May 1999 STRESS IN ECOLOGICAL SYSTEMS 431

Ecological Applications, 9(2), 1999, pp. 431– 440

q 1999 by the Ecological Society of America

STUDYING STRESS: THE IMPORTANCE OF

ORGANISM-LEVEL RESPONSES
LORRAINE MALTBY1
Department of Animal and Plant Sciences, The University of Sheffield, Sheffield, S10 2TN UK

Abstract. The importance of studying the effects of stress on individual organisms is

addressed by considering the use of individual-level information to: (1) elucidate the mech-
anistic bases of interpopulation variation; (2) predict population-level effects; and (3) mon-
itor stress in natural communities. Examples discussed include interpopulation variation in
the sensitivity of freshwater shrimps to zinc stress; the use of individual-based models to
predict the effects of copper stress on earthworm populations; the use of single-species in
situ assays to monitor pollution. It is contended that knowledge of organism-level responses
is essential for understanding how stressors cause adverse biological effects and the strat-
egies adopted by organisms to tolerate stress. It is also contended that the effects of stressors
on populations can be predicted from a knowledge of the effects of stressors on individual
energy budgets. Organism-level responses can be used to monitor stress in natural envi-
ronments. In situ assays, based on the physiological energetics of ecologically relevant
species, can provide sensitive and general stress indicators that are correlated with com-
munity-level responses.
Key words: bioassays; energy budgets; Gammarus feeding rate; interpopulation variation, mech-
anistic basis; physiological models, individual-based; population-level effects; stress monitoring using
bioassays; stress responses, individual and community level; zinc tolerance.

INTRODUCTION stress responses in individuals is used to predict or

Ecotoxicologists study the fate and effects of toxi-
cants in ecosystems with the aim of understanding how
toxicants affect the structure and functioning of pop-
ulations, communities, and ecosystems. Although the
ultimate level of concern may be populations, com-
munities, or ecosystems, chemicals affect individual
organisms, and the consequences of stress may be man-
ifested at all levels of biological organization. There
is not a ‘‘right’’ level at which to study stress. Rather,
different levels of organization provide information
that, in combination, give insight into the effects of
stress, their mechanistic bases, and their ecological and
evolutionary consequences. Studies of populations and
communities can provide a description of the effects
of stress but do not, in themselves, provide information
on how effects are caused. Conversely, studies at the
molecular and cellular level can provide detailed in-
formation on how chemicals interact with target sites
but provide little or no information on the conse-
quences of these effects for higher levels of organi-
zation. What is required is an integrated approach in
which an understanding of the mechanistic bases of
Manuscript received 20 October 1997; accepted 7 July
1998. For reprints of this Invited Feature, see footnote 1,
page 429.
1 E-mail: L.maltby@sheffield.ac.uk
431
interpret their ecological consequences.
Here I will consider how understanding the physi-
ological responses of individuals to stress can (1) pro-
vide insight into the development of stress tolerance,
and (2) be used to predict population-level effects.
Knowledge of the mechanistic bases of stress tolerance
is essential in order to understand why species differ
in their susceptibility to stressors and how populations
can persist in contaminated environments. Moreover,
it is necessary to translate effects on individuals to
effects on populations in order to evaluate the ecolog-
ical consequences of stress. Physiologically based in-
dividual models combined with structured population
models provide a means of predicting population-level
effects from information on individual organisms. Fi-
nally, the application of individual-level physiological
responses to the study of stress effects on natural eco-
systems will be discussed.
MECHANISTIC BASES FOR STRESS TOLERANCE
Numerous studies have demonstrated interpopula-
tion variation in stress response; organisms from con-
taminated populations are less sensitive than those from
uncontaminated populations (e.g., Klerks and Weis
1987, Posthuma and Van Straalen 1993). Individuals
from contaminated sites may be an order of magnitude
less sensitive than individuals of the same species from
uncontaminated sites (Table 1). In order to elucidate
 Ecological Applications
432 INVITED FEATURE Vol. 9, No. 2

TABLE 1. Sensitivity of invertebrates to chemical stress.

Relative
Species Stressor Response sensitivity Reference
Polychaeta
Nephthys hombergi copper survival 4.3 Bryan 1976
Nereis diversicolor copper survival 2.8 Bryan 1976
Oligochaeta
Limnodrilus hoffmeisteri cadmium survival 4 Klerks and Levinton 1989
Crustacea
Asellus aquaticus lead survival 2.7 Fraser et al. 1978
zinc survival 1.5 Naylor et al. 1990
Asellus meridianus lead survival 4 Brown 1976
growth 7.3 Brown 1976
copper survival 2.1 Brown 1976
growth 3.6 Brown 1976
Corophium volutator copper survival 1.6 Bryan 1976
Gammarus pulex zinc survival 5 Roberts 1996
cadmium survival 7 Roberts 1996
Hyalella azteca low pH survival 2.8–12 France and Stokes
1987
Porcellio scaber cadmium growth 6 Donker and Bogert
1991
Mollusca
Onychiurus armatus zinc/cadmium growth 2 Tranvik et al. 1993
reproduction 2 Tranvik et al. 1993
Orchesella cincta cadmium growth 1.3 Posthuma 1990
Scrobicularia plana copper survival 2 Bryan 1976
Insecta
Lucilia cuprina diflubenzuron survival 10 Kotze et al. 1997
Notes: For each species, the average response of individuals from a contaminated site is presented relative to the average
response of individuals from a reference site. Values of relative sensitivity .1 indicate that animals from the contaminated
population are less sensitive to the stressor than those from the reference population.

the mechanisms resulting in differences in sensitivity,
it is necessary to focus on the stress responses of in-
dividuals. On exposure, chemicals enter individuals
and may accumulate in body tissues. Interactions be-
tween accumulated chemical and target molecules
cause damage that may eventually result in disease,
malfunction, and death. An accumulated chemical may
induce defense mechanisms that reduce its effect on
target tissues, and damage may be repaired, thus re-
ducing the severity of the response.
There are several mechanisms by which the suscepti-
bility of individuals to toxicants may be reduced. The
effects of toxicant exposure may be reduced by decreased
uptake or increased depuration, enhanced detoxification
and sequestration processes, reduced target-site suscep-
tibility, or improved repair processes (Brattsten et al.
1986, Posthuma and Van Straalen 1993, McKenzie and
Batterham 1994). For example, metal-tolerant poly-
chaetes, Nereis diversicolor, were less permeable and
hence absorbed less water-borne metal than nontolerant
polychaetes (Bryan and Hummerstone 1973). Increased
excretion resulted in increased metal tolerance in the
midge Chironomus riparius and the springtail Orchesella
cincta (Van Straalen et al. 1987). Increased detoxification
has been reported for the metal-tolerant oligochaete Lim-
nodrilus hoffmeisteri (Klerks and Levington 1989) and
the polychaetes Nereis diversicolor and Nephthys hom-
bergi (Klerks and Weis 1987). Enhanced monooxygenase
activity was correlated with diflubenzuron tolerance in
the Australian sheep blowfly Lucilia cuprina (Kotze et
al. 1997) whereas organophosphate resistance in mos-
quitoes (Culex pipiens) was due to elevated esterase B
production caused by gene amplification (Mouchès et al.
1986, Raymond et al. 1989). Increased storage capacity
occurs in metal-tolerant midges Chironomus riparius
(Postma et al. 1996), and an example of reduced target-
site sensitivity is provided by the leafhopper Nephotettix
cincticeps. Strains of this species have acetylcholinester-
ase that is insensitive to certain carbamate and organo-
phosphate insecticides (Brattsten et al. 1986). Resistance
to cyclodien insecticides (e.g., dieldrin) provides another
example of target site modification. A point mutation,
resulting in the substitution of serine for analine in a
Drosophila GABA receptor, reduces binding by cyclodien
insecticides and confers resistance (ffrench-Constant et
al. 1993).
Studies of metal tolerance have focused on uptake,
excretion, detoxification, and sequestration. Population
variation in response to metals may, however, be due
to other factors. Metal-tolerant Gammarus pulex, for
 May 1999 STRESS IN ECOLOGICAL SYSTEMS
example, did not accumulate less metal than reference-
site individuals and there was no evidence that indi-
viduals from the two populations differed in metal de-
toxification (i.e., metal-binding proteins) or sequestra-
tion (i.e., storage in hepatopancreas) processes. Despite
the lack of interpopulation variation in metal accu-
mulation and handling, individuals from the contami-
nated site were five times less susceptible to zinc and
seven times less susceptible to cadmium (Roberts
1996). What is the mechanistic basis for this marked
difference in metal sensitivity? Gills are a major site
of aqueous metal uptake in crustaceans and are sen-
sitive to metal-induced damage (e.g., Bubel, 1976,
Couch 1977, Lawson et al. 1995) which may result in
respiratory and osmoregulatory impairment (Spicer
and Weber 1991, 1992, Nonnotte et al. 1993). Inter-
population differences in the effect of metal exposure
on osmoregulation and susceptibility to respiratory im-
pairment were observed with Gammarus pulex. Os-
moregulation of individuals from the metal-contami-
nated population was less sensitive to metal exposure
than that of individuals from the reference population
(Spicer et al. 1998). Moreover, individuals from the
metal-contaminated population were less sensitive to
hypoxia and consequently less susceptible to metal-
induced respiratory impairment (Roberts 1996). As os-
moregulation was relatively insensitive to zinc expo-
sure, it was concluded that the observed interpopula-
tion difference in metal sensitivity was linked to dif-
ferences in respiratory physiology. It appears that
reduced susceptibility to metal stress was a result of
physiological adaptation rather than variation in ac-
cumulation or defense mechanisms.
If studies of stress focused only on populations and
communities, we would observe that organisms could
persist in contaminated habitats but would not know
why. Only by studying the effects of stress on indi-
viduals can we understand how organisms cope with
stress and elucidate the mechanistic bases of stress tol-
erance.
PREDICTING POPULATION-LEVEL EFFECTS
One of the major challenges facing ecotoxicologists
is evaluating the ecological relevance of individual-
level effects. Does it matter that the behavior, physi-
ology, or survival of individuals is impaired? What are
the consequences to the population if 50% of individ-
uals are killed by a toxicant? These are difficult ques-
tions to address without a detailed understanding of:
(1) the individual and population-level consequences
of suborganism effects; (2) the processes regulating
population size, and (3) the minimum viable population
size. The first point can be addressed by understanding
the mechanisms by which changes in the performance
of individuals may impact the population to which they
belong.
As stated above, individuals may respond to a stres-
433
sor by inducing defense and repair processes. The pro-
duction of detoxification enzymes (e.g., mixed-func-
tion oxidases), metal-binding proteins (e.g., metallo-
thionein), heat-shock proteins, and increased protein
turnover all require energy and may consequently result
in increased maintenance costs. Given that resources
available to an individual are finite, increasing main-
tenance costs will mean that fewer resources are avail-
able for growth and reproduction. An example of the
possible trade-off between defense and reproduction is
provided by the work of Krebs and Loeschcke (1994).
Heat-shock genes in Drosophila melanogaster were ac-
tivated by exposing female flies to elevated tempera-
tures for a short period of time. Flies pre-exposed to
elevated temperatures were better able to survive sub-
sequent thermal stress but were less fecund than control
flies. Krebs and Loeschcke (1994) argued that the re-
duction in fecundity resulted from energy allocation to
reproduction being reduced due to increased energy
requirements for heat-shock protein production. More
recently, a negative association between heat-shock
protein concentration and survival in the absence of
stress has been reported (Krebs and Feder 1997), sug-
gesting the presence of a trade-off between thermo-
tolerance and performance.
The amount of energy available for growth and re-
production can be estimated by measuring an organ-
ism’s energy budget and calculating its ‘‘scope for
growth.’’ Scope for growth (SfG) is defined as the dif-
ference between energy absorbed from food and that
lost via excretion and metabolism (Warren and Davis
1967), and is determined by measuring energy ingest-
ed, egested, respired, and excreted. A positive SfG in-
dicates that energy is available for production, while a
negative SfG indicates that reserves must be used to
maintain the individual. Short-term measures of SfG
correlate well with long-term measures of growth and
reproduction (e.g., Bayne et al. 1985, Maltby and Nay-
lor 1990, Maltby 1994). I have already postulated that
exposure to chemical stressors may increase energy
expenditure due to the costs of defense and repair pro-
cesses. However, it is clear from the results of a number
of studies on a variety of species and stressors, that
exposure to toxicants generally results in a decrease in
feeding and hence in energy acquisition (Table 2).
Stress-induced reductions in energy acquisition often
occur at exposures lower than those known to affect
maintenance costs, measured as changes in oxygen up-
take (e.g., Donkin and Widdows 1986, Maltby 1992).
Information on how toxicants affect energy budgets
can be incorporated into physiologically based models
to predict the effects of toxicants on the growth, sur-
vival, and reproduction of individuals (Calow and Sibly
1990). Most work in this area has focused on the fresh-
water cladoceran Daphnia; one of the earliest studies
was performed by Paloheimo et al. (1982). Data from
feeding and assimilation experiments were combined
 Ecological Applications
434 INVITED FEATURE Vol. 9, No. 2

TABLE 2. Studies of stress-induced feeding inhibition in invertebrates.

Species Stressor Reference

Crustacea
Callinectes sapidus cadmium Guerin and Stickle 1995
Daphnia magna cadmium Allen et al. 1995
vanadium Allen et al. 1995
sodium bromide Allen et al. 1995
3,4-dichloroaniline Allen et al. 1995
Gammarus pulex low pH Hargeby and Petersen 1988
ammonia Maltby 1994
3,4-dichloroaniline Maltby et al. 1990a
pentachlorophenol Maltby 1994
Lindane Warwick (1997)
zinc Maltby et al. 1990a
copper Tattersfield 1993
cadmium Stuhlbacher and Maltby 1992
Orchestia gammarellus copper Weeks 1993
zinc Weeks 1993
Oniscus asellus cobalt Drobne and Hopkin 1994
Porcellio scaber cadmium Donker and Bogert 1991
cobalt Drobne and Hopkin 1994
zinc Donker et al. 1996
Mollusca
Mytilus edulis Carbaryl Donkin et al. 1996, 1997
2,4-dichlorophenol Donkin et al. 1996, 1997
Dichlorvos Donkin et al. 1996, 1997
Endrin Donkin et al. 1996, 1997
Flucythrinate Donkin et al. 1996, 1997
Lindane Donkin et al. 1996, 1997
pentachlorophenol Donkin et al. 1996, 1997
Permethrin Donkin et al. 1996, 1997
2,4,5-trichlorophenol Donkin et al. 1996, 1997
TBT, DBT Widdows and Page 1993
Helix aspersa Aminocarb Schuytema et al. 1994
Azinphosmethyl Schuytema et al. 1994
Carbaryl Schuytema et al. 1994
Fenitrothion Schuytema et al. 1994
methyl parathion Schuytema et al. 1994
Paraquat Schuytema et al. 1994
Trichlorfon Schuytema et al. 1994
Brotia hainanensis copper Lai and Lam 1994
low pH Lai and Lam 1994
cadmium Lam 1996
Thais lapillus oil Stickle 1985

with literature values on respiration rate to predict
growth and reproduction. Predicted and observed
growth curves were very similar (Fig. 1a), but the mod-
el underestimated reproduction by as much as 43%
(Fig. 1b). One possible reason for this discrepancy be-
tween predicted and actual reproduction is that energy
budget measurements, including SfG, provide an in-
stantaneous measure of the energy available for pro-
duction and do not take into account production from
energy reserves. Subsequent energy budget models
have incorporated a storage component, although the
precise allocation rules vary between models. In some
models, assimilate enters the blood/reserve compart-
ment from which it is allocated to reproduction or
growth plus maintenance (Kooijman 1986). In others,
assimilate is allocated immediately to reproduction or
to growth (including storage) and maintenance (Gurney
et al. 1990, McCauley et al. 1990).
By combining physiologically based individual mod-
els with demographic population models it is possible,
in principle, to use information based on studies of
individuals to predict population-level responses. Two
types of models have been used to predict population
dynamics from individual responses: those that use av-
erage values and treat all individuals as if they were
the same, and those that predict population dynamics
by specifying the variation in responses of individual
members of that population (Metz et al. 1988, Caswell
1989, DeAngelis and Gross 1992). Whereas the former
is less data intensive and computationally less de-
manding, the latter is more realistic as it incorporates
intrapopulation variation. The data requirements of in-
 May 1999 STRESS IN ECOLOGICAL SYSTEMS
FIG. 1. Predicted (open symbols) and observed (solid
symbols) (a) growth and (b) reproduction of Daphnia pulex
that were fed Chlamydomonas reinhardtii (104 cells/mL) and
maintained at 188C. Predictions are based on an energy budget
model (Paloheimo et al. 1982).
dividual-based models may be reduced by grouping
individuals into distinct age or size classes or devel-
opmental stages (e.g., embryo, juvenile, adult), and de-
veloping an age-, size-, or stage-structured population
model. Kooijman and Metz (1984), for example, used
an age-structured model to predict the dynamics of
chemically stressed Daphnia populations from infor-
mation on the effect of toxicants on individual energy
budgets. This energy budget approach has since been
developed and applied to a range of organisms (Kooij-
man 1993).
Klok and de Roos (1996) used an individual-based
model (Kooijman and Metz 1984) to predict the effect
of copper-induced changes in feeding and metabolism
on the growth and reproduction of the worm Lumbricus
rubellus. The model assumes that a fixed proportion of
energy is spent on maintenance and growth, the re-
mainder being allocated to reproduction. It also as-
sumes that energy requirements for maintenance have
priority over those for growth. Klok and de Roos (1996)
investigated two different effects of toxic stress on en-
ergy budgets: (1) a decrease in energy assimilated, and
(2) an increase in maintenance costs. The model pre-
435
dicted that, over the concentration range tested (13–
362 mg Cu/kg), reproduction would be reduced by a
toxicant-induced reduction in assimilation, but not by
a toxicant-induced increase in maintenance costs. Both
scenarios resulted in a decrease in individual growth.
Predictions of individual performance were translated
into population-level consequences using a size-struc-
tured matrix model. With both scenarios, populations
exposed to the highest test concentration (i.e., 362 mg/
kg) would become extinct, even though there was no
effect of increased maintenance costs on reproduction.
The reason for the population decline was the severe
reduction in individual growth resulting from either
reduced energy assimilation or increased maintenance
costs. The impairment of growth was such that animals
would not attain reproductive size and therefore be in-
capable of reproducing. Using this approach, Klok and
de Roos (1996) predicted copper concentrations at a
critical level (i.e., population growth rate equals zero)
of between 200 and 300 mg Cu/kg, which corresponded
well to the observed steep decline in the size of field
populations at copper concentrations exceeding 200 mg
Cu/kg (Ma 1988).
Individual-based models have been developed and
tested using carefully controlled laboratory systems.
However, the dynamics of natural populations are de-
termined, not only by the properties of individuals mak-
ing up that population, but also by a variety of biotic
and abiotic factors, the interactions between which may
be altered by the presence of a chemical stressor. For
example, chemical stressors are known to alter pred-
ator–prey and competitive interactions (e.g., Clements
et al. 1989, Ferrando et al. 1993), which may confound
or mask the direct effects of stressors on individuals.
Another limitation of energy budget models is that,
whereas they can provide a prediction of mortality due
to starvation, they do not, in themselves, predict mor-
tality due to the direct effects of toxicants with specific
modes of action. These data have to be derived from
dose-response relationships determined experimental-
ly. Furthermore, assessing the importance of toxicant-
induced mortality to overall population size and struc-
ture is far from straightforward. If a population is under
strong density-dependent control, the loss of 50% of
juveniles due to the presence of a toxicant may have
little effect on overall population dynamics, but would
affect the genetic structure of the population. These
criticisms are not, however, meant to constitute an ar-
gument for abandoning an individual-based approach.
Rather, they are an appreciation that, whereas infor-
mation about the effects of toxicants on individuals
may provide insight into the potential effect of stressors
on populations and the communities to which they be-
long, the actual effects observed will be a function of
a number of interacting factors.

436 INVITED FEATURE
TABLE 3. Use of scope for growth or feeding inhibition to monitor pollution.
Species Pollution
Mollusca
Anadara granosa industrial
Mytilus edulis oil
hydrocarbons, TBT
and organochlorines
industrial
Mytilus hydrocarbons, PCBs,
galloprovincialis pesticides
Crustacea
Gammarus pulex Malathion
Carbofuran
organic enrichment
metals
hydrocarbons
low pH, aluminum
zinc
† SfG 5 scope for growth (see Predicting population-level effects).
APPLICATION: MONITORING STRESS
USING INDIVIDUALS
Measures of community structure have traditionally
been used to monitor the effects of stress on aquatic
ecosystems (Rosenberg and Resh 1993). Diversity in-
dices (Washington 1984) provide good measures of the
community structure but take no account of species
identity. Biotic indices incorporate taxa-specific infor-
mation by weighting taxa according to their sensitivity
to pollution (Metcalfe 1989). Diversity indices detect
changes in the number of species present and their
relative abundance, and biotic indices detect changes
in the number of species or families present in a com-
munity. Multivariate ordination and classification tech-
niques can be used to compare communities, and to
group together sites with similar communities (e.g.,
Gauch, 1982, Clarke and Warwick 1994, Manly 1994).
Many factors, both natural and anthropogenic, influ-
ence the structure of communities. If differences in
community structure are detected, it is not possible to
establish to what extent the changes observed are
caused by the stressor being investigated. Nor is it pos-
sible to establish how the stressor results in changes
in community structure. Species may be reduced in
abundance either because of the direct effects of the
stressor or because of effects on competitors, predators,
or prey (DeAngelis 1996). These questions can only
be addressed by knowing how stressors affect individ-
ual organisms and understanding the consequences of
these effects for the populations and communities to
which the individuals belong.
Community-level stress measures, such as biotic and
diversity indices or multivariate analyses, provide use-
ful and potentially sensitive descriptions of community
structure, but they are insensitive to sublethal levels of
stress (Gray et al. 1990, Dawson-Shepherd et al. 1992).
In contrast, individual-level measures of stress can be
used to detect sublethal effects, and have the added
Ecological Applications
Vol. 9, No. 2
Response† Reference
SfG Din and Ahamdad 1995
SfG Widdows et al. 1995
SfG Widdows et al. 1995
SfG Roddie et al. 1996
SfG Widdows et al. 1996
feeding Crane et al. 1995
feeding Matthiessen et al. 1995
feeding Veerasingham and Crane 1992
feeding Crane and Maltby 1991
feeding Forrow 1995
feeding McCahon et al. 1989
feeding Roddie et al. 1992
advantage of short response times and the potential to
provide information on causal agents. Single-species
in situ assays provide useful tools for studying stress
in terrestrial, marine, and freshwater ecosystems. In
aquatic systems, caged fish have been used to detect
the presence of oestrogenic chemicals (Purdom et al.
1994), mussels have been used to detect pollution from
dump sites, oil terminals, and industrial discharges
(Roddie et al. 1996) and crustaceans have been used
to study the impact of acid pulses (McCahon et al.
1989), pesticides (Matthiessen et al. 1995), and met-
alliferous discharges (Crane and Maltby 1991).
Single-species in situ assays use resident or trans-
planted organisms, and measurement endpoints are
based on lethal or sublethal responses (Crane et al.
1996). Whole-organism endpoints such as death, mor-
phological deformities, and growth, provide general
measures of stress and can be used to detect changes
in environmental quality. Molecular-level responses
may be more toxicant specific and have the potential
to be used as diagnostic tools. For example, inhibition
of acetylcholinesterase has been used as an indicator
of organophosphate and carbamate pesticide exposure,
and inhibition of aminolevulinic acid dehydratase has
been used as a indicator of lead exposure (Peakall
1992).
A key question to be addressed with any single-spe-
cies approach is: Which species should be used? Stan-
dard laboratory species include freshwater cladocerans
(e.g., Daphnia magna), marine copepods (e.g., Acartia
tonsa), marine bivalves (e.g., Crassostrea gigas, My-
tilus edulis), freshwater and marine fish (e.g., Onco-
rhynchus mykiss, Pimephales promelas, Cyprinodon
variegatus), earthworms (e.g., Eisenia foetida), and
birds (e.g., Anas platyrhynchos, Colinus virginianus)
(Calow 1998). These standard species may not, how-
ever, be the best species to use in in situ studies. The
choice of test species should be driven by the precise
 May 1999 STRESS IN ECOLOGICAL SYSTEMS
question being addressed, but, in general, test species
should be sensitive and ecologically relevant. The se-
lection of test species therefore requires some under-
standing of the system to be monitored and the relative
sensitivity of the species present. Community-based
studies could be used to inform this selection process
by identifying sensitive species in relevant habitats and
assemblages.
By selecting ecologically relevant species and end-
points it is possible to use the results of single-species
in situ assays as short-term predictors of more long-
term effects on populations and communities. The am-
phipod Gammarus pulex is an important detritivore in
many freshwater ecosystems and is used in a 6-d in
situ feeding rate assay (Maltby et al. 1990b, Crane and
Maltby 1991). The rate of detritus processing in
streams is dependent upon the feeding rate of detriti-
vores such as Gammarus pulex (Maltby 1996). Several
laboratory and field studies have demonstrated that
Gammarus feeding rate is depressed by exposure to a
variety of chemical stressors (Maltby 1994). Studies in
artificial streams have demonstrated a positive corre-
lation between Gammarus feeding rate, measured in a
6-d assay, and the processing of leaf material by benthic
macroinvertebrates (Tattersfield 1993). More recent
studies have demonstrated a similar relationship be-
tween Gammarus feeding rate and leaf processing in
natural streams (S. Clayton, unpublished data). More-
over, as discussed earlier, toxicant-induced changes in
feeding rate, and consequently SfG, are indicative of
longer term changes in growth and reproduction and
can be used to predict population-level effects. The
feeding rate and SfG of molluscs and crustaceans have
been used to monitor different types of aquatic pol-
lution (Table 3).
CONCLUSIONS
1) Organism-level responses are essential for elu-
cidating the mechanistic bases of interpopulation dif-
ference in stress tolerance. Commonly reported mech-
anisms of reduced susceptibility are: decreased uptake;
increased excretion, detoxification, sequestration, re-
pair; decreased target-site sensitivity. Susceptibility
may also be reduced by adaptation, genetic or phe-
notypic, of physiological processes. Interpopulation
differences in the susceptibility of G. pulex to zinc were
associated with differences in respiratory physiology.
2) Organism-level responses can be used to predict
the effect of stress on populations. Individuals exposed
to stress have reduced energy intake and possibly en-
hance energy expenditure on defense and repair pro-
cesses. Individual-based energy budget models and
structured population models have been used to trans-
late stress-induced changes in energy acquisition and
allocation to population-level effects.
3) Organism-level responses provide a sensitive and
general stress indicator that is correlated with com-
437
munity-level effects. The feeding rate of G. pulex is
inhibited by a variety of stressors and is positively
correlated with leaf processing by benthic communi-
ties. The in situ Gammarus feeding rate assay can be
used to indicate population- and community-level ef-
fects. The use of in situ assays that combine general
stress responses and toxicant-specific molecular re-
sponses can provide ecologically relevant, sensitive,
and diagnostic monitoring tools.
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