apparently related to
fc&ale weight sad thus to previous growth history (Figure 26). At each
ration level, offspring nucbor appeared to increase as :esale wsigh;
-------
o
^
o
Q.
Oi
a
V
"a
v
1600
1400
1200
1000
800
600
400
200
1200
1000
800
SCO
400
200
High rotion:
• Control
H H
Low rotion-
O Control
QL3* dieldhn
x .
i
^'i
'. i
40 60 80 100 S20 140 160 160 2CO 220 2^0 260 230
Age of female a! reproduction (daysl
Figure 24. Effect of dieldrin on adult growth of parental fish at low and
high rations. Vortical lines represent two standard deviations
for feaale weight and horizontal Unas represent two standard
deviations for feaale age at reproduction. Each point is an
•verage of ten fish. After faUbicki (i960).
7?
-------
Patents:
* Hujb iQliofl (309)
OLofi lotion (50!)
r-i:
High ration
• Conlioi (151)
• I o« dicldiin (15?)
-a---oV>v--A—A—A
i i i
Low mliofl
O Conliol (64)
Oio«dieldiin (73)
6 0 10
Age (weeks)
Figure 25. emulative juvenile nortallt/ of parental ou.l F-l generation fish. Ilio initial mtnlicr of
fish la oiith trcatucnt is given in parenthesea. After Kulbicki (I960).
-------
Table 3. Suaaary of the reproductive perforaances of female parental fish.
The first number is the aeon value for ten fish and the second is
s/~n"T All weights are in ag. .
r!CH RATON
Clatch
oamber
a
8
1
2
3
4
CJatch
anmber
Z
a.
a
o
.4
c
1
2
3
4
Utttch
ai raver
Z
3
5
a
t
2
3
4
Age
(d*yi)
131.1
1.6
172.3
2.2
212.3
2.7
252.3
2.9
Age
(din)
129.2
1.2
169.0
0.8
207.0
1- 5
245.7
2.5
A|t
(d«yj)
125.9
2.3
168.7
1.9
204.2
1.7
242.3
2.1
Gotttioa
period
40.9
0.0
40.0
0.7
40.0
0.5
GcJtitiaa
period
(d»v» )
38.8
0.8
38.0
1. 0
38.8
1. 1
Gaiudaa
period
(diyt)
41. i
1.2
35.6
0. 4
37.9
I1;. 6
Ftmtit
680
45
914
77
1117
128
1270
140
rem»u
weigh?
(mg,
507
26
729
41
816
30
980
45
Female
weight
<«!)
365
23
600
41
733
44
777
52
Mcu
clutch
lite
23.2
1.7
31.1
2.2
22.4
4.2
21.3
2.3
¥
Me 10
clutch
fin
19.2
2. 1
21.5
3.0
34.0
4.4
22.9
3.7
Mc&a
clorth
til*
11.9
2.5
11.0
2.4
24.3
4.0
IS. 9
3.4
Meaa
clutch
weight
118
14
169
17
123
23
132
!2
Veto
clutch
weight
92
12
111
19
Io3
22
121
21
Me*a
elate*
weigh*
48
10
51
13
114
19
83
19
Veto
weight of
ofbpriog
5.00
0.34
5.36
0- 27
5.50
0. 18
0.27
0.21
Meu
weight of
offspring
4.75
0.27
5.05
0.42
4. 9^
0. 17
5.07
0- 24
«...
weigh! of
offiprtnf
4. 15
0. 24
4.22
0. 30
4.64
0-15
5.13
0.21
-------
• low RATION
Clutch
CONTROL
LOW DIHD1UN
KIWI Ota IDOt ••
1
2
3
4
Clutch
1
2
3
4
Catch
VttSiHf
1
2
3
4
AI«
(day*)
132.4
3.8
168.4
3-9
208.6
4. 0
248. 1
4.3
AC*
«d*yi)
134.1
3.8
171.0
5.6
209.4
5.4
255.3
3.9
A,t«
(d*y»>
141.1
3.4
183.0
4.5
219.6
4.4
258. b
4.2
Ccstatiav
pcrioa
-------
60
2.0
J2
E
60
40
20
40
20
Control:
• High ration
o Low ration
o ^
^— * "
- *a
• •
2000
2150.
1600
Low disidrinr
• High ration
oLow ration
High dieldrin'-
*High ration
*Low ration
100 200 400 600 800 1000 1200 1400
Weight of female (mg)
Figure 26. Relationship between clutch si:e and female weight. Each large
point represents the average clutch si:e and f«aale weight for
a given gestation period. After Kulbicki (1980).
-------
increased over a range of lower weights but, at higher weights, appeared
to level off. Variability in offspring nuaber increased with fesale
weight. .
Offspring production was dependent upon ration level as well as
feoale weight, with fish of a given weight at La producing few offspring
than fish of the saae weight at HR (Figure 26). Thus, fish of a given
age at HR had larger clutches than fish of that age at LR (Table 3), both
because they were larger at that age and because the/ ingested a greater
mount of energy which could be channelled into reproductive products.
The relevance of food consumption rate and previous growth history
(female weight at reproduction) to offspring production is particularly
evident at first reproduction. At HR. fish were fed a greater anount of
food, grew acre rapidly as juveniles (Figure 23). attained a larger size
at first reproduction (Table 3, and produced about three tiass aore off-
spring at first reproduction than fish at LR.
Because of the apparent dependence of clutch size on fesale weight,
M
there say be reproductive consequences of toxicant effects on juvenile
and adult growth, with decreased growth resulting in reduction in weight
of a feaale of a given age and consequent reduction in age-specific clutch
size. But a toxicant nay also directly effect clutch si:*, bringing about
reduction in the nusber of offspring produced by fish of a given weight.
This is evidenced by a lowering of the relationship between clutch si=e
and body weight.
Interpretation of the effects of dieldrin on clutch si:a is sosewhat
difficult because of the relatively high variability in clutch sire of
fish of a given weight (Figure 26) or age, and because there was statis-
tically significant interaction between ration levti, dioldrin concen-
tration, and gestation tiaes, this precluded statistical comparisons
CKulbicki, 1980).
-------
At both HR and LR. KD reduced the size of the first clutch produced
by fenale guppies. First clutches were saaller in fish exposed to HD at
least in part because their weight at first reproduction was lower than
the weight of control fish. However, at low ration, size of the first
clutch at KD was 40 percent lower than first clutch size at LD, even
though the fscales naintained siailar weights (303 ng at LD and 306 ag
at KD). This suggests that HD may have directly affected size of the
first clutch.
At HR, KD reduced both age- and size-specific clutch size for the
second through fourth clutches (Table 1, Figure 26). At all dieldrin
treataents at LR and LD at HR, very little effect was apparent on age-
or size-specific clutch size. Even though dieldrin reduced growth and
thus fesale weight at a given age at both LR arJ HR (Figure 24), by the
tiao fish produced their second clutch they had apparently reached the
plateau of offspring production for that ration so that increases or
decreases in fetaale weight at reproduction did not affect clutch size.
Thus, reproductive consequences of effects on growth are aainly evident
at first reproduction, over the weight range that clutch size is dependent
upon body weight. -
Fish receiving the HR had a greater intrinsic rate of increase (r)
than fish receiving the LR (Figure 27). These differences in r can be
attributed to development of different life history patterns at LR and HR.
At HR, fish had greater juvenile growth, attained a large1* size at first
reproduction and produced a larger first clutch than fish at LR. In
general, the.first reproduction makes the greatest contribution to the
value of r. In addition, fish at KR get* faatar as adults, attained a
*
larger sise at each reproduction, and produced larger clutches at each
size and age than fish a: LR,
83
-------
CX0220
aoaco
j§ aotso
2.
1 aoiso
•2 0.0140
o
«o
~ aoi2o
a
o
aoioo
O.C080
0.0060
— 0.0040
O.OC20
High ration:
• Control
• Lev* dieidrin
A High dieidrin
Low ration:
O Control
a Low dieidrin
A High dieidrin
0
2 3
Clutch number
Figure 27. Values of the intrinsic rate of increase calculated for successive
reproductions. Comparisons between treataents Mere based on the
values of r at the fourth clutch. If survival and reproduction
hod bean aonirored through sore than four clutches, the calculated
values of r would not have been substantially different than the
value r calculated at the fourth clutch (Suibicki, 1S80).
Reproduction by the youngest age classes aakes the greatest
contribution to the value of the intrinsic rate of increase.
After JCulbicki (19301
-------
At both ration levels, the magnitude of r for cortrol fish and fish
exposed to LD were similar. Even though fish at LD grew more slowly than
control fish, there was little difference in age at first reproduction aid
clutch sizes between these treatments.
At both ration levels, the values of r for fish exposed to KD were lower
than those of control fish. KD reduced juvenile and adult growth and the
size of the first and, at HR, of subsequent clutches. In addition, at LR,
HD delayed age at first reproduction.
At least at KD, dieldrin altered guppy life history patterns in
relatively simple aquariua experiments in a way broadly similar to the
way the toxicant altered life history patternns in the laboratory eco-
systems. In the aquarium experiments and in the laboratory ecosystems,
dieldrin reduced newborn survival (Figure 25), growth (Figures 16, 23,
and 24), and reproduction (Figures 19 and 26; Table 3). Further possible
relationships will be considered in the discussion.
-------
: DISCUSoIffii
f*
Generalisations pertaining to the organization, development, persistence,
productivity, and adaptation of ecological systems were presented la the
introduction and will be incorporated her* to accoxnt in part for the per*
£bnance", of the laboratory coasunities, thus deaonstrating the usefulness
and confers!ty with observation of such system of generalisation«. Any
perforsanee of an arganisnic system can to understood ja the consequence
of the »yst«n's capacity ana of its en.iran^mt.. The 16 laboratory eco-
system were established with similar potential capacities for developoent,
structure, and persistence. Their potential capacities arise froa
incorporation of the potential capacities of th^ intvxiuced species and
entail all possibilities for interacti/* per-orasntes of these species.
Some understanding of these capacities was obtained by exposing the
t
system to different develipsmtal envircnaents, which consisted of
different oxploitation rates, different l«vn',s of habitat availability
and energy input, and exposure to a toxicant. Under «ach set of environ-
aental conditions, the systeas developed steady-state structures. Thus,
ecological system can be tuought of v» being ariltistbady-stito systeus,
with steady-state structures being datarsdned by system potential capacity
and systea developmental envlrumwat. The responsfts of the system to
toxicant introduction w&s affected by conditions in the systeos' environ-
oents, including rate of ex?'.Citation aa- level of habitat availability
end energy input. At the low level of h*i.:at availability and energy
input, responses ranged froa slight perturbation and subsequent recovery
of systea structure at zero exploitation rate to aajot perturbarion of
systea structure including population extinction at 40 percent
exploitation rate.
S6
-------
The capacities of systems are determined by the way they are organized.
The trophic organization of the laboratory ecosystems entails incorporation
and concordance of the capacities of the species populations. System
organization underlies and determines system structure — species kinds and
densities -- under each set of system environmental conditions.
Predation, competition, commensalisa, and mutualism represent classes
.of relationships between species populations that may be concordant.
Guppies and snails are the dominant species in the laboratory ecosystems
and-together with amphipods appear to compete for the common food resource,
organic sediments. In addition to being competitors, amphipods are also
prey of the guppies. Coexistence of the competing species is not wain.-:
tainedsimply by exploitation of one of the competitors (Paine, 1966;
Menge, 1975) because all populations are able to persist at near steady-
states when the guppy population is unexploited. Changes in exploitation
rate, however, alter the densities of guppy populations and so indirectly
affect amphipod and snail populations, this leading to different community
structures (Figures 5, 7-11).
Behavior observations suggest that resource partitioning may be im-
portant in system organization and determination of steady-state structure.
Guppies, amphipods, and snails feed heavily on the organic sediment derived
from the alfalfa ration. But these populations also prey upon food re-
sources other than the organic sediment. Snails appear to prey extensively
upon attached algae, thus reducing overlap in food utilization between
competitors. The structure and organizaton of the algal subcommunity and
its role in the laboratory ecosystems, including its utilization by snails,
has begun to be evaluated. Guppy populations also apparently prey somewhat
upon nenatodes (Finger, 1980) and perhaps other microinvertebrates as well
as amphipods.
87
-------
In addition, guppies may prey most extensively on the a..falfa ration
just after it is introduced as it sinks through the water column and comes
to rest on the surface of the rock substrate. Food material that settles
into the rock substrate is not as available to the fish and is preyed upon
primarily by benthic dwelling snails,, anriiipods, and microorganisms.
Thus, partitioning of the habitat between benthic snails and amphipods and
the more pelagic guppies may result in partitioning of the alfalfa food
resource.
Anphipod populations maintain relatively small populations at both
high and low levels of habitat availability and energy input. This results
in part because of the interrelationships between the amphipod, guppy, and
sn'U.l populations, with amphipods not only competing with guppies and
snails for food but also being preyed upon by guppies. In addition, the
food and perhaps physical and chemical aspects of the habitat may not be
very favorable for amphipods. The rock substrate serves as a refugiua for
amphipods where they can escape guppy predation. In the presence of
guppies, aaphipods prefer the rock substrate, but in their absence (such
as after guppy population extinction), the amphipods move freely through-
out the tank. Such habitat partitioning favors persistence and coexistence
of the predator and prey.
Increased habitat availability and energy input altered system
structure by increasing densities of organic sediments, guppies, amphi-
pods, and snails at each exploitation rate. On phase planes representing
the interactions between populations, the relationships between population
densities generated by changing exploitation rate were shifted upward and
to the right (Figures 9,10,11). The structure of the nicroinvertebrate
subcoansaiity was also altered with species dominance shifting from
88
-------
nematodes, protozoans, and ciliates at low productivity to euglenoid
x'
flagellates at high productivity (Finger 1980).
A generalized isocline model representing some possible effects on
steady-state system structure and organization of energy input, exploitation,
competition, presence of alternative prey, and a toxicant is shown in
Figure 28. It demonstrates how population interactions including predation
and competition, exploitation, and rate of energy input jointly determine
community structure and organization and response to toxic substances. At
each energy input rate, a relationship between predator &nd prey biomass
defined by a prey isocline or family of prey isoclines is (experimentally
or theoretically) generated by changing exploitation rate. In the generalised
model, this relationship is shown to be similar to the relationship between
guppy and amphipod populations at low habitat and energy input (Figure 7)
or that between guppy and sediment at high habitat and energy input
(Figure 11), with increasing exploitation rate bringing about reduction in
steady^-state predator biomass and increased prey biomass. Increased energy
input rate shifts to the right on each phase plane the relationship between
predator and prey biomass defined by a prey isocline or family of prey
isoclines, this increasing both predator and prey biomass at each exploi-
tation rate. Similar responses to increased energy input rate were observed
in the laboratory ecosystems (Figures 9, 10, 11).
The presence of a competitor of the predator, or competitors of the
prey, or competitors on lower trophic levels leading to the prey shifts to
the left the relationship between predator and prey defined by the prey
isoclines at each rate of energy input, resulting in reduced predator and
prey biomass at each exploitation rate (Booty, 1976). Coexistence of the
competitors is dependent upon rate of energy input and rate of exploitation.
At low energy input, the exploited predator is capable of persisting at
89
-------
Figure 28. A. Generalized phase plane and isocline systems representing
... . • the interaction between predator and prey, and some possible
• -••'•• effects of energy input rate, competition (comp.), toxic
substances (tox.), plant nutrients (nut.), exploitation (E),
and alternative prey (alter, prey). Steady-state points are
indicated at the intersections of predator and prey isoclines.
At each rate of energy input, presence of a competitor, toxic
substances, or decrease in plant nutrients can shift the
prey isocline to the left on the phase plane and can cause
reduction in steady-state predator and prey biomass at each
exploitation rate. At each exploitation rate, presence of
• ! ' alternative prey can increase ,and toxic substances lower a
predator isocline, as shown at 20E. If a predator isocline
identified by a particular level of environmental factor (e.g.
higher E or 40E, TOX.) does not intersect a prey isocline
identified by another environmental factor or factors (e.g.
low energy input with competitor present — dashed prey
isocline), then the predator population cannot persist under
that set of environmental conditions (solid hexagon).
B. Theoretical relationship between predator relative growth
rate and prey biomass shewing direct effect of a toxicant on
growth rate relationship.
C. Predator steady-state production and yield curves and how the
magnittxdes of these curves can be affected by energy input,
competition, toxicants, plant nutrients, and alternative"
prey. Each curve is derivxl from a prey isocline on the
predator-prey phase plane.
90
-------
Figure 28-
LOW
ENERGY
INPUT
en
2
O
5
O
UJ
e
Q.
HIGH
ENERGY
INPUT
\ \
COM, TOX. r~"T*wiiT
*NUT. \ \ *NU~
.O
CO MR, TOX
'\
V
\
OE
10 E .
,«
tALTEP. PREY.0-
*|TOX. 20 E
1-^40 E
HIGHER E
-40E,TOX.
PREY BIOMASS
a
ui
J^
O>Q:
O
PREY BIOMASS
ALTER. PREY
COMR,TOX\1U
*NUT.
HIGH
ENERGY
INPUT
PREDATOR BIOMASS
ALTER. PREY
HIGH
NERGY
INPUT
PREDATOR BIOMASS
91
-------
high exploitation rates (higher E) in the absence of competiton (dotted
hexagon). But, in the presence o£ the competitor, the predator isocline
identified by "higher E" does not intersect the prey isocline (dashed
isocline). Coexistence is not possible under these conditions and the
heavily exploited predator is driven to.extinction (solid hexagon). The
exploited predator and its competitor are capable of coexisting at lower
exploitation rates (other solid symbols), or at high exploitation rates
(higher E) at the high rate of energy input (open hexagon). The presence
of additional or alternative prey for the exploited predator shifts the
I •jdator isocline upward at each exploitation rate and thus may facilitate
coexistence of competitors at the low level of energy input. Exploitation
or predation on the competitor (cf. Paine, 1966; Menge, 1975) would tend to
reduce the amount of leftward shift of the prey isocline and thus would also
facilitate coexistence at high exploitation rates.
A competition phase plane relating the biomass of the exploited
predator to the biomass of its competition can also be constructed. Like
the predator-prey phase plane shown in Figure 29, the competition phase
plane could illustrate the effects of exploitation, predation, energy input,
and other environmental conditions on steady-state bomasses of the com-
peting populations (Booty, 1976; Liss, 1377). Relationships similar to
those between guppies and snails (Figures 8 and 10) could '•« deduced. In-
creases in exploitation rate could be shown to bring about reductions in.
the density of the exploited predator (the guppy) and increases in the
density of the competitor (the snail), with the relatonship between the
competitors being shifted to tha right on the competition phase plane with
increases in energy input rate. Thus, in Figure 29, at each energy input
rate, the presence of a competitor shifts the prey isocline to the left
92
-------
Figure 29. Possible changes in steady-state predator population adaptive
• •• • capacities corresponding to changes in steady-state predator
• population densities- Each circle represents how well ?r.
individual is adapted to each of two sets of environmental
' ' 'conditions, OE, No Tox and OE, Tox. The set of circles
labelled with (1) represents the adaptive capacity of the
population when it is at steady-state at low energy input,
OE, No Tox. The individuals are not well adapted to toxicant.
Introduction of toxicant reduces steady-state predator
population density (2). But the population adapts evolutionarily
to the toxicant and increases in density (5), It is now reason-
• ; ' ' • ably well adapted to toxicant and has evolved a different capacity
at (3) than it had at (1).
93
-------
LOW
ENERGY
INPUT
HIGH
ENERGY
INPUT
en
O
CD
•O
UJ
IT
X
g
O
2
UJ
O
O
I—
2
O
|
O
IT
sn
UJ
u.
PREY BIOMASS
CD _ (D
) (D
©_(D
LIFE HISTORY ADAPTATION TO OE, TOX
94
-------
and steady-state competitor biomass increases as the biomass of the predator
is reduced by exploitation.
The presence of a toxic substance can have diverse and complex effects
on community structure and organization, some of these possible effects being
illustrated in Figure 28. If a toxicant directly affected the prey or
affected lower trophic levels leading to the prey, the relationship between
predator and prey defined by the prey isocline would be shifted to the left
at each energy input, reducing predator and prey biomass at each exploitation
rate. Inhibition by toxicants of the activities of decomposers may lead to
reduction in rate of regeneration of plant nutrients (N) and will likely alter
the position of prey isoclines. Such leftward shifts in prey isoclines, may
jeopardize predator persistence at higher exploitation rates and lower energy
input rates.
A toxicant directly affecting predator survival, growth, or reproduction
can shift the predator isocline downward at each exploitation rate, bringing
about reduction in predator biomass. Such an effect on predator relative
growth rate is shown in Figure 28B. As a result of the downward shift in
predator isoclines, heavily exploited predator populations in systems with
low rates of energy input may be the most vulnerable to extinction as a result
of exposure to toxicants.
In the laboratory ecosystems, dieldrin directly influenced only the
guppy populations, in effect lowering the predator isoclines at each
exploitation rate and thus bringing about reduction in the biooasses of
populations exploited at 0.10, and 20 percent and apparently causing ex-
tinction of the population exploited at 40 percent (Figure 12). Since an
increase in input rate of energy and materials shifts the prey isocline(s)
to the right, populations exploited at 40 percent at the high level of
95
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habitat and availability and energy input nay be capable of persisting
when exposed to 1 ppb of dieldrin. The effect of increased energy input
.rate on the response of the laboratory.communities to dieldrin is presently
being evaluated,
Toxicant effects on populations, including extinction, are not a simple
consequence only of conditions in the environment of the community such as
exploitation and energy input, but are determined also by the organization
'of the community. The presence of competitors of guppies for the organic
sediment food resource (snails, amphipods) in effect, shifted prey isoclines
to the left at each energy inpuc rate and by so doing may have facilitated
guppy population extinction. This is to say that had competitors of the
guppy not been present, they may have been able to persist at higher
exploitation rates in the presence of dieldrin.
Changes in population abundance can be operationally accounted.for in
terns of rates of gain and loss of population biomass and how these rates
are affected by environmental conditions. Population production and yield
are rate terms that have been of special interest to biologists. Each
particular production and yield -value is- a consequence of the population's
capacity for production and yield and conditions in the population's
environment, in a way that changing environmental conditions bring about
changes in the production and yield of a population with a given capacity.
Communities provide the environaental context for populations. Thus,
the organization of the community of which a population is a part as well
as factors such as energy input rate and exploitation rate fundamentally
influence the abundance, production, 2nd yield of a population of interest.
Ivlev (1945) recognized the importance of ecosystem organization in deter-
mining population production. He distinguished production on the particular
96
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density-dependent rate of tissue elaboration of a population of interest
from the productivity of an ecosystem, on its ability to support population
production. This view of ecosystem productivity has been exteided and has
proven useful in explanation and understanding of salmonid production in
laboratory streams and how it is affected by various pollutants (Brocksen,
Davis, and Warren, 1968, 1970; Warren, 1971). Using isocline theory, Booty
(1976) formalized productivity theory. Liss (1977) articulated fisheries
exploitation theory with productivity theory by dealing with the ability of
ecosystems to support population recruitment and yield as well as production.
Pxed?.tor production and yield bear dome-shaped relationships to predator
population biomass. Predator production can be computed as the product of
predator relative growth rate and predator biomass. Each steady-state
predator production curve is derived from a prey isocline defining a density-
dependent relationship between steady-state predator and prey biomass, and
from a relationship between steady-state predator relative grouch rate and
prey biomass as shown in Figure 28. Each production curve is taken to define
a level cf ecosystem productivity, including all production values associated
with different biomasses along it. Each yield curve is also cerived from a
particular prey isocline (Liss, 1977).
Any change in the position or form of either the relationship between
steady-state predator and prey biomass defined by a prey isocline or in the
relationship between predator growth rate and prey biomass will lead to a
change in the magnitude and form of the steady-state production and yield
curves, this defining a change in system productivity.
Increased ecosystem productivity can result from increased rate of
energy input, which shifts the prey isocline to right on the phase.plane
and increases the magnitude of the production and yield curves. Changes
97
-------
in exploitation rate, however, alter neither the position of the prey iso-
clines or the predator growth rate relationship and thus do not constitute
changes in productivity, according to the isocline system. Increased
exploitation rate results in decreased predator biomsss and increased prey
biomass, shifting the steady-state point downward along a particular prey
isocline and to the left, toward the origin, on the curves of production
and yield.
In the laboratory ecosystems, increased habitat availability and energy
input shifted the relationships between -guppy biomass and the biomass of
their prey to right on phase planes (Figures 9,10,11) and increased the
magnitude of guppy production and yield curves (Figure 14). Changes in
guppy exploitation rate did not appear to alter the magnitude of the curves,
but rather shifted guppy biomass along each of the curves.
The presence of competitors of the predator or competition on lower
trophic levels leading to the predator shift the prey isoclines to the
left and thus lead to decreases in system productivity and reductions in
the magnitude of predator production and yield. Reduction rate of re-
generation of plant nutrients has a similar effect. Exploitation of the
predator population can alter system productivity by removing material.*
from the system that would otherwise have decomposed to plant nutrients.
The presence of additional prey, so long as they are not competitors, can
increase system productivity by effectively increasing predator growth rate
relationships (Liss, 1977).
Toxic substances can alter the. productivity of an ecosystem for a popu-
lation of interest by causing shifts in the position of the prey isoclines
or by altering the predator growth rate-prey relationship (Figure 28). If a
toxicant adversely affected the prey or lower trophic levels leading to the
98
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prey (plants, etc.), the p-.ey isocline could be shifted to the left on the
phase plane and the magnitudes of predator production and yield could be
reduced. A toxicant could, however, increase predator .;ibundance and increase
the ability of the system to support predator production and yield if it
selectively reduced the abundance of the competitor, this effectively shift-
ing prey isoclines to the right on the phase plane,
A toxicant directly altering the relationship between predator growth
rate and prey biooass can result in reduction jn system productivity and
decrease in the magnitude of predator production and yield curves (Figure 28C)
In the laboratory ecosystems this appears to be the mechanism by which guppy
production and yield curves were lowered. Dieldrin directly affected guppy
populations, apparently by reducing not only guppy relative growth rate (in
effect the relationship between growth rate and prey bioirass) but also guppy
reproduction and survival. Evaluation in separate aquarii m experiments of
the effects of dieldrin on prey and competitors of guppies indicated that
these organisms would probably not be affected by 1 ppb of dieldrin intro-
i
ouced into the laboratory ecosystems. Thus, any changes in their abundance
probably resulted from changer, in guppy population biomass induced by dieldrin.
Populations come to havu their capacities to persist and their capacities
for production and yield through incorporation of the life history capacities
of their individuals. But how are the life history capacities of individual
organisms related to popv.lation density and community structure? Many kinds
of toxicity tests are intended to evaluate toxicant effects on aspects of in-
dividual organism life histories, including survival, growth, and reproduction.
Undertanding the relevance of results of these tests must be based upon some
understanding of the relationhip between life histories and community structure
Individual organisms have capacities to alter their life history patterns
99
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in response to changes in their environments and in ways favoring the
persistence o£ their populations under thsse conditions. Through such
developmental as well as evolutionary alterations in life history patterns,
individuals and their populations maintain concordance with their environ-
mental systems. The community provides the environmental context in which
individuals develop and populations must be adapted to persist. Different
community structures ~ different kinds and densities of prey, predators,
and competitors -- constitute different developmental environments forindi-
viduals and different evolutionary environments for populations. Changes
in community structure bring about changes in the kinds of individual organ-
ism life history capacities composing populations and changes in individual
organism life history patterns. Thus, different life history patterns can
be associated with different community structures.
In the laboratory ecosystems, changes in conditions in the environment
of the community such as exploitation rate, habitat availability and energy
input, and exposure to toxic substances alter steady-state community structure.
Different steady-state guppy life history patterns existed at different
community structures. This may be best illustrated by referring to the
generalized model shown in Figure 28. At each level of energy input, increases
in exploitaton rate result in reduction in steady-state predator biomass and
increases in steady-state prey biomass. Steady-state predator life history
patterns that may exist at lower and higher exploitaton rates are summarirsd
in Table 4.
As exploitation rate and, thus, mortality due to fishing increase, we
might expect reduction in length of life and number of clutches produced in
an individual's lifetime. But due to reduction in predator biomass and
increase in the biomass of their food resource, we might also expect faster
100
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Table 4. Some possible predator life history patterns at low and high
exploitation rates (After Kulbicki, 1979).
Life History Traits
Low Exploitation Rate High Exploitation Rate
Longevity
long lifespan
low adult mortality
shorter lifespan due to
very high mortality
resulting from
exploitation.
Number of
clutches in a
lifetime '
many due to
long lifespan
fewer due to the high
mortality and shorter
lifespan
Growth Rate
low due to low food
availability and
high population
density
high due to high food
availability and low
population density
Age at first
reproduction
later due to low
food availability
and low adult
mortality
earlier due to high food
availability and/or
higher mortality
Size at first
reproduction
smaller due to
slower growth
larger size at first
reproduction
Clutch size
low food availability
will result in small
clutches
larger clutches because
of high food availa-
bility and better growth
101
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juvenile and adult growth (Figure 16), increased si:e at first reproduction
(or perhaps decreased age at first reproduction), and increase;! fecundity
(Figures 17 and 19). Thus, when guppy populations are exploited at high
rates, they may develop life history patterns normally associated with higher
values of the intrinsic rate of increase - acre rapid growth, earlier
maturity or larger size at naturity, and higher fedundity at iirst and at
subsequent reproductions. Such life history characteristics can be under-
stood as adaptations to environments that bring about shortening of life-
span and reduction in number of clutches in a lifetime. That populations
come to be composed of individuals that have life history capacities to
exhibit these kinds of life history characteristics enables the populations
to persist at high exploitation rates. Populations whose organisms car.nct
manifest those kinds of characteristics may not be able to persist at high
levels of exploitation.
These kinds of changes in life history pattern in response to exploitation
are familiar to fishery biologists. They have been observed in the laboratory
ecosystems and in other exploited guppy populations (Liss, 1974),.in clupeids
(Burd and Gushing, 1962; Beverton, 1963), in trout and perch (Ala, 1959), and
in whitefish (Miller, 19S6). This suggests that these kinds of changes in
life history patterns may be important, but they are not the only ways that
populations adapt to high exploitation rates.
crtfeT/isbS)
Murphy &!£&& believed that sardine populations adapted with long life and
^
many reproductions to life in highly variable oceanic environments where
probability of successful reproduction in any one year is very low. Heavy
exploitation of the California sardine reduced sardine life span and thus the
number of possible tines a sardine could reproduce in its lifetime, essentially
stripping away the mechanisa that had adapted the sardine to life in highly
102
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variable environments. Severe reductions in the sardine population took place
and a nost valuable fishery collapsed.
Toxic substances can have similar kinds of effects on adaptive capacities,
altering life history patterns so that populations are no longer able to persist
or may persist at reduced densities under .given sets of environmental conditions.
In the laboratory ecosystem, dieldrin apparently altered guppy life history
patterns by reducing growth and fecundity and, at 40 percent exploitation, by
increasing mortality of offspring. At the 40 percent exploitation rate, dieldrin
may have caused extinction of the population by effectively preventing the
individuals from exhibiting the life history patterns — more rapid growth,
higher fecundity, increased offspring survival — that adapted the population
to persist at this very high exploitation rate. These changes in life history
pattern effectively lower the predator isocline at 40 E, as shown in Figure 28,
until it does not intersect the prey isocline.
Such heavily exploited populations, where rapid growth, high fecundity,
and good juvenile survival are essential for persistence, may be more "sensit-.ve"
to reductions in growth,fecundity, and survival caused by toxic substances. At
lower exploitation rates, alterations in life history pattern caused by dieldrin
resulted in reductions in guppy population density, but the populations were able
to persist. But surely higher concentrations of toxicant, which would bring about
more severe alterations in life history patterns — greater reductions in growth,
fecundity, and survival — would cause extinction of populations exploited at lower
rates.
Now, at the higher rates of energy input, because of the greater availability
of food, a population may be able to persist when exposed to a toxicant and
exploited at 40E, as shown i*i Figure 28. The range of exploitation rates over
which populations can persist when exposed to a given level of toxicant nay be
103
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greater at high energy input rates than at low rates. But there will surely be
some exploitation rate higher than 40E at which the population at a high energy
input rate will not be able to persist.
Exploitation and exposure to toxicants alter adaptive capacities of popu-
lations by bringing about evolutionary changes in the kinds of individual organisn
life history capacities composing the populations. The gupp/ population,
exploited at 0 percent in the laboratory ecosystems, probably underwent evolu-
tionary changes in becoming more "resistant" to dieldrin and recovering from
perturbation. '
Evolutionary alteration in adaptive capacity can be illustrated with graphs
resembling Levin's (1968) fitness sets. Each point in Figure 29 represents the
life history capacity of an individual organism. Its position indicates how well
the life history pattern exhibited by the individual under each set of environ-
mental conditions is adapted to those conditions. The set of all individual
organisa life history capacities defines the steady-state adaptive capacity
of the population at OE, Mo Toxicant (1) OE, Toxicant (2); OE, Toxicant
After Recovery (5). Exposure to toxicants altered adaptive capacity, with
the composition of the population shifting from one in which most individuals
were poorly adapted to OE, Toxicant (l~) to one in which aost individuals are
well-adapted to these conditions (5). Thus-, even though the population while
being exposed to the toxicant, has returned to the density it maintained prior
to toxicant introduction, it has a very different capacity. It has adapted
evolutionarily to the toxicant. But, in adapting to the toxicant, the popu-
lation may have lost its adaptive capacity for other environmental conditions.
In the laboratory ecosystems, populations exploited at 10 and 20 percent
did not recover from toxicant perturbation throughout the "ias that dieldrin
was being introduced. The unexploited population maintained a greater density
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than the populations exploited at 10 and 20 percent. Perhaps greater
population density increased the probability that "resistant" individuals were
present in the population and so speeded evolutionary adaptation and recovery
from perturbation.
Populations adapt to changes in conditions in their environment through
life history and evolutionary adaptation. Toxic substances can alter individual
organism life history patterns and the adaptive capacities of populations and
thus bring about changes in population densities and community structure. Many
kinds of toxicity tests are intended to provide evaluation of hazards of toxic
substances based upon their effects on aspects of individual organism life
*
histories. But in order to be useful in this regard, toxicant effects observed
in simple toxicity tests must bear some relation to possible effects the toxi-
cant may have upon life histories, populations, and communities in natural
ecosystems.
Aquarium experiments intended to evaluate the effects of dieldrin on guppy
life history patterns were conducted in conjunction with the laboratory eco-
system studies. This provided the opportunity for examining some of the possible
relationships between effects observed on life history patterns in experiments
more like simple toxicity tests with effects on life history patterns, popu-
lations, and communities observed in the laboratory ecosystems. Understanding
the relevance of test results on life history patterns must be based at least
in part upon an understanding of the relationship between life history pattern
and community structure.
We have shown how different guppy steady-state life history patterns can
be associated with different steady-state comunity structures -ji both the
laboratory ecsystems ard with the generalized isocline model (Figure 30,
Table 4). In particular, changes in exploitation rate brought about changes
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in steady-state life history pattern, population density, and community
structure. Increased exploitation rate resulted in reduction "in population
density and density-dependent increases in size-specific growth and repro-
duction occasioned by increased food availability. Steady-state age- and
size-specific patterns of growth and reproduction at low and at high
exploitation rates (Table 3, Figures 15-19) are broadly similar to guppy
life history patterns observed at LR and at HR, respectively (Figures 23-27).
Thus, different food rations in aquarium experiments generated life history
patterns similar to those at different exploitation rates (with the exception,
of course, that exploitation reduced lifespan and number of clutches).
Using isocline and other ecological theory, perhaps such meaning and.
relevance can be "written onto" life history patterns observed in individual
organism experiments. That is, the theory gives the results of these
experiments meaning. In the broadest sense, perhaps life history patterns
observed in these simple experiments can be thought of_ as steady-state life
history patterns that would exist at some steady-state community structure
generated by some fixed set of community environmental conditions.
This provides at least some rationale for evaluating toxicant effects
on life history pattsrns under different sets of important environmental
conditions, for the life history patterns that develop under these conditions
may be taken to represent those that would develop at different community
structures. One important environmental factor is food availability.
Determination of life history patterns at different levels of food availa-
bility may at least begin to be representative of life history patterns that
would develop if changes in community environmental conditions or community
organization altered prey densities. These might include changes in
exploitation rate (or mortality rate), changes in energy input at a given
106
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exploitation rate, or introduction of a competitor (Figure 30). It is important
to realize, however, that other factors as well as alteration in prey density
mould life history patterns.
In the aquarium experiments, dieidrin reduced newborn survival (Figure 25),
juvenile and parental growth (Figures 23 and 24), and clutch size (Table 3,
Figure .26). . As far as we were able to ascertain, these same kinds of effects
on guppy life history patterns occurred in the laboratory ecosystems. (Figures
16 and 19). But effects on population abundance and persistence resulting from
exposure to dieidrin ranged from perturbation and recovery at zero exploitation
rate to extinction at 40 percent exploitation rate. It is far less easy to see
how such a diversity of effects could have been anticipated from the individual
organism experiments. However, it is possible that with appropriate theory, such
effects may have become more apparent. Perhaps the point here is that interpre-
tation of individual organism experiments, if they can be given meaning at all,
is not a simple matter of direct extrapolation to complex systems, but:entails
the use of theory as a ''vehicle" for extrapolation, and it is in the context
of such theory that results of relatively sLnple tests on individual organisms
may find meaning.
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REFERENCES . "
1. American Public Health Association. 1971. Standard Methods for the
Examination of Water and Wastewater. 13TH EDITION. APHA,
Washington, D.C., p. 734-745. '. . ,
2. Aim, G. 1959. Connection between maturity, size, and age in fishes.
Experiments carried out at the Kalarne.Fishery Research Station.
Ann. Rap. Inst. Freshwater Res. Drotinghalm. 40:5-145.
3. Berg, M.G. and E.H. Gardner. 1978. Methods of soil anzlysis used
in the soil testing laboratory at Oregon State University. Special
Report 321, Agricultural Experiment Station, Corvallis.
4. Beverton, R.J.H. 1963. Maturation, growth, and mortality of Clupeid
and Engraulid stocks in relation to fishing. Rapp. Proces Verbaux
Reun. Cons* Perm. Intern. Explor. Her. 154:44-67.
5. Birch, L.C. 1948. The intrinsic rate of natural increase of an insect
population. J. Anim. Ecol. 17:15-26.
6. Booty, W.M. '1976. A theory of resource utilization.' MS Thesis*
Oregon State University, Corvallis.
7. Brocksen, R.L., G.E. Davis, and C.E. Warren. 1968. Conpetition,
food consumption, and production of sculpins 'and trout in laboratory
stream communities. J. Wildl. Manage. 32:51-75.
8. Burd, A.C. and D.H. Gushing. 1962. Studies on the Dunmore herring
stock. I. A population assessment. J. Cons. Intern. Explor. Mer.
29:277-301.
9. Chadwick, G.G., J.R. Palensky, and 3.L. Shumway. 1972. r.ontinuous-
flow dilution apparatus for toxicity studies. Proc. of 39th Pacific
NW Industrial Waste Management Conference, p. 101-105. Portland,
Oregon.
10. Chapman, D.W. 1968. Production in fish populations. In S.O. Gerking
(ed.). The Biological Basis of Freshwater Fish Production, p. 5-29.
Blaekwell Scientific Publications. Oxford.
11. Connell, J.H. 1975. Some mechanisms producing structure in natural
ccssaunities: a model and evidence from field experiments. In M.L. Cody
and J.M. Diamond (eds.), Ecology and Evolution of Cocaunities, p. 460-
490. Harvard University Press, Cambridge.
12. Connell, J.H. and E. Orias. 1964. The ecological regulation of
species diversity. Am. Nat. 98:399-414.
108
-------
15. Diamond, J.M. 1975. Assembly of species communities. In M.L. Cody
and J.M. Diamond (eds.), Ecology and Evolution of Communities,
p. 342-444. Harvard University Press, Cambridge.
14. Finger, S.E. 1980. Effects of perturbation on community structure
and organization of aquatic microcosms. MS Thesis, Oregon State
University, Corvallis.
15. Moiling, C.S. 1973. Resilience and stability of ecological systems.
Ann. Rev. Ecol. Syst. 4:1-23.
16. Holling, C.S. (editor). 1978. Adaptive Environmental Assessment and
Management. Intern. Series on Applied Syst. Analysis Vol. 5. John Wiley
and Sons, New York.
17. Ivlev, V.S. 194S. Biologicheskaya produktivnost vodoemov. Uspekhi
Sovremennoi Biologii 19:98-120. (Translated by W.E. Ricker, 1966.
Tie biological productivity of waters. J. Fish. Res. Bd. Can. 25:
1727-1759).
18. Kulbicki, M.L. 1980. The effects of dieldrin and different food
levels on life history tactics of the guppy (Poecilia reticulata
Peters). MS Thesis, Oregon State University, Corvallis.
19. Levins, R. 1968. Evolution in Changing Environment^. Princeton
University Press, Princeton.
20. Liss, W.J. 1974. Dynamics cZ exploited guppy populations exposed
to dieldrin. MS Thesis, Oregon State University, Corvallis.
21. Liss, W.J. 1977. Toward a general theory of exploitation of fish
populations. Ph.D. Thesis, Oregon State University, Corvallis.
22. Liss, W.J. and C.E. Warren. In Press. Ecology of Aquatic Systems.
In R-L. Lackey and L. Nielsen (eds.), Fisheries Management, p. 41-80.
Blackwell Scientific Publications, Oxford.
23. Lotka, A.J. 1925. Elements of Physical Biology. Williams and
Wilkins, Baltimore.
24. MacArthur. R.L. 1972. Geographical Ecology. Harper and Row, New
York.
25. Menge, B.A. 1976. Organization of the New England rocky intertidal
community: roles of predation, competition, and environmental
heterogeneity. Ecol. Monogr. 46:355-393.
26. Menge, B.A. and J.P. Sutherland. 1976. Species diversity gradients:
synthesis of the roles of predation, competition, and temporal
heterogeneity. Am. Nat. 110:351-369.
109
-------
27. Miller, R.B. 1956. The collapse and recovery of a snail whitefish
fishery. J. Fish. Res. Bd. Can. 13:133-146.
28. >tophy, G-I. ,1967. Vital statistics of the Pacific sardine CSardinops
caerulea) and the population consequences. Ecology 43:721-736.
29. Marphy, G.I. 1968. Pattern in life history and the environment.
. . .An. Nat. 102:391-403.
30. Paine, R.T. 1966. Food web complexity and species diversity. An.
.Nat. 100:63-75. "
31. Pianka, E.R. 1966. Latitudinal gradients in species diversity: a
review of concepts. Am. Nat. 100:33-46.
32. Sanders, H.L. 1969. Benthic marine.diversity and the stability-
time hypothesis. Brookhaven Symp. in Biol. 22:71-81.
33.' Sinnhuber, R.O., J.H. Hendricks, J.H. Wiles, and G.3. Putnam. 1977.
Neoplasm in rainbow trout, a sensitive animal model for environmental
carcinogenesis. Ann. N.Y. Acad. Sci. 298-389.
34. Warren, C.E. 1971. Biology and Water Pollution Control.
W.3. Saisders, Philadelphia.
33. Warren, C.E., M.W. Allen, and J.W. Haeiher. 1979. Conceptual
frameworks and the philosophical foundations of general living
systems theory. Behavioral Sci. 24:296-310.
36. Warrsn, C.E. and W.J. Liss. 1977. Design and evaluation of
laboratory ecological system studies, ecological Research Series,
USEPA, EPA-600/3-77-022.
37. Warren, C.E. and W.J. Liss. In Press. Adaptation to aouatic
environments. In R.L. Lackey and L. Nielsen (eds.), Fisheries
Management, p. 15-40. Blackwell Scientific Publications, Oxford.
58. Weltering, D.M. 1981. Organization and adaptation of aquatic
laboratory ecosystems to the resource availability, exploitation,
and a toxicant. Ph.D. Thesis, Oregon State University, Corvallis.
110
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