- Email: [email protected]
Community and population indicators of ecosystem health: targeting links between levels of biological organisation
AljlUllC 1llmcliul6Y
ELSEVIER
Aquatic
Toxicology
38 (1997) 183-197
Community and population indicators of ecosystem health targeting links between levels of biological organisation Martin
J. Attrill*,
Michael
:
H. Depledge
Marine Biology and Ecotoxicology Group, Plymouth Environmental Research Centre. University of Plymouth, Drake Circus, Plymouth, PL4 SAA. UK Accepted
17 September
1996
Abstract Risk assessments have regularly utilised analysis at the community level as a tool for determining the health of an aquatic system. Using relevant examples, the pros and cons of community level investigation are reviewed, highlighting both the recent advances employing coarse levels of taxonomic identity and the suitability of fish communities for such analyses. Community structure, however, is merely an expression of variation in the populations of the constituent species and the response of these populations to environmental stress. In turn: the maintenance of populations is dictated by the input of individuals within that population in terms of growth (biomass) and reproductive output (persistence), parameters which can provide useful information on the health of a system. It is therefore important to explore the mechanisms linking the different levels of biological organisation to understand how
individual toxicological responses may be expressed at the community level and conversely what mechanisms are producing observed community structures in stressed systems. This also has consequences in terms of risk assessment, determining which level of organisation provides the most sensitive Keywords:
and robust
Fish communities;
method
of assessing
Risk assessment;
environmental
Environmental
health.
impact
1. Introduction The structure of aquatic ecosystems can be defined as successive layers of biological organisation with each compartment controlling the composition of the subsequent level (e.g. community structure is dictated by input from constituent populations of species). To investigate the health of an aquatic system, risk assessments can employ a suite of techniques targeted at one of these levels of biological *Corresponding author. Tel.: +44 1752 232916; e-mail: [email protected].
fax: +44 1752 232970
0166-445X/97/$17.00 0 1997 Elsevier Science B.V. All rights PIISOl66-445X(96)00839-9
reserved
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organisation. However, the community is the most popular level of investigation for environmental assessment (Warwick, 1993) and has been suggested as the most important level for impact studies (Clements and Kiffney, 1994; Martin and Richardson, 1995), so the aim of this paper is to provide an overview of the use of field data from communities and populations in ecological risk assessment. As the majority of community studies have focused on invertebrates, the emphasis of this review will be on data gathered from fish studies where many analytical techniques have only recently, or rarely, been applied. Examples will be provided from marine, estuarine and freshwater environments. It is not the intention to ‘sell’ fish community analysis, but to attempt to use this group as a vehicle for presenting analytical techniques and to focus on important parameters that may provide information on the links between levels of biological organisation.
2. Why use community
analysis?
Investigations at the community level have a number of fundamental advantages over assessments targeted at lower levels of organisation. First, they are the most ecologically relevant as alterations in community structure can be extrapolated to the health of the ecosystem (including humans) through changes in the food web, competition/predation, etc. Second, investigations at lower levels (e.g. individual toxicity tests) tend to focus on the responses of a single species. The community, however, provides a multispecies response, with a suite of species (often covering a wide taxonomic range) that have a range of sensitivities to any given contaminant. Toxicity tests tend to concentrate on species that survive well under laboratory conditions (e.g. Mytilus edulis, Duphnia magna, Carcinus maenas) and that have a relatively high tolerance to contamination. These are not necessarily the most relevant to the natural situation, nor the species that will be removed at the community level, indeed species chosen for toxicity tests are often not even present in the ecosystem under investigation (Richardson and Martin, 1994). This is often justified by using the example of taking canaries down mines-canaries are not humans and do not occur in mine shafts, but have been used to indicate toxic concentrations of chemicals. However, this is a rather ill-conceived analogy. The aim of toxicity tests should be to predict the impact on species that naturally inhabit the system under investigation and are so subject to that environment’s ambient conditions; a canary would not be the most suitable species for predicting effects on the indigenous subterranean community of organisms. Analysis of the community therefore allows the definition of those species most sensitive to environmental change and prediction of consequences at the ecosystem level. Third, changes in community structure reflect integrated conditions over a longterm period of time, as well as responding to catastrophic events. The impact of a complex mix of contaminants when influenced by a suite of environmental variables is difficult, if not impossible, to predict from laboratory experiments. The commu-
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nity is reflecting the effects of many processes at lower levels of biological organisation that result in the removal of species, or reduction in their fitness. Fourth, community analysis utilising samples taken from the field is non-experimental and so cost effective in terms of capital expenditure. This is particularly important in locations where suitable laboratory facilities and equipment may not be available. However, community level investigations have several limitations. First, community level analysis is not sensitive enough to determine deterioration in ecosystem health. Once an effect is detectable at the community level it is too late (‘the ghost of pollution past’) as it is merely an expression of pollution effects at lower levels of organisation. Therefore, it has been suggested that if an early warning system is required, other methods may be more suitable. However, workshops held by the Group of Experts on the Effects of Pollutants (GEEP) (e.g. Bayne et al., 1988) produced no evidence to suggest that community analyses were less sensitive in detecting pollution effects than methods targeted at the individual, cellular or molecular level (Warwick, 1993). Second, there are no properly randomised controls in a field situation, so it is difficult to account for the influence of natural variables. Modern statistical techniques, such as CANOCO (Ter Braak, 1988) or BIOENV (Clarke and Ainsworth, 1993) have, however, allowed the relationship between environmental variables (including contaminant levels) and community structure to be investigated (e.g. Gray et al., 1990; Somerfield et al., 1994). In addition, such multivariate techniques greatly aid interpretation of complex community data sets.
4
B
1
33 27
6
8
73
9
35
32 26
4
Ire2;4 :
12 2
'
,JO I":29
Species
29 25
5 14
Species (acidity)
Family (acidity)
Fig. 1. Multi-dimensional scaling (MDS) ordinations for a stream microcrustacean community structure over an acidification gradient: (a) ordination of sites at the species level of identification; (b) the same ordination with circles superimposed on sites corresponding to levels of acidity, the larger the circle the more acidic the site; (c) ordination for data aggregated to family level, with the acidification gradient still apparent (after Rundle and Attrill, 1995). MDS plots represent the similarity in community structure between sites, the closer the sites on the ordination, the more similar their community structure. Statistical analyses can be undertaken to investigate links between community structure and environmental variables, and to test the significance in separation of groups of replicates or relationships between similarity matrices (see Clarke, 1993, for full review).
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Third, the process is extremely labour-intensive and time-consuming, due to both the expertise required to identify all components of the community under investigation and the person-hours required to sort samples and undertake the identification. This is a major logistic drawback to the use of community analysis, particularly when targeting benthic invertebrate communities that contain many difficult groups (e.g. polychaetes, chironomids, nematodes, oligochaetes, etc.). Identification of these organisms requires a high level of experience and training, often resulting in data sets with a mix of taxonomic levels from phylum (e.g. Nematoda) to species. One solution to this problem is to aggregate the data to higher taxonomic levels (e.g. family) which requires a lower level of expertise and less processing time. Studies over the last decade (Warwick, 1988) have demonstrated that the impact of certain environmental stressors can be detected by utilising such coarse levels of taxonomy. Rundle and Attrill (1995) described the community structure of stream meiofauna over an acidification gradient (Fig. l), with the pattern of community change along this gradient at the species level being preserved when data were aggregated to family. In marine systems aggregation to even higher taxonomic levels is possible due to the larger number of phyla. Warwick (1988) analysed the benthic invertebrate data obtained before and after the Amoco Cadiz oil tanker disaster off the coast of Brittany, demonstrating that the patterns of community change following the oil spill were equally apparent at species and phylum level (Fig. 2). The latter analysis involved just five groupings (Annelida, Echinodermata, Crustacea, Mollusca,
A4
,A CA b’
D-E\
Oil Spill 1
’ y.___
'E
i
Oil Spill
F% \
A
T-u
S-----R
P-Q/
k+.l
i
Species
0"
'L
F I
/ Phylum
Fig. 2. MDS ordinations of macrofauna community data from the Bay of Morlaix before and after the Amoco Cadiz oil spill. Samples are in temporal order from A-U, with the spill occurring between E and F, indicating how the community changed following the pollution incident. Samples further apart on the MDS plot are more dissimilar in their community structure. (a) Community change as represented at the species level; (b) the pattern preserved when data are aggregated to the phylum level (after Warwick. 1988, 1993).
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others), which would require a very low level of operator expertise to detect an impact. The aggregation of data to high taxonomic levels also allows geographically separated stressed systems (with naturally different species complements, but similar ranges of phyla, families, etc.) to be directly compared, a useful tool when assessing the relative effects of disturbance (see Warwick and Clarke, 1993a; Rundle and Attrill, 1995).
3. How useful are fish communities
for impact studies?
Warwick (1993) outlined a set of advantages and disadvantages for the use of different components of the marine biota (including fish) in environmental impact studies, which can be adapted and extended to encompass lake, river and estuarine fish communities. Due to their large size when compared with macro- and meioinvertebrates and their position in the food web, the use of fish in impact studies has several inherent benefits. First, the general high mobility of fish species allows them to be utilised to asses large-scale, regional effects. As many species cover a wide area during their lifecycle, they are influenced by the health of the system as a whole (e.g. Mediterranean Sea, Great Lakes) rather than the impact of localised pollution. Perhaps such mobile fish communities are therefore true indicators of ecosystem health. Second, the taxonomy of fish is comparatively easy, particularly in Europe and North America, so processing of samples is much quicker at a species level than for similar benthic invertebrate samples. Local knowledge of fish species in other parts of the world also tends to be much greater than for other components of the biota. Third, fish have a very high public profile and commercial importance, so any detectable effect on fish communities or populations can be directly related to human welfare. Certain fish species are considered by the public to be the ultimate indicators of clean water, such as the return of Atlantic salmon (Salvo salur) to the river Thames following an extensive restocking programme (Higgins, 1982). This provided the basis of both public relations and management policy despite the natural rehabilitation of many other fish and invertebrate species (Wheeler, 1979). Whilst it is important to focus on good indicators of ecological health in terms of biological response, such logistical benefits cannot be ignored. Fourth, investigating fish communities allows a multitrophic approach, as most feeding types are represented within fish communities. Many species are near the top of the food web, so could be considered sentinel species for the health of the underlying ecosystem structure. This attribute has been utilised in the development of integrative indices based around the analysis of fish communities and selected parameters from lower levels of organisation, such as the Index of Biotic Integrity (e.g. Karr, 1981; Fausch et al., 1990). Despite these advantages, the use of fish communities in field assessments is comparatively uncommon when compared with benthic invertebrates. This is due to three main reasons which seriously reduce their usefulness. First, quantitative sampling is difficult. Community analysis tends to rely on
188
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L-
1984
M.H. Depledgel Aquatic
1
~~~
1985
1986
Toxicology
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1987
1988
38 (1997)
~__~_l~
1989
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~_~
1990
I
1991
YEAR
Fig. 3. Number of fish species recorded in fortnightly samples taken between 1974 and 1992 from the West Thurrock power station cooling water intake screens on the Thames Estuary. Regression lines fitted for the years 197&1983 and 1983-1992 (courtesy of Environment Agency, Thames Region).
quantitative samples in order to provide temporal and spatial comparisons. Due to both their size and their mobility, fish are difficult to sample. Most netting techniques are .qualitative as little idea of area or volume sampled is achieved and many species display a strong avoidance behaviour to traditional nets (e.g. bass, Dicentrarchus lubrax, to trawls) so biasing the sample. In addition, catching fish is often expensive and labour intensive. Certain techniques do provide at least semi-quantitative data, but are not universally applicable, such as electrofishing in rivers (e.g. Paller et al., 1988; Lobon-Cervia et al., 1994) and the use of cooling water intakes of power stations (e.g. Van Den Broek, 1979; Claridge and Potter, 1984). Second, the conflict of mobility vs site fidelity. An advantage of using fish communities was their ability to integrate conditions over a wide area. However, the majority of impact assessments focus on localised pollution effects, so such attri-
M.J. Attrill, M.H. Depledgel Aquatic Toxicology 38 (1997)
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189
U = un-mined
U
“”
u
“”
u
M = mined
“uu u
M
U
M M
M
M
M
M M M M
M
Fig. 4. MDS ordination for reef-top coral fish communities from the Maldives, illustrating the impact of coral mining (after Dawson-Shepherd et al., 1992). Any significant effect of mining can be investigated using the ANOSIM permutation test (Clarke and Green, 1988).
butes are undesirable for such studies. Site fidelity is more important at a local scale, the target community having to respond to the stressor in situ, any change in community structure therefore being due to comparative sensitivities rather than any natural movement cycles. This mobility has concentrated localised impact assessments on the use of more sedentary benthic macroinvertebrates (Warwick, 1993), but in certain environments, such as some rivers; coral reefs and estuaries, a comparatively stationary, predictable community of fish is present and has been used in a few cases to determine impact. The rehabilitation of the Thames estuary in London has been documented by monitoring the recovery of fish communities entrained on the estuary’s power station intake screens (e.g. Huddart and Arthur, 1971; Wheeler, 1979; Andrews, 1984). This work was continued by the National Rivers Authority (Thames Region) until the closure of West Thurrock power station in 1993, providing an extensive, and probably unique, long-term data set on the dynamics of estuarine fish communities in response to environmental conditions. Fig. 3 illustrates the change in species richness recorded from fortnightly samples taken from West Thurrock power station intake screens, suggesting a continual recovery of the fish community from 19741982, stabilising over the ensuing 9 years. This study emphasises the importance of constructing long-term data sets to assess ecosystem recovery, but also highlights the large amount of time and expense required. Fish community structure was also employed by Dawson-Shepherd et al. (1992) to assess the impact of coral mining in the Maldives, concluding that mining reef flats results in a significantly different fish community (Fig. 4). There was also a much greater spread of replicates from mined areas in the ordination, this increased variation being an additional, quantifiable indication of environmental stress (Warwick and Clarke, 1993b). Increased variability has also been suggested as a tool for assessing pollution effects at the cellular (Hinton et al., 1995), individual (Depledge, 1990) and population (Odum et al., 1979) level. It could be argued that variability, at whatever level, is one of the most important parameters to investigate as survival
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Years lo recover
0
50
100
150
200
250
Distance (km) from recoloinisation source
Fig. 5. Comparative speed of recovery of fish and invertebrate communities Wyoming following treatment with rotenone (after Detenbeck et al., 1992).
in the Green
River,
of a population when exposed to stress may rely on those individuals exhibiting the most extreme responses to toxicity tests (Depledge, 1990). Third, fish communities demonstrate a slow response time to disturbance. This factor is important if monitoring programmes are to be constructed to document recovery from disturbance or community change during chronic pollution events. In the 1960s 715 km of the Green river, Wyoming were treated with rotenone in order to create a sports fishery (Detenbeck et al., 1992). Fish and invertebrate communities were removed and recolonisation was only possible from a single source, so speed of community recovery could be monitored over a 250-km stretch (Fig. 5) with invertebrate communities recovering considerably faster than fish communities. Monitoring programmes focusing on invertebrates would therefore prove more cost effective due to the shorter time-span required to document community recovery, although it could be argued that ecosystem recovery has not occurred until all components of the biota have recovered. In this case, it could be more important to document the return of fish to the system as it may be assumed that the supporting food web structure (microbes, plants, invertebrates) would also be in place.
4. The input from populations Certain impact studies utilising fish communities also focus on the populations of sentinel species within that community (e.g. Carline et al., 1992; Sandstrom, 1994). Community structure is the expression of the population dynamics of all its constituent species and the responses of these populations to environmental stress.
M.J. Attrill, M.H. DepledgeIAquatic Table 1 Indicators of response to stressors (adapted from Evans et al., 1990)
Toxicology 38 (1997)
at the population
Indicator
Input
(a) Density/abundance Biomass Size structure Growth (b) Fecundity Sex ratio Reproductive life span Age of maturity Generation time dispersal (c) Physiological adaptability Genetic diversity Body condition
Size of population
their
input
to community
191
structure
to community
Persistence
Indirect
level and
183-197
in community
in community
at any one time
over time
input to (a) and (b)
There are many population parameters that can be investigated (Table 1) and related to environmental variables, but to link changes at population level to higher levels of organisation it is important to focus on how these parameters influence community structure and thus which are perhaps the most relevant to measure. Changes at the population level can be expressed at the community level in two main ways: 1. 2.
the size of the population within the community at any given time (i.e. abundance, biomass), the persistence of that population within the community over a longer period of time (i.e. successful reproduction, recruitment, etc.).
4.1. Size Comparisons of relative biomass and abundance of populations within communities can yield useful information relating to environmental stress. Warwick (1986) adapted k-dominance curves (Lambshead et al., 1983) to compare both parameters on the same axis, the abundance and biomass of each species being ranked and presented as a percentage cumulative figure (abundance biomass comparison (ABC) curves, Fig. 6). Warwick related the comparative patterns to well-documented cases of benthic invertebrate community change along a gradient of organic pollution (e.g. Pearson and Rosenberg, 1978), disturbed environments tending to be characterised by small r-selected species in high abundances. Therefore, in polluted conditions, the abundance curve would lie well above that for biomass, with the reverse occurring under undisturbed conditions (Fig. 6). This method has been extensively tested and validated for marine benthic systems (e.g. Beukema, 1988; Dauer et al., 1993) and has led to the development of single statistics describing the separation of the curves (Clarke, 1990; Meire and Dereu, 1990). Coeck et al. (1993) successfully
hf./.
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Abundance
Species rank
Grossly
Moderately
Polluted
Polluted
Unpolluted
Fig. 6. Hypothetical abundance biomass comparison (ABC) curves for unpolluted, moderately polluted and grossly polluted conditions (after Warwick, 1986). Species present in the community are ranked in order of the proportion of biomass and abundance they represent (different species may provide the largest contribution to biomass and abundance in the community). These data are then plotted on a cumulative axis, giving interpretable results without the need for historical data.
applied the ABC method to the analysis of fish communities in Belgian rivers, detecting a significant decrease in the ABC index (Meire and Dereu, 1990) downstream of polluting discharges in channelised lowland rivers (Fig. 7), suggesting the technique may have wider applications. 4.2. Persistence The persistence
of a species within
-10
-15
*-
a community
may be predicted
by analysing
ABCindex
-5
0
L
0 Upstream 4 Downstream : --.-:I
_&
C-l
Fig. 7. ABC index calculated for fish communities at sites upstream and downstream of polluting sources in lowland Belgian rivers. A negative index indicates heavily stressed, zero moderately stressed and a positive index unstressed conditions (data from Coeck et al.. 1993).
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1ndividualslsq.m 0
1
2
3
0
3
1
2
in areas
of a Finnish
0
1
2
3
1982 ,983 19a4
1985
1986
1987
1988
1989
1990
Fig. 8. Density of Coregonus albula larvae (after Hakkari and Bagge, 1992).
lake influenced
by paper
mill effluent
parameters associated with reproductive output (Table 1). In particular, there are three aspects of fecundity that can be measured which affect community structure in the long term and can be influenced by environmental stressors. 4.2. I. Survival of oflspring Adults of the species reproduce successfully, but young stages are intolerant to the ambient environmental conditions and so die or fail to develop successfully. Larval stages of organisms often have different sensitivities than adults, a factor that is often neglected in toxicity tests. For example, some estuarine species (e.g. Callinectes sapidus, Eriocheir sinensis) survive in low salinity areas as adults, but have to undertake large-scale migrations to fully marine conditions to spawn, the larvae being unable to survive hyposaline conditions. Hakkari and Bagge (1992) recorded the densities of vandace (Coregonus albula) larvae in areas of a Finnish lake influenced to varying degrees by the effluent from a paper mill. Adults were present at all sites, but a significant decrease in larval density was noted under polluted conditions between 1982-85 (Fig. S), consequent reductions in density being due to overfishing. 4.2.2. Number of offspring produced The actual number of young (or eggs) produced per individual adult is reduced under conditions of environmental stress, reflecting a decreased scope for reproduction at the individual level that is expressed as a lower total reproductive output by the population. This parameter can be easily measured in organisms that brood young. Rundle (1993) recorded a significant decrease in clutch size of the harpacticoid copepod Bryocamptus praegeri in acid streams compared with populations in neutral conditions (Fig. 9).
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70
1
0
o-4
5-0
9-12
13-16
16+
1
Clutch size Fig. 9. Clutch 1993).
sizes of the copepod
Bryocamprus praegeri in acidic and neutral
streams
(after
Rundle,
4.2.3. Successful production of gametes Under stressed conditions, scope for reproduction is reduced so that proportions of the population fail to reproduce at all. Casillas et al. (1991) induced English sole (Purophuys vet&s) from Puget Sound to spawn in the laboratory, correlating a marked decrease in the proportion of the population successfully producing eggs with increasing PAH concentration in the sediment (Fig. 10).
5. Linking the levels It is clear from the previous examples that the physiological condition of the individual organism is related to its reproductive output, the persistence of the population and thus the structure of the resulting community (though probably in a very non-linear way). This highlights the importance of targeting the param-
Fig. 10. Spawning
success of Purophrys vrtulu.v over a pollution
gradient
(after Casillas
et al., 1991)
M.J. Attrill,
M.H.
DepledgeIAquatic
I
Fig.
I I. Levels of biological
organisation,
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indicating
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I
how investigative
processes
should
be targeted
eters that link the levels in order to develop an understanding of the mechanisms determining pollution effects at the population level and above. The results from individual-level toxicity tests or biochemical biomarkers may significantly correlate with environmental stress, but are they directly causing detrimental effects at higher levels of organisation? It is no real surprise that organisms show a response to pollutants at the individual or cellular level, but for these responses to be of use in determining ecosystem health they have to be validated by scientifically investigating consequences at higher levels of biological organisation, rather than a genera1 practice of making unsound extrapoIations from one level to another based on statistical correlations (“correlation is not causation”-Schindler, 1987; Depledge, 1994). Similarly, most community level studies lack any perception of underlying processes determining the observed community structure, the establishment of causality being an important final stage in any investigative framework (Clarke and Warwick, 1994). Therefore, focusing on the mechanisms linking the levels of biological organisation is important for environmentalists working at both ends of the scale and should dictate how future investigative processes are targeted (Fig. 11). Studies are required that are not restricted to a single level of investigation, but consider what is the large-scale relevance of any individual response or which individual parameters are dictating any observed community structure.
Acknowledgements We would like to thank Myles Thomas (Environment Agency, for permission to use Fig. 3 and Marshall Adams for providing write this review.
Thames Region) the incentive to
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Lambshead, P.J.D., H.M. Platt and K.M. Shaw (1983) The detection of differences among assemblages of marine benthic species based on an assessment of dominance and diversity. J. Nat. Hist. 17, X59-874. Lobon-Cervia, J., C.G. Utrilla and E. Querol (1994) An evaluation of the 3-removal method with electrofishing techniques to estimate fish numbers in streams of the Brazilian Pampas. Arch. Hydrobiol. 130, 371-381. Martin, M. and B.J. Richardson (1995) A paradigm for integrated marine toxicity research? Further views from the Pacific Rim. Mar. Pollut. Bull. 30, 8-13. Meire, P.M. and J. Dereu (1990) Use of the abundance/biomass comparison method for detecting environmental stress: some considerations based on intertidal macrozoobenthos and bird communities. J. Appl. Ecol. 27, 210-223. Odum, E.P., J.T. Finn and E.H. Frantz (1979) Perturbation theory and the subsidyystress gradient. Bioscience 29, 349-352. Paller, M.H., R.C. Heidinger and W.M. Lewis (1988) Impact of nonchlorinatcd secondary and tertiary effluents on warm water fish communities. Water Resour. Bull. 24, 65-76. Pearson, T.H. and R. Rosenberg (1978) Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr. Mar Biol. A. Rev. 16, 229-311. Richardson, B.J. and M. Martin (1994) Marine and estuarine toxicity testing: a way to go? Additional sitings from northern and southern hemisphere perspectives. Mar. Pollut. Bull. 28, 1388142. Rundle, SD. (1993) Temporal and demographic patterns of microcrustacean populations in upland Welsh streams of contrasting pH. Arch. Hydrobiol. 128, 91-106. ‘, Rundle, SD. and M.J. Attrill (1995) Comparison of meiobenthic crustacean community structure across freshwater acidification gradients. Arch. Hydrobiol., 133: 441456. Sandstrom, 0. (1994) Incomplete recovery in a coastal fish community exposed to effluent from a modernized Swedish bleached kraft mill. Can. J. Fish. Aquat. Sci. 51, 2195-2202. Schindler, D.W. (1987) Detecting ecosystem responses to anthropogenic stress. J. Fish Aquat. Sci. 44, 6 25. Somerfield, P.J., J.M. Gee and R.M. Warwick (1994) Soft sediment meiofaunal community structure in relation to a long-term heavy metal gradient in the Fal estuary system. Mar. Ecol. Prog. Ser. 105, 7988. Ter Braak, C.J.F. (1988) CANOCO - a FORTRAN program for canonical community ordination by [partial] [detrended] [canonical] correspondence analysis, principle components analysis and redundancy analysis (Version 2.1). Report LWA-88-02, Agricultural Mathematics Group, Wageningen. Van Den Broek, W.L.F. (1979) A seasonal survey of fish populations in the lower Medway Estuary, Kent, based on power station screen samples. Estuar. Cstl. Mar. Sci. 9, l-15. Warwick, R.M. (1986) A new method for detecting pollution effects on marine macrobenthic communities. Mar. Biol. 92, 5577562. Warwick, R.M. (1988) The level of taxonomic discrimination required to detect pollution effects on marine benthic communities. Mar. Pollut. Bull. 19, 259-268. Warwick, R.M. (1993) Environmental impact studies on marine communities: pragmatical considerations. Aust. J. Ecol. 18, 63380. Warwick, R.M. and K.R. Clarke (1993a) Comparing the severity of disturbance: a meta-analysis of marine macrobenthic community data. Mar. Ecol. Prog. Ser. 92, 221-231. Warwick, R.M. and K.R. Clarke (1993b) Increased variability as a symptom of stress in marine communities. J. Exp. Mar. Biol. Ecol. 172, 215-226. Wheeler, A. (1979) The Tidal Thames. The History of a River and its Fishes. Routledge and Kegan Paul, London, 228 pp.
ELSEVIER
Aquatic
Toxicology
38 (1997) 183-197
Community and population indicators of ecosystem health targeting links between levels of biological organisation Martin
J. Attrill*,
Michael
:
H. Depledge
Marine Biology and Ecotoxicology Group, Plymouth Environmental Research Centre. University of Plymouth, Drake Circus, Plymouth, PL4 SAA. UK Accepted
17 September
1996
Abstract Risk assessments have regularly utilised analysis at the community level as a tool for determining the health of an aquatic system. Using relevant examples, the pros and cons of community level investigation are reviewed, highlighting both the recent advances employing coarse levels of taxonomic identity and the suitability of fish communities for such analyses. Community structure, however, is merely an expression of variation in the populations of the constituent species and the response of these populations to environmental stress. In turn: the maintenance of populations is dictated by the input of individuals within that population in terms of growth (biomass) and reproductive output (persistence), parameters which can provide useful information on the health of a system. It is therefore important to explore the mechanisms linking the different levels of biological organisation to understand how
individual toxicological responses may be expressed at the community level and conversely what mechanisms are producing observed community structures in stressed systems. This also has consequences in terms of risk assessment, determining which level of organisation provides the most sensitive Keywords:
and robust
Fish communities;
method
of assessing
Risk assessment;
environmental
Environmental
health.
impact
1. Introduction The structure of aquatic ecosystems can be defined as successive layers of biological organisation with each compartment controlling the composition of the subsequent level (e.g. community structure is dictated by input from constituent populations of species). To investigate the health of an aquatic system, risk assessments can employ a suite of techniques targeted at one of these levels of biological *Corresponding author. Tel.: +44 1752 232916; e-mail: [email protected].
fax: +44 1752 232970
0166-445X/97/$17.00 0 1997 Elsevier Science B.V. All rights PIISOl66-445X(96)00839-9
reserved
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organisation. However, the community is the most popular level of investigation for environmental assessment (Warwick, 1993) and has been suggested as the most important level for impact studies (Clements and Kiffney, 1994; Martin and Richardson, 1995), so the aim of this paper is to provide an overview of the use of field data from communities and populations in ecological risk assessment. As the majority of community studies have focused on invertebrates, the emphasis of this review will be on data gathered from fish studies where many analytical techniques have only recently, or rarely, been applied. Examples will be provided from marine, estuarine and freshwater environments. It is not the intention to ‘sell’ fish community analysis, but to attempt to use this group as a vehicle for presenting analytical techniques and to focus on important parameters that may provide information on the links between levels of biological organisation.
2. Why use community
analysis?
Investigations at the community level have a number of fundamental advantages over assessments targeted at lower levels of organisation. First, they are the most ecologically relevant as alterations in community structure can be extrapolated to the health of the ecosystem (including humans) through changes in the food web, competition/predation, etc. Second, investigations at lower levels (e.g. individual toxicity tests) tend to focus on the responses of a single species. The community, however, provides a multispecies response, with a suite of species (often covering a wide taxonomic range) that have a range of sensitivities to any given contaminant. Toxicity tests tend to concentrate on species that survive well under laboratory conditions (e.g. Mytilus edulis, Duphnia magna, Carcinus maenas) and that have a relatively high tolerance to contamination. These are not necessarily the most relevant to the natural situation, nor the species that will be removed at the community level, indeed species chosen for toxicity tests are often not even present in the ecosystem under investigation (Richardson and Martin, 1994). This is often justified by using the example of taking canaries down mines-canaries are not humans and do not occur in mine shafts, but have been used to indicate toxic concentrations of chemicals. However, this is a rather ill-conceived analogy. The aim of toxicity tests should be to predict the impact on species that naturally inhabit the system under investigation and are so subject to that environment’s ambient conditions; a canary would not be the most suitable species for predicting effects on the indigenous subterranean community of organisms. Analysis of the community therefore allows the definition of those species most sensitive to environmental change and prediction of consequences at the ecosystem level. Third, changes in community structure reflect integrated conditions over a longterm period of time, as well as responding to catastrophic events. The impact of a complex mix of contaminants when influenced by a suite of environmental variables is difficult, if not impossible, to predict from laboratory experiments. The commu-
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nity is reflecting the effects of many processes at lower levels of biological organisation that result in the removal of species, or reduction in their fitness. Fourth, community analysis utilising samples taken from the field is non-experimental and so cost effective in terms of capital expenditure. This is particularly important in locations where suitable laboratory facilities and equipment may not be available. However, community level investigations have several limitations. First, community level analysis is not sensitive enough to determine deterioration in ecosystem health. Once an effect is detectable at the community level it is too late (‘the ghost of pollution past’) as it is merely an expression of pollution effects at lower levels of organisation. Therefore, it has been suggested that if an early warning system is required, other methods may be more suitable. However, workshops held by the Group of Experts on the Effects of Pollutants (GEEP) (e.g. Bayne et al., 1988) produced no evidence to suggest that community analyses were less sensitive in detecting pollution effects than methods targeted at the individual, cellular or molecular level (Warwick, 1993). Second, there are no properly randomised controls in a field situation, so it is difficult to account for the influence of natural variables. Modern statistical techniques, such as CANOCO (Ter Braak, 1988) or BIOENV (Clarke and Ainsworth, 1993) have, however, allowed the relationship between environmental variables (including contaminant levels) and community structure to be investigated (e.g. Gray et al., 1990; Somerfield et al., 1994). In addition, such multivariate techniques greatly aid interpretation of complex community data sets.
4
B
1
33 27
6
8
73
9
35
32 26
4
Ire2;4 :
12 2
'
,JO I":29
Species
29 25
5 14
Species (acidity)
Family (acidity)
Fig. 1. Multi-dimensional scaling (MDS) ordinations for a stream microcrustacean community structure over an acidification gradient: (a) ordination of sites at the species level of identification; (b) the same ordination with circles superimposed on sites corresponding to levels of acidity, the larger the circle the more acidic the site; (c) ordination for data aggregated to family level, with the acidification gradient still apparent (after Rundle and Attrill, 1995). MDS plots represent the similarity in community structure between sites, the closer the sites on the ordination, the more similar their community structure. Statistical analyses can be undertaken to investigate links between community structure and environmental variables, and to test the significance in separation of groups of replicates or relationships between similarity matrices (see Clarke, 1993, for full review).
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Third, the process is extremely labour-intensive and time-consuming, due to both the expertise required to identify all components of the community under investigation and the person-hours required to sort samples and undertake the identification. This is a major logistic drawback to the use of community analysis, particularly when targeting benthic invertebrate communities that contain many difficult groups (e.g. polychaetes, chironomids, nematodes, oligochaetes, etc.). Identification of these organisms requires a high level of experience and training, often resulting in data sets with a mix of taxonomic levels from phylum (e.g. Nematoda) to species. One solution to this problem is to aggregate the data to higher taxonomic levels (e.g. family) which requires a lower level of expertise and less processing time. Studies over the last decade (Warwick, 1988) have demonstrated that the impact of certain environmental stressors can be detected by utilising such coarse levels of taxonomy. Rundle and Attrill (1995) described the community structure of stream meiofauna over an acidification gradient (Fig. l), with the pattern of community change along this gradient at the species level being preserved when data were aggregated to family. In marine systems aggregation to even higher taxonomic levels is possible due to the larger number of phyla. Warwick (1988) analysed the benthic invertebrate data obtained before and after the Amoco Cadiz oil tanker disaster off the coast of Brittany, demonstrating that the patterns of community change following the oil spill were equally apparent at species and phylum level (Fig. 2). The latter analysis involved just five groupings (Annelida, Echinodermata, Crustacea, Mollusca,
A4
,A CA b’
D-E\
Oil Spill 1
’ y.___
'E
i
Oil Spill
F% \
A
T-u
S-----R
P-Q/
k+.l
i
Species
0"
'L
F I
/ Phylum
Fig. 2. MDS ordinations of macrofauna community data from the Bay of Morlaix before and after the Amoco Cadiz oil spill. Samples are in temporal order from A-U, with the spill occurring between E and F, indicating how the community changed following the pollution incident. Samples further apart on the MDS plot are more dissimilar in their community structure. (a) Community change as represented at the species level; (b) the pattern preserved when data are aggregated to the phylum level (after Warwick. 1988, 1993).
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others), which would require a very low level of operator expertise to detect an impact. The aggregation of data to high taxonomic levels also allows geographically separated stressed systems (with naturally different species complements, but similar ranges of phyla, families, etc.) to be directly compared, a useful tool when assessing the relative effects of disturbance (see Warwick and Clarke, 1993a; Rundle and Attrill, 1995).
3. How useful are fish communities
for impact studies?
Warwick (1993) outlined a set of advantages and disadvantages for the use of different components of the marine biota (including fish) in environmental impact studies, which can be adapted and extended to encompass lake, river and estuarine fish communities. Due to their large size when compared with macro- and meioinvertebrates and their position in the food web, the use of fish in impact studies has several inherent benefits. First, the general high mobility of fish species allows them to be utilised to asses large-scale, regional effects. As many species cover a wide area during their lifecycle, they are influenced by the health of the system as a whole (e.g. Mediterranean Sea, Great Lakes) rather than the impact of localised pollution. Perhaps such mobile fish communities are therefore true indicators of ecosystem health. Second, the taxonomy of fish is comparatively easy, particularly in Europe and North America, so processing of samples is much quicker at a species level than for similar benthic invertebrate samples. Local knowledge of fish species in other parts of the world also tends to be much greater than for other components of the biota. Third, fish have a very high public profile and commercial importance, so any detectable effect on fish communities or populations can be directly related to human welfare. Certain fish species are considered by the public to be the ultimate indicators of clean water, such as the return of Atlantic salmon (Salvo salur) to the river Thames following an extensive restocking programme (Higgins, 1982). This provided the basis of both public relations and management policy despite the natural rehabilitation of many other fish and invertebrate species (Wheeler, 1979). Whilst it is important to focus on good indicators of ecological health in terms of biological response, such logistical benefits cannot be ignored. Fourth, investigating fish communities allows a multitrophic approach, as most feeding types are represented within fish communities. Many species are near the top of the food web, so could be considered sentinel species for the health of the underlying ecosystem structure. This attribute has been utilised in the development of integrative indices based around the analysis of fish communities and selected parameters from lower levels of organisation, such as the Index of Biotic Integrity (e.g. Karr, 1981; Fausch et al., 1990). Despite these advantages, the use of fish communities in field assessments is comparatively uncommon when compared with benthic invertebrates. This is due to three main reasons which seriously reduce their usefulness. First, quantitative sampling is difficult. Community analysis tends to rely on
188
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o’-i--1983
L-
1984
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~~~
1985
1986
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~.
1987
1988
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~__~_l~
1989
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~_~
1990
I
1991
YEAR
Fig. 3. Number of fish species recorded in fortnightly samples taken between 1974 and 1992 from the West Thurrock power station cooling water intake screens on the Thames Estuary. Regression lines fitted for the years 197&1983 and 1983-1992 (courtesy of Environment Agency, Thames Region).
quantitative samples in order to provide temporal and spatial comparisons. Due to both their size and their mobility, fish are difficult to sample. Most netting techniques are .qualitative as little idea of area or volume sampled is achieved and many species display a strong avoidance behaviour to traditional nets (e.g. bass, Dicentrarchus lubrax, to trawls) so biasing the sample. In addition, catching fish is often expensive and labour intensive. Certain techniques do provide at least semi-quantitative data, but are not universally applicable, such as electrofishing in rivers (e.g. Paller et al., 1988; Lobon-Cervia et al., 1994) and the use of cooling water intakes of power stations (e.g. Van Den Broek, 1979; Claridge and Potter, 1984). Second, the conflict of mobility vs site fidelity. An advantage of using fish communities was their ability to integrate conditions over a wide area. However, the majority of impact assessments focus on localised pollution effects, so such attri-
M.J. Attrill, M.H. Depledgel Aquatic Toxicology 38 (1997)
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189
U = un-mined
U
“”
u
“”
u
M = mined
“uu u
M
U
M M
M
M
M
M M M M
M
Fig. 4. MDS ordination for reef-top coral fish communities from the Maldives, illustrating the impact of coral mining (after Dawson-Shepherd et al., 1992). Any significant effect of mining can be investigated using the ANOSIM permutation test (Clarke and Green, 1988).
butes are undesirable for such studies. Site fidelity is more important at a local scale, the target community having to respond to the stressor in situ, any change in community structure therefore being due to comparative sensitivities rather than any natural movement cycles. This mobility has concentrated localised impact assessments on the use of more sedentary benthic macroinvertebrates (Warwick, 1993), but in certain environments, such as some rivers; coral reefs and estuaries, a comparatively stationary, predictable community of fish is present and has been used in a few cases to determine impact. The rehabilitation of the Thames estuary in London has been documented by monitoring the recovery of fish communities entrained on the estuary’s power station intake screens (e.g. Huddart and Arthur, 1971; Wheeler, 1979; Andrews, 1984). This work was continued by the National Rivers Authority (Thames Region) until the closure of West Thurrock power station in 1993, providing an extensive, and probably unique, long-term data set on the dynamics of estuarine fish communities in response to environmental conditions. Fig. 3 illustrates the change in species richness recorded from fortnightly samples taken from West Thurrock power station intake screens, suggesting a continual recovery of the fish community from 19741982, stabilising over the ensuing 9 years. This study emphasises the importance of constructing long-term data sets to assess ecosystem recovery, but also highlights the large amount of time and expense required. Fish community structure was also employed by Dawson-Shepherd et al. (1992) to assess the impact of coral mining in the Maldives, concluding that mining reef flats results in a significantly different fish community (Fig. 4). There was also a much greater spread of replicates from mined areas in the ordination, this increased variation being an additional, quantifiable indication of environmental stress (Warwick and Clarke, 1993b). Increased variability has also been suggested as a tool for assessing pollution effects at the cellular (Hinton et al., 1995), individual (Depledge, 1990) and population (Odum et al., 1979) level. It could be argued that variability, at whatever level, is one of the most important parameters to investigate as survival
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Years lo recover
0
50
100
150
200
250
Distance (km) from recoloinisation source
Fig. 5. Comparative speed of recovery of fish and invertebrate communities Wyoming following treatment with rotenone (after Detenbeck et al., 1992).
in the Green
River,
of a population when exposed to stress may rely on those individuals exhibiting the most extreme responses to toxicity tests (Depledge, 1990). Third, fish communities demonstrate a slow response time to disturbance. This factor is important if monitoring programmes are to be constructed to document recovery from disturbance or community change during chronic pollution events. In the 1960s 715 km of the Green river, Wyoming were treated with rotenone in order to create a sports fishery (Detenbeck et al., 1992). Fish and invertebrate communities were removed and recolonisation was only possible from a single source, so speed of community recovery could be monitored over a 250-km stretch (Fig. 5) with invertebrate communities recovering considerably faster than fish communities. Monitoring programmes focusing on invertebrates would therefore prove more cost effective due to the shorter time-span required to document community recovery, although it could be argued that ecosystem recovery has not occurred until all components of the biota have recovered. In this case, it could be more important to document the return of fish to the system as it may be assumed that the supporting food web structure (microbes, plants, invertebrates) would also be in place.
4. The input from populations Certain impact studies utilising fish communities also focus on the populations of sentinel species within that community (e.g. Carline et al., 1992; Sandstrom, 1994). Community structure is the expression of the population dynamics of all its constituent species and the responses of these populations to environmental stress.
M.J. Attrill, M.H. DepledgeIAquatic Table 1 Indicators of response to stressors (adapted from Evans et al., 1990)
Toxicology 38 (1997)
at the population
Indicator
Input
(a) Density/abundance Biomass Size structure Growth (b) Fecundity Sex ratio Reproductive life span Age of maturity Generation time dispersal (c) Physiological adaptability Genetic diversity Body condition
Size of population
their
input
to community
191
structure
to community
Persistence
Indirect
level and
183-197
in community
in community
at any one time
over time
input to (a) and (b)
There are many population parameters that can be investigated (Table 1) and related to environmental variables, but to link changes at population level to higher levels of organisation it is important to focus on how these parameters influence community structure and thus which are perhaps the most relevant to measure. Changes at the population level can be expressed at the community level in two main ways: 1. 2.
the size of the population within the community at any given time (i.e. abundance, biomass), the persistence of that population within the community over a longer period of time (i.e. successful reproduction, recruitment, etc.).
4.1. Size Comparisons of relative biomass and abundance of populations within communities can yield useful information relating to environmental stress. Warwick (1986) adapted k-dominance curves (Lambshead et al., 1983) to compare both parameters on the same axis, the abundance and biomass of each species being ranked and presented as a percentage cumulative figure (abundance biomass comparison (ABC) curves, Fig. 6). Warwick related the comparative patterns to well-documented cases of benthic invertebrate community change along a gradient of organic pollution (e.g. Pearson and Rosenberg, 1978), disturbed environments tending to be characterised by small r-selected species in high abundances. Therefore, in polluted conditions, the abundance curve would lie well above that for biomass, with the reverse occurring under undisturbed conditions (Fig. 6). This method has been extensively tested and validated for marine benthic systems (e.g. Beukema, 1988; Dauer et al., 1993) and has led to the development of single statistics describing the separation of the curves (Clarke, 1990; Meire and Dereu, 1990). Coeck et al. (1993) successfully
hf./.
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Abundance
Species rank
Grossly
Moderately
Polluted
Polluted
Unpolluted
Fig. 6. Hypothetical abundance biomass comparison (ABC) curves for unpolluted, moderately polluted and grossly polluted conditions (after Warwick, 1986). Species present in the community are ranked in order of the proportion of biomass and abundance they represent (different species may provide the largest contribution to biomass and abundance in the community). These data are then plotted on a cumulative axis, giving interpretable results without the need for historical data.
applied the ABC method to the analysis of fish communities in Belgian rivers, detecting a significant decrease in the ABC index (Meire and Dereu, 1990) downstream of polluting discharges in channelised lowland rivers (Fig. 7), suggesting the technique may have wider applications. 4.2. Persistence The persistence
of a species within
-10
-15
*-
a community
may be predicted
by analysing
ABCindex
-5
0
L
0 Upstream 4 Downstream : --.-:I
_&
C-l
Fig. 7. ABC index calculated for fish communities at sites upstream and downstream of polluting sources in lowland Belgian rivers. A negative index indicates heavily stressed, zero moderately stressed and a positive index unstressed conditions (data from Coeck et al.. 1993).
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1ndividualslsq.m 0
1
2
3
0
3
1
2
in areas
of a Finnish
0
1
2
3
1982 ,983 19a4
1985
1986
1987
1988
1989
1990
Fig. 8. Density of Coregonus albula larvae (after Hakkari and Bagge, 1992).
lake influenced
by paper
mill effluent
parameters associated with reproductive output (Table 1). In particular, there are three aspects of fecundity that can be measured which affect community structure in the long term and can be influenced by environmental stressors. 4.2. I. Survival of oflspring Adults of the species reproduce successfully, but young stages are intolerant to the ambient environmental conditions and so die or fail to develop successfully. Larval stages of organisms often have different sensitivities than adults, a factor that is often neglected in toxicity tests. For example, some estuarine species (e.g. Callinectes sapidus, Eriocheir sinensis) survive in low salinity areas as adults, but have to undertake large-scale migrations to fully marine conditions to spawn, the larvae being unable to survive hyposaline conditions. Hakkari and Bagge (1992) recorded the densities of vandace (Coregonus albula) larvae in areas of a Finnish lake influenced to varying degrees by the effluent from a paper mill. Adults were present at all sites, but a significant decrease in larval density was noted under polluted conditions between 1982-85 (Fig. S), consequent reductions in density being due to overfishing. 4.2.2. Number of offspring produced The actual number of young (or eggs) produced per individual adult is reduced under conditions of environmental stress, reflecting a decreased scope for reproduction at the individual level that is expressed as a lower total reproductive output by the population. This parameter can be easily measured in organisms that brood young. Rundle (1993) recorded a significant decrease in clutch size of the harpacticoid copepod Bryocamptus praegeri in acid streams compared with populations in neutral conditions (Fig. 9).
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70
1
0
o-4
5-0
9-12
13-16
16+
1
Clutch size Fig. 9. Clutch 1993).
sizes of the copepod
Bryocamprus praegeri in acidic and neutral
streams
(after
Rundle,
4.2.3. Successful production of gametes Under stressed conditions, scope for reproduction is reduced so that proportions of the population fail to reproduce at all. Casillas et al. (1991) induced English sole (Purophuys vet&s) from Puget Sound to spawn in the laboratory, correlating a marked decrease in the proportion of the population successfully producing eggs with increasing PAH concentration in the sediment (Fig. 10).
5. Linking the levels It is clear from the previous examples that the physiological condition of the individual organism is related to its reproductive output, the persistence of the population and thus the structure of the resulting community (though probably in a very non-linear way). This highlights the importance of targeting the param-
Fig. 10. Spawning
success of Purophrys vrtulu.v over a pollution
gradient
(after Casillas
et al., 1991)
M.J. Attrill,
M.H.
DepledgeIAquatic
I
Fig.
I I. Levels of biological
organisation,
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indicating
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I
how investigative
processes
should
be targeted
eters that link the levels in order to develop an understanding of the mechanisms determining pollution effects at the population level and above. The results from individual-level toxicity tests or biochemical biomarkers may significantly correlate with environmental stress, but are they directly causing detrimental effects at higher levels of organisation? It is no real surprise that organisms show a response to pollutants at the individual or cellular level, but for these responses to be of use in determining ecosystem health they have to be validated by scientifically investigating consequences at higher levels of biological organisation, rather than a genera1 practice of making unsound extrapoIations from one level to another based on statistical correlations (“correlation is not causation”-Schindler, 1987; Depledge, 1994). Similarly, most community level studies lack any perception of underlying processes determining the observed community structure, the establishment of causality being an important final stage in any investigative framework (Clarke and Warwick, 1994). Therefore, focusing on the mechanisms linking the levels of biological organisation is important for environmentalists working at both ends of the scale and should dictate how future investigative processes are targeted (Fig. 11). Studies are required that are not restricted to a single level of investigation, but consider what is the large-scale relevance of any individual response or which individual parameters are dictating any observed community structure.
Acknowledgements We would like to thank Myles Thomas (Environment Agency, for permission to use Fig. 3 and Marshall Adams for providing write this review.
Thames Region) the incentive to
References Andrews, M.J. (1984) Thames Estuary: pollution and recovery. In: Effects of Pollutants at the Ecosystem Level, edited by P.J. Sheehan, D.R. Miller, G.C. Butler and Ph. Bourdeau, John Wiley and Sons Ltd, pp. 195-227.
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