v
WATER QUALITY AND STRESS INDICATORS
IN MARINE AND FRESHWATER ECOSYSTEMS:
LINKING LEVELS OF ORGANISATION
(INDIVIDUALS, POPULATIONS, COMMUNITIES)
Edited by
DAVID W. SUTCLIFFE
Published by the Freshwater Biological Association
Invited papers from a joint Associations specialised conference
held at
Napier University, Edinburgh on 6-7 September 1993
by
The Freshwater Biological Association,
The Ferry House, Far Sawrey, Ambleside, Cumbria LA22 OLP, England
and
The Marine Biological Association of the United Kingdom,
The Laboratory, Citadel Hill, Plymouth PL1 2PB, England
and
The Scottish Association for Marine Science,
PO Box 3, Oban, Argyll PA34 4AD, Scotland
© Freshwater Biological Association 1994
ISBN 0-900386-54-1
Stress, shredders and streams: using Gammarus energetics
to assess water quality
L. M A L T B Y
Department of Animal and Plant Sciences, University of Sheffield, Western Bank,
PO Box 601, Sheffield S10 2UQ, UK
This paper reviews the effectiveness of Gammarus scope for growth (SfG) as an indicator of
water quality. In addition, the link between physiological changes and effects at higher levels
of biological organisation is addressed.
Exposure to a range of toxicants resulted in decreases in Gammarus SfG which were
qualitatively and quantitatively correlated with subsequent reductions in growth and
reproduction. Reductions in SfG were due principally to a decrease in energy intake (i.e.
feeding rate) rather than an increase in energy expenditure. Gammarus pulex is an important
shredder in many stream communities and stressed-induced reductions in its feeding activity
were correlated with reductions in the processing of leaf litter by a semi-natural stream
community. Hence, changes in the physiological energetics of Gammarus provide a general
and sensitive indicator of stress which can be linked to effects at higher levels of biological
organisation. Under long-term stress and hence prolonged reductions in SfG, animals may
adapt by modifying their life-history strategies and producing fewer, larger offspring.
Introduction
Changes in water quality may affect all levels of biological organisation, from molecules
through to communities (Fig. 1). There is, therefore, a wide range of response criteria upon
which stress indicators could be based. However, in reality, stress indicators are usually based
on either changes in community structure (e.g. Wright et al. in this volume) or, less frequently,
suborganismic responses, either molecular or physiological (e.g. Widdows 1985; Widdows &
Donkin 1991; and several contributions in this volume). An advantage of measuring
community-level effects is that it is usually the status of the community, or individual species
within it, which forms the focus of concern. However, changes in community structure may
take many months or even years to become apparent and consequently such measures cannot
provide rapid indicators of changes in water quality. In contrast, suborganismic responses may
be manifested within hours or days of exposure and may therefore be useful as early-warning
indicators (Peakall 1992).
If we are to understand how changes in water quality result in altered community structure
or what the implications of changes in the biochemistry or physiology of an organism are for
the population and community to which it belongs, then we must begin to link effects at
different levels of biological organisation in a mechanistic way (Maltby & Calow 1989). This
paper addresses the question of linkage for a stress indicator based on the physiological
energetics of the freshwater amphipod Gammarus pulex (L.). G. pulex is a common constituent
of stream communities and is an important prey item for many fish species (Smyly 1957;
Maitland 1966; Welton 1979). It is a shredder, feeding primarily on detrital material such as
autumn-shed leaves (Willoughby & Sutcliffe 1976; Welton 1979; Willoughby & Earnshaw
1982) and consequently plays a key role in the incorporation of terrestrially-fixed organic
Using Gammarus to assess water quality
99
material into the freshwater food web. Any disruption of this process, either through reduced
shredder abundance or reduced feeding activity, could have considerable implications for the
structure and functioning of the systems as a whole (Maltby 1992a).
The use of physiological energetics as a stress indicator
Stress indicators based on physiological energetics involve the measurement of energy budgets
or their components: ingestion, egestion, excretion, respiration and production (Grodzinski et
al. 1975). Early studies on physiological energetics were performed on fish (e.g. Fry 1947,
1971; Winberg 1960) and, in 1967, Warren & Davis (1967) suggested that the parameter
Figure 1. Flow diagram of effects which may be induced by exposure to a pollutant. (After Sheehan
1984).
100
L. Maltby
"scope for growth" (SfG) may be a useful indicator of stress in fish. They defined scope for
growth as "the difference between the energy of the food an animal consumes and all other
energy utilizations and losses". It is, therefore, a measure of the energy potentially available for
production, either somatic or gametic. Scope for growth may be positive - in which case
energy is available for growth and/or reproduction, negative - indicating that body reserves are
being utilized to fuel maintenance processes, or zero - implying that energy intake matches
energy expenditure.
The rationale for using SfG as an indicator of stress rather than measuring growth or
reproduction directly is that, whereas it may take weeks to detect changes in growth rates or
reproductive output, energy budget parameters can be measured in hours or days. In addition,
as a reduction in SfG may be the result of either a reduction in energy intake or an increase in
energy expenditure, measuring energy budget components may provide insight into possible
toxic mechanisms (Bayne et al. 1985). Other benefits of using this technique to assess water
quality have been discussed by Donkin & Widdows (1986).
Since the early work on fish, SfG has been used to assess the effects of environmental
stressors on a range of marine invertebrates, including bivalve molluscs (Bayne & Newell
1983; Worrell et al. 1983; Martin 1985; MacDonald & Thompson 1986; Foe & Knight 1987),
gastropod molluscs (Stickle et al. 1984), echinoderms (Shirley & Stickle 1982 a,b), cnidarians
(Zamer & Shick 1987) and crustaceans (Edwards 1978; Johns & Pechenik 1980; Capuzzo
1985). However, the most intensely studied organism has been the common mussel, Mytilus
edulis (Bayne et al. 1985; Willows, in this volume). In contrast, with the exception of
Gammarus pulex, few studies have been performed on freshwater invertebrates.
Physiological energetics of Gammarus pulex
Methods for determining the energy budget of Gammarus pulex have been described by
Nilsson (1974) and Naylor et al. (1989), and in both cases microbially conditioned alder leaves
were used as a food source. Leaf material may be conditioned with either an unknown mixture
of fungal species (Nilsson 1974) or standardized by inoculating with a single, known fungal
strain (Naylor et al. 1989). Although conditioned alder leaves provide an ecologically relevant
and nutritional food source, G. pulex will consume a range of other food types, both natural
(Willoughby & Sutcliffe 1976) and artificial (Taylor et al. 1993).
Energy budget components are influenced by a range of intrinsic and extrinsic factors
(Nilsson 1974; Ivleva 1980; Sutcliffe 1984). It is therefore essential to standardize
experimental conditions and animal quality. The Gammarus bioassay described by Naylor et
al. (1989) uses large adult male gammarids obtained from a single population. All laboratory
studies have been conducted at 15°C using a standard food and a defined artificial medium.
Under these conditions, SfG was reduced by exposure to a range of different toxicants,
including organic compounds (e.g. chlorinated ethers, 3,4-dichloroaniline, pentachlorophenol),
heavy metals (e.g. cadmium, chromium, copper, zinc), dissolved gases (e.g. oxygen, ammonia)
and pH (Naylor et al. 1990; Maltby et al. 1990a; Maltby 1992b; Stuhlbacher & Maltby 1992;
Tattersfield 1993). In the majority of cases, a reduction in energy intake was observed before
an increase in energy expenditure (Table 1). The increased sensitivity of energy intake relative
to energy expenditure has been observed for other species and stressors (Widdows 1985), the
exception being substances which either inhibit or uncouple oxidative metabolism (e.g.
pentachlorophenol, alkyltins) (Widdows & Page 1993; Willows, in this volume).
Stress-induced changes in Gammarus feeding rates were strongly correlated with lethal
effects (Fig. 2; r2 = 0.83, d.f. = 6, p<0.05) and, on average, feeding rate was approximately 8
times more sensitive than the LC50 value as a measure of stress (range: 1.5 to 68).
Using Gammarus to assess water quality
101
Table 1. Relative sensitivity of energy intake (feeding) and expenditure (respiration) in Gammarus pulex exposed to
various toxicants.
Values represent the lowest concentration at which there was a significant difference from control values.
NSE = no significant effect detected.
Sources: 1, Maltby 1992b; 2, Maltby et al. 1990a; 3, A. Pedersen, unpublished; 4, Tattersfield 1993;
5, Stuhlbacher & Maltby 1992; 6, C. Naylor, unpublished; 7, Naylor et al. 1989; 8, L. Maltby, unpublished.
Figure 2. Logarithmic relationships between LC50 values and critical concentrations (μmol 1-1) for feeding
rate (i.e. concentration at which feeding rate differed significantly from that of control animals,Cc) . Each
data point represents a different stressor (see the text) and the regression line is defined by the equation:
log10 C c = log LC50- 0.89.
Because changes in SfG were determined principally by reductions in energy intake, for
monitoring or screening purposes the assay may be simplified to a measure of feeding rate
(Maltby 1992b). The feeding rate of G. pulex can be measured in situ by placing animals in
individual cages with a known amount of food and recording the amount consumed over a set
period of time (i.e. 6 days). This method has been used successfully to monitor a range of
discharges, including those from sewage treatment works, fish farms, watercress farms, coal
mines, quarries, dairy farms and motorways (Maltby et al. 1990b; Crane & Maltby 1991;
102
L. Maltby
Roddie et al. 1992; Veerasingham & Crane 1992; Bermingham 1993). Gammarus feeding rate
has also been shown to be sensitive to acid and ammonia pulses (McCahon et al. 1989, 1991).
Perturbations in the physiological energetics of Gammarus have therefore been
demonstrated to provide a general and sensitive stress indicator which can be used in
laboratory toxicity tests to predict potential impact and deployed in situ to monitor effects in
natural systems. However, what does a reduction in SfG, or its major component, feeding rate,
mean to individual gammarids and the communities to which they belong?
Implications for individuals and communities
Physiology to organism level
Implicit in the use of SfG as a stress indicator is the assumption that perturbations translate into
changes in either growth and/or reproduction and are therefore related, in a rigorous and
mechanistic way, to effects at higher levels of biological organisation (Calow & Sibly 1990).
The acquisition and allocation of energy determines developmental rates, growth rates,
fecundity and survival; all are important components of fitness and determinants of population
structure and dynamics. Gammarus energy budgets have been successfully used to predict the
concentrations of pollutants at which growth and reproduction will be impaired as well as the
magnitude of this impairment. For example, a knowledge of the effect of unionized ammonia
on the energy budget of juvenile G. pulex was used to predict the effect of this stressor on
growth rates. The resulting correlation between predicted and observed specific growth rates
was highly significant (Fig. 3; r2 = 0.92, d.f. = 4, p < 0.001), the regression coefficient not
differing significantly from unity (t = 1.4, d.f. = 4, p > 0.05).
Stress-induced reductions in SfG have also been shown to be correlated with reductions in
reproductive output, both in the form of reduced offspring size and brood viability (Maltby &
Naylor 1990; Tattersfield 1993). Reproduction is energetically costly and investment in
reproduction is negatively correlated with future survival and/or reproductive potential (Bell &
Koufopanou 1986). A female gammarid can produce several broods in a life time (Nilsson
1977; Welton & Clarke 1980) but must moult between each brood, a process which also
requires energy (Lynch 1989). A brooding female therefore requires energy for maintenance,
Figure 3. Relationship between predicted and observed specific growth rates (% per day) of juvenile
Gammarus pulex exposed to unionized ammonia. Regression equation: Predicted Gs = 0.83 (Observed
Gs) + 0.09.
Using Gammarus to assess water quality
103
Figure 4. The effect of zinc exposure (mg Zn l-1) on mean (+ SE) offspring size (mm length). (After
Maltby&Naylor l990).
moulting and egg provisioning. If energy intake is reduced, then stored energy may be utilized
to either maintain the animal (Nisbet et al. 1989) or to provision offspring (Kooijman 1986).
Further reductions in energy intake would result in a reduced allocation to reproduction
resulting in reduced offspring size and/or number.
The development of eggs in the ovaries of G. pulex takes two instars; oocytes produced in
one instar are provisioned in the subsequent instar after which they are passed into the brood
pouch to continue their development (Sutcliffe 1992). The link between stress-induced
reductions in SfG and resource allocation to reproduction can therefore be investigated
experimentally by exposing brooding females to concentrations of toxicant known to reduce
SfG for one brood and then recording the number and size of offspring produced in the
subsequent brood (i.e the brood that was being provisioned during exposure). Such an
experiment has been performed using zinc as the stressor; exposure to 0.3 mg Zn1-1resulted in
a significant reduction in both SfG and offspring size (Fig. 4; Maltby & Naylor 1990). There is,
therefore, evidence of a mechanistic link between reduction in SfG and reduced offspring size.
However, as a result of the trade-off between offspring size and number, natural selection
would act to optimize offspring size to that which ensures maximum offspring survival but
little more (Lloyd 1987). Consequently, the size of offspring produced by unstressed animals
may be close to the minimum viable size and hence further reductions would greatly reduce
offspring viability. Under such circumstances, large reductions in energy intake may result in
missing out some broods, rather than decreasing the size of the offspring (Perrin et al. 1990).
If energy availability reduces to such an extent that a brooding female does not have enough
energy to maintain herself and her brood through the instar and moult successfully at the end,
the brood may be aborted and the offspring ingested (Tattersfield 1993). However, even if a
female ingests all her offspring, she will not recover the energy expended on that brood and,
consequently, brood abortion must be a response to short-term unpredictable stress rather than
an adaptation to long-term or predictable stressors. The way life-history patterns may be
modified under long-term stress is considered later.
Physiology to community level
Indicators of stress based on individual species can only identify direct effects and provide no
information about indirect effects resulting from interactions between species (e.g.
104
L. Maltby
competition, predation, parasitism). However, by concentrating on key organisms and
processes, it may be possible to design single-species tests that provide real insight into the
effects of stress and disturbance on ecosystems. For example, detritivores such as G. pulex are
important to the economy of allochthonous-based systems. Impeding their rate of energy intake
could reduce the rate at which terrestrially-fixed organic matter is incorporated into the aquatic
food web, which will have consequences not only for the detritivores themselves and the
organisms that prey upon them, but for the functioning of the system as a whole (Maltby
1992a). Accumulations of leaf material are common in stressed flowing-water systems
(Wallace et al. 1982; Carpenter et al. 1983; Chamier 1987) and stress-induced reductions in
Gammarus feeding rate have been shown to be correlated with reductions in the processing of
leaf material by a semi-natural stream community (Fig. 5; Tattersfield 1993).
In addition to links between Gammarus energetics and community function, results from a
number of field trials indicated that between-station differences in Gammarus feeding rate
were correlated with between-station differences in community structure (Fig. 6; r - 0.68, d.f.
= 9, p < 0.05; Crane & Maltby 1991; Veerasingham & Crane 1992). However, this correlation
is not the result of a causal relationship between Gammarus energetics and community
structure; rather, it illustrates the point that this assay may be used to indicate deteriorations in
water quality which, if they persist, may result in changes in community structure.
Adaptation to long-term stress
The consequences of prolonged reductions in energy acquisition and SfG would be reduced
growth rates, increased developmental times and/or reduced fecundities (Lynch 1989). All
these effects would reduce individual fitness and influence population structure (Calow &
Sibly 1990). However, organisms may adapt to long-term stress. There are many examples of
animals from polluted sites being more resistant to stressors than individuals from unpolluted
sites (e.g. Bryan 1976; Benson & Birge 1985; Price & Swift 1985). In addition, animals may
also respond to stress by modifying their life histories (Maltby et al. 1987). Life-history theory
can be used to predict what type of life-history patterns should be selected for under particular
sets of environmental conditions (Southwood 1988). For example, Sibly & Calow (1985) have
proposed a habitat classification scheme based on two variables, an index of age-specific
survival (S; ratio of juvenile to adult survival) and an index of juvenile growth (G). The basic
predictions arising from this model are: (i) as S increases, investment in reproduction should
increase, (ii) as G increases, this investment should be allocated into fewer, larger offspring.
This model can therefore be used to predict how much resource animals in stressed
environments should invest in reproduction and how this resource should be allocated between
offspring.
Exposure to toxicants has been shown to reduce feeding rates in a wide range of species
including fish (Weis & Weis 1989), crustaceans (Kersting & van der Honing 1981; Donker &
Bogert 1991), molluscs (Widdows 1985; Foe & Knight 1987), cnidarians (Zamer & Shick
1987) and echinoderms (Shirley & Stickle 1982a). Stress-induced reductions in feeding rate
would translate into decreased SfG and hence growth. Therefore, according to the Sibly/Calow
model, animals in stressed environments should produce fewer, larger offspring than those in
non-stressed environments.
Several laboratory experiments have indicated that juveniles are more sensitive to stressors
than adults (e.g. Buikema & Benfield 1979; McCahon & Pascoe 1988; Naylor et al. 1990).
Therefore, according to the Sibly/Calow model, stress would result in a decrease in agespecific survival and hence select for reduced reproductive investment. However, results from
laboratory experiments are usually conducted on animals from unpolluted sites and may not,
Using Gammarus to assess water quality
105
Figure 5. Relationship between the feeding rate of Gammarus pulex (joulesmg-1day-1) exposed to copper,
and the processing of leaf material (% weight loss) by communities exposed to copper in artificial
streams. (Data from Tattersfield 1993).
Figure 6. Relationship between the ratio of the feeding rate of Gammarus upstream and downstream of a
discharge, and the ratio of the BMWP score upstream and downstream of a discharge. (Data from Crane
& Maltby 1991; Veerasingham & Crane 1992; Crane & Maltby unpublished).
therefore, provide a true reflection of the responses of animals from stressed populations. For
example, selective mortality may mean that age-specific effects are greater in animals from
polluted populations than from clean populations, thus selecting for greater reproductive effort
than expected (Fraser 1980; Naylor et al. 1990). Alternatively, exposure to chemicals which
accumulate, or which cause damage which is cumulative, may result in a reduction in agespecific differences and in extreme cases may result in adults being more sensitive than
106
L. Maltby
Figure 7. Above, reproductive effort (mg offspring body wt per mg female body wt) and below, size of
offspring produced by Asellus aquaticus upstream (open bars) and downstream (hatched bars) of a coal
mine discharge into the River Don, Sheffield. (After Maltby 1991).
juveniles. In general, basing predictions on results obtained using animals from unstressed
populations will simply mean that the magnitude of the effect of stress on reproductive
investment has either been under- or over-estimated. Only in extreme cases will the prediction
be wrong; that is, animals in stressed environments have increased, rather than reduced, their
investment in reproduction (e.g. Donker et al. 1993). In conclusion, therefore, animals may
adapt to long-term stress and reduced scope for growth by investing less in reproduction and
allocating resources into fewer but larger offspring (Fig. 7; Maltby 1991).
Conclusions
(1). Bioassays based on the physiological energetics of Gammarus pulex, either scope for
growth or feeding rate, provide a sensitive and general measure of water quality.
(2). Energy budgets can predict stress-induced reductions in growth, offspring size and brood
viability.
(3). Reductions in feeding rates are correlated with changes in community function (i.e. leaf
Using Gammarus to assess water quality
107
processing) and may be indicative of changes in community structure.
(4). Stress-induced changes in Gammarus energetics can therefore be linked, in a mechanistic
way, to effects at higher levels of biological organisation.
(5). Organisms may adapt to long-term stress by altering reproductive investment and
producing fewer, larger offspring.
The author would like to thank Caroline Naylor, Mark Crane and Lisa Tattersfield for their valuable
contributions to the work described in this paper and for permission to cite unpublished information.
References
Bayne, B. L., Brown, D. A., Burnes, K., Dixon, D. R., Ivanovici, A., Livingstone, D. R., Lowe, D. M.,
Moore, M. N., Stebbing, A. R. D. & Widdows, J. (1985). The Effects of Stress and Pollution on Marine
Animals. Praeger, New York. 384 pp.
Bayne, B. L. & Newell, R. C. (1983). Physiological energetics of marine molluscs. In The Mollusca,
Volume 4 (ed. A. S. M. Saleuddin & K. M. Wilbur), pp. 407-515. Academic Press, New York.
Bell, G. & Koufopanou, V. (1986). The cost of reproduction. Oxford Surveys in Evolutionary Biology, 3,
83-131.
Benson, W. H. & Birge, W. J. (1985). Heavy metal tolerance and metallothionein induction in fathead
minnows: results from field and laboratory investigations. Environmental Toxicology and Chemistry,
4, 209-217.
Bermingham, S. (1993). The effect of drainage waters from an abandoned coal-mine on leaf litter
processing in a freshwater stream. Unpublished PhD Thesis, University of Sheffield.
Bryan, G. W. (1976). Some aspects of heavy metal tolerance in aquatic organisms. In Effects of Pollutants
on Aquatic Organisms (ed. A. P. M. Lockwood), pp. 7-34. Cambridge University Press, Cambridge.
Buikema, A. L. Jr & Benfield, E. F. (1979). Use of macroinvertebrate life history information in toxicity
tests. Journal of the Fisheries Research Board of Canada, 36, 321-328.
Calow, P. & Sibly, R. M. (1990). A physiological basis of population processes: ecotoxicological
implications. Functional Ecology, 4, 283-288.
Capuzzo, J. M. (1985). The effects of pollutants on marine zooplankton populations: sublethal
physiological indices of population stress. In Marine Biology of Polar Regions and Effects of Stress
on Marine Organisms (eds J. S. Gray & M. E. Christiansen), pp. 475-491. John Wiley & Sons, New
York.
Carpenter, J., Odum, W. E. & Mills, A. (1983). Leaf litter decomposition in a reservoir affected by acid
mine drainage. Oikos, 41, 165-172.
Chamier, A.-C. (1987). Effect of pH on microbial degradation of leaf litter in seven streams of the
English Lake District. Oecologia, 71, 491-500.
Crane, M. & Maltby, L. (1991). The lethal and sublethal responses of Gammarus pulex to stress:
sensitivity and sources of variation in an in situ bioassay. Environmental Toxicology and Chemistry,
10,1331-1339
Donker, M. H. & Bogert, C. G. (1991). Adaptation to cadmium in three populations of the isopod
Porcellio scaber. Comparative Biochemistry and Physiology, 100C, 143-146.
Donker, M. H., van Capelleveen, H. E. & van Straalen, N. (1993). Metal contamination affects sizestructure and life-history dynamics in isopod field populations. In Ecotoxicology of Metals in
Invertebrates (eds R. Dallinger & P. S. Rainbow), pp. 383-399. Lewis Publishers, Boca Raton.
Donkin, P. & Widdows, J. (1986). Scope for growth as a measurement of environmental pollution and its
interpretation using structure-activity relationships. Chemistry and Industry, Nov. 1986, 732-737.
Edwards, R. R. C. (1978). Effects of water soluble oil fractions on metabolism, growth and carbon budget
of the shrimp Crangon crangon. Marine Biology, 46, 259-265.
Foe, C. & Knight, A. (1987). Assessment of the biological impact of point source discharges employing
Asiatic clams. Archives of Environmental Contamination and Toxicology, 16, 39-51.
Fraser, J. (1980). Acclimation to lead in the freshwater isopod Asellus aquaticus. Oecologia, 45, 419-420.
Fry, F. E. J. (1947). Effects of the environment on animal activity. University of Toronto Studies in
Biology Series, 55, 1-62.
108
L. Maltby
Fry, F. E. J. (1971). The effect of environmental factors on the physiology of fish. In Physiology of
Fishes, Volume 1 (eds W. S. Hoar & D. J. Randall), pp. 1-98. Academic Press, London.
Grodzinski, W., Klekowski, R. Z. & Duncan, A. (1975). Methods for Ecological Energetics, IBP
Handbook No. 24. Blackwell Scientific Publications, Oxford. 367 pp.
Ivleva, I. V. (1980). The dependence of crustacean respiration rate on body mass and habitat temperature.
Internationale Revue der Gesamten Hydrobiologie und Hydrographie, 65, 1-47.
Johns, D. M. & Pechenik, J. A. (1980). Influence of the water-accomodated fraction of No. 2 fuel oil on
energetics of Cancer irroratus larvae. Marine Biology, 55, 247-254.
Kersting, K. & van der Honing (1981). Effect of the herbicide dichlobenil on the feeding and filtering rate
of Daphnia magna. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte
Limnologie, 21, 1135-1140.
Kooijman, S. A. L. M. (1986). Energy budgets can explain body size relations. Journal of Theoretical
Biology, 121, 269-282.
Lloyd, D. G. (1987). Selection of offspring size at independence and other size-versus-number strategies.
American Naturalist, 129, 800-817.
Lynch, M. (1989). The life history consequences of resource depression in Daphnia pulex. Ecology, 70,
246-256.
MacDonald, B. A. & Thompson, R. J. (1986). Influence of temperature and food availability on the
ecological energetics of the giant scallop Placopecten magellanicus. III. Physiological ecology, the
gametogenic cycle and scope for growth. Marine Biology, 93, 37-48.
Maitland, P. S. (1966). Notes on the biology of Gammarus pulex in the River Endrick. Hydrobiologia, 38,
142-152.
Maltby, L. (1991). Pollution as a probe of life-history adaptation in Asellus aquaticus (Isopoda). Oikos,
61,11-18.
Maltby, L. (1992a). Detritus processing. In The Rivers Handbook, Volume 1 (eds P. Calow & G. E.
Petts), pp. 331-353. Blackwell Scientific Publishers, Oxford.
Maltby, L. (1992b). The use of the physiological energetics of Gammarus pulex to assess toxicity: a study
using artificial streams. Environmental Toxicology and Chemistry, 11, 79-85.
Maltby, L. & Calow, P. (1989). The application of bioassays in the resolution of environmental problems:
past, present and future. Hydrobiologia, 188/189, 65-76.
Maltby, L. & Naylor, C. (1990). Preliminary observations on the ecological relevance of the Gammarus
'scope for growth' assay: effect of zinc on reproduction. Functional Ecology, 4, 393-397.
Maltby, L., Naylor, C. & Calow, P. (1990a). Effect of stress on a freshwater benthic detritivore: scope for
growth in Gammarus pulex. Ecotoxicology and Environmental Safety, 19, 285-291.
Maltby, L., Naylor, C. & Calow, P. (1990b). Field deployment of a scope for growth assay involving
Gammarus pulex, a freshwater benthic invertebrate. Ecotoxicology and Environmental Safety, 19, 292300.
Maltby, L., Calow, P., Cosgrove, M. & Pindar, L. (1987). Adaptation in aquatic invertebrates; speculation
and preliminary observations. Annales Societé Royal Zoologique Belgique (Supplement 1), 117, 105115.
Martin, M. (1985). State mussel watch: toxic surveillance in California. Marine Pollution Bulletin, 16,
140-146.
McCahon, C. P. & Pascoe, D. (1988). Use of Gammarus pulex (L.) in safety evaluation tests: culture and
selection of a sensitive life stage. Ecotoxicology and Environmental Safety, 15, 245-252.
McCahon, C. P., Brown, A. F., Poulton, M. J. & Pascoe, D. (1-989). Effects of acid, aluminium and lime
additions on fish and invertebrates in a chronically acidic Welsh stream. Water, Air and Soil Pollution,
45, 345-359.
McCahon, C. P., Poulton, M. J., Thomas, P. C, Xu, Q. & Pascoe, D. (1991). Lethal and sublethal toxicity
of field simulated farm waste episodes to several freshwater invertebrate species. Water Research, 25,
661-671.
Naylor, C , Maltby, L. & Calow, P. (1989). Scope for growth in Gammarus pulex, a freshwater benthic
detritivore. Hydrobiologia, 188/189, 517-523.
Naylor, C , Pindar, L. & Calow, P. (1990). Inter- and intraspecific variation in sensitivity to toxins; the
Using Gammarus to assess water quality
109
effects of acidity and zinc on the freshwater crustaceans Asellus aquaticus (L.) and Gammarus pulex
(L.). Water Research, 24, 757-762.
Nilsson, L. M. (1974). Energy budget of a laboratory population of Gammarus pulex (Amphipoda).
Oikos, 25, 35-42.
Nilsson, L. M. (1977). Incubation time, growth and mortality of the amphipod Gammarus pulex under
laboratory conditions. Oikos, 29, 93-98.
Nisbet, R. M., Gurney, W. S. C , Murdoch, W. W. & McCauley, E. (1989). Structured population models:
a tool for linking effects at individual and population level. Biological Journal of the Linnean Society,
37, 77-99.
Peakall, D. (1992). Animal Biomarkers as Pollution Indicators. Chapman & Hall, London. 291 pp.
Perrin, N., Bradley, M. C. & Calow, P. (1990). Plasticity of storage allocation in Daphnia magna. Oikos,
59, 70-74.
Price, E. E. & Swift, M. C. (1985) Inter- and intra-specific variability in the response of zooplankton to
acid stress. Canadian Journal of Fisheries and Aquatic Sciences, 42, 1749-1754.
Roddie, B., Kedwards, T. & Crane, M. (1992). Potential impact of watercress farm discharges on the
freshwater amphipod, Gammarus pulex (L.). Bulletin of Environmental Contamination and
Toxicology, 48, 63-69.
Sheehan, P. J. (1984). Effects on individuals and populations. In Effects of Pollutants at the Ecosystems
Level (eds P. J. Sheehan, D. R. Miller, G. C. Butler & Ph. Bourdeau), pp. 23-99. John Wiley & Sons
Ltd, Chichester.
Shirley, T. C. & Stickle, W. B. (1982a). Responses of Leptasterias hexactis (Echinodermata: Asteroidea)
to low salinity. I. Survival, activity, feeding, growth and absorption efficiency. Marine Biology, 69,
147-154.
Shirley, T. C. & Stickle, W. B. (1982b). Responses of Leptasterias hexactis (Echinodermata: Asteroidea)
to low salinity. II. Nitrogen metabolism, respiration and energy budget. Marine Biology, 69, 155-163.
Sibly, R. M. & Calow, P. (1985). The classification of habitats by selection pressures: a synthesis of
life-cycle and r/K theory. In Behavioural Ecology. Ecological Consequences of Adaptive Behaviour
(eds R. M. Sibly & R. H. Smith), pp. 75-90. Blackwell, Oxford.
Smyly, W. J. P. (1957). The life history of the bullhead or miller's thumb (Cottus gobio L.). Proceedings
of the Zoological Society of London, 128, 431-453.
Southwood, T. R. E. (1988). Tactics, strategies and templates. Oikos, 52, 3-18.
Stickle, W. B., Rice, S. D. & Moles, A. (1984). Bioenergetics and survival of the marine snail Thais lima
during long-term oil exposure. Marine Biology, 80, 281-289.
Stuhlbacher, A. & Maltby, L. (1992). Cadmium resistance in Gammarus pulex (L.). Archives of
Environmental Contamination and Toxicology, 22, 319-324.
Sutcliffe, D. W. (1984). Quantitative aspects of oxygen uptake by Gammarus (Crustacea, Amphipoda): a
critical review. Freshwater Biology, 14, 443-489.
Sutcliffe, D. W. (1992). Reproduction in Gammarus (Crustacea, Amphipoda): basic processes.
Freshwater Forum, 2, 102-128.
Tattersfield, L. J. (1993). Effects of copper on the energy budget of a stream detritivore: validation and
ecological relevance. Unpublished PhD Thesis, University of Sheffield.
Taylor, E. J., Jones, D. P. W., Maund, S. J. & Pascoe, D. (1993). A new method for measuring the feeding
activity of Gammarus pulex (L.). Chemosphere, 26, 1375-1381.
Veerasingham, M. & Crane, M. (1992). Impact of farm waste on freshwater invertebrate abundance and
the feeding rate of Gammarus pulex (L.). Chemosphere, 25, 869-874.
Wallace, J. B., Webster, J. R. & Cuffney, T. F. (1982). Stream detritus dynamics: regulation by
invertebrate consumers. Oecologia, 53, 197-200.
Warren, C. E & Davis, G. E. (1967). Laboratory studies on the feeding, bioenergetics and growth of fish.
In The Biological Basis of Freshwater Fish Production (ed. S. D. Gerking), pp. 175-214. Blackwell
Scientific Publications, Oxford.
Weis, J. S. & Weis, P. (1989). Tolerance and stress in a polluted environment. BioScience, 39, 89-95.
Welton, J. S. (1979). Life-history and production of the amphipod Gammarus pulex in a Dorset chalk
stream. Freshwater Biology, 9, 263-275.
110
L. Maltby
Welton, J. S. & Clarke, R. T. (1980). Laboratory studies on the reproduction and growth of the amphipod,
Gammarus pulex. Journal of Animal Ecology, 49, 581-592.
Widdows, J. (1985). Physiological responses to pollution. Marine Pollution Biology, 16, 129-134.
Widdows, J. & Donkin, P. (1991). Role of physiological energetics in ecotoxicology. Comparative
Biochemistry and Physiology, 100C, 69-75.
Widdows, J. & Page, D. S. (1993). Effects of tributyltin and dibutyltin on the physiological energetics of
the mussel, Mytilus edulis. Marine Environment Research, 35, 233-249.
Willoughby, L. G. & Earnshaw, R. (1982) Gut passage times in Gammarus pulex (Crustacea,
Amphipoda) and aspects of summer feeding in a stony stream. Hydrobiologia, 97, 105-117.
Willoughby, L. G. & Sutcliffe, D. W. (1976). Experiments on the feeding and growth of the amphipod,
Gammarus pulex (L.) related to its distribution in the River Duddon. Freshwater Biology, 6, 577-586.
Winberg, G. G. (1960). Rate of metabolism and food requirement of fishes. Fisheries Research Board of
Canada Translation Service,. 194, 1-253.
Worrell, C. M., Widdows, J. & Lowe, D. M. (1983). Physiological ecology of three populations of the
bivalve, Scrobicularia plana. Marine Ecology Progress Series, 1, 267-279
Zamer, W. E. & Shick, J. M. (1987). Physiological energetics of the intertidal sea anemone Anthopleura
elegantissima. Marine Biology, 93, 481-491.