Why do ecological monitoring?

Marine Pollution Bulletin, Vol. I I, pp. 6 2 ~ 5 Pergamon Press Ltd. 1980. Printed in Great Britain.

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Viewpoint is a column which allows authors to express their own opinions about current events.

Why do Ecological Monitoring? JOHN S. GRAY

The author is Professor in the Institute for Marine Biology and Limnology, University of Oslo, Norway. He was formerly a member of the Wellcome Marine Laboratory, at Robin Hood's Bay, Yorkshire, England. Recently, criticism has been raised against ecological monitoring on the grounds that it is time-consuming to obtain the species lists and species abundances which are the basic data, or that ecological monitoring is relatively insensitive. The insensitivity arises because usually only absences of species can be used since the natural changes in abundance of a species from time to time (the background noise) are difficult to separate from pollution effects. The feeling seems to be that if effects of pollutants could be detected on individuals at the physiological or biochemical level before abundance changes then such techniques for monitoring must be preferable. Certainly ecological monitoring has suffered from the type of approach that the only 'good' ecological monitoring is where all the species are monitored all the time. In such studies massive surveys are undertaken and countless hours spent identifying and counting species and the whole repeated as often as is practical. Much money has been wasted doing surveys in the guise of obtaining so-called 'base-lines' which due to their inadequate design could never fulfil their goal of detecting effects of a particular pollutant. Many companies may be getting away with murder since their surveys cannot possibly show any effects except those obvious to the untutored layman where massive mortalities occur. Equally many companies may be employing enormous teams of biologists who wile away their time collecting data that cannot be of any relevance to even the most altruistic company. So how can one come up with a passable ecological monitoring programme that can be expected to answer the questions being posed? Before doing this I would like first to consider alternatives to ecological monitoring. Much effort has been expended recently on physiological monitoring and especially of techniques which are similar in approach to ecological monitoring stich as the estimation of 'scope for growth'. In this technique the energy that an animal absorbs is estimated and from this the amounts going to respiration and that excreted are subtracted giving a balance called the 'scope for growth'. Usually in winter the 'scope' is negative when food reserves are utilized and positive in summer when the reserves are building up. Detailed work has shown that if one compares two populations, one from a polluted area, such as Swansea Harbour, and the other from an unpolluted area, the Swale estuary, one finds that the overall 'scope' is less in the population from the polluted area. Is this surprising, since one could tell that Swansea Harbour was polluted before the investigation began? Similarly it has been claimed that using approximately the 62

same technique but measuring not energy but carbon flux in two populations of Mya arenaria, one from a heavily oil polluted beach and another from an unpolluted area, that the 'scope' is 50% less at the polluted beach over a year. Yet statistical analysis of the data (not done in the studies in question), showed no significant difference between the two populations for two separate studies reported in the literature. So I am not convinced that the technique of measuring 'scope for growth' is in fact more sensitive than the more commonly used ecological techniques. Furthermore 'scope for growth' is an extremely time-consuming measurement to make since one must make detailed seasonal analysis of absorption efficiency, respiration and excretion. The above techniques should in theory be more sensitive since physiological changes can be detected on any individual before the effect can be noted at the population and community level. Some extremely interesting and important new findings on stress physiology have resulted from these studies, but I believe that the apparent lack of sensitivity of these methods so far, lies in the fact that the organisms used are ecologically not the most appropriate. Scope for growth has been measured in a monitoring context on Mytilus edulis and Mya arenaria, two species that are robust and widespread in their distribution, which penetrate into brackish waters and are commonly found in quite polluted waters. With such wide natural tolerances of stress it is to be expected that such species can in fact adapt to many varied forms of pollution and will be insensitive. There are many other species that would on ecological grounds be more appropriate and are a priori likely to be more sensitive. The exact species will vary from geographical region to geographical region and what I will attempt to do is to give a rationale for locating which species to use but of course there are many other ways to tackle this problem. The arguments will be ecological and it is my aim not to decry the use of physiological techniques, but rather to ask for a joint approach of both physiological and ecological monitoring on the same species. Ecological monitoring can be on the structural characteristics of a community such as the numbers or biomass of individuals and species or on the functioning of the community neglecting species identity and measuring, for example, total community respiration or in situ production by the 14C technique. In general, total community respiration has not been found to give results which can be readily interpreted and the technique is extremely difficult to do and is complicated by the anaerobic metabolism of many sediment-living species. Whilst the 14C method is

Volume 11/Number 3/March 1980

now a standard technique it requires regular sampling at frequencies of at least fortnightly intervals if an overall annual figure is to be obtained. In an interesting statistical analysis of data from the Baltic Sea it was calculated that reducing the frequency of observations from weekly to the four per year that the funding agencies thought reasonable, would give confidence limits of 5:200°70 of the actual annual mean! Only when the frequency approaches fortnightly sampling does the confidence limit approach a reasonable figure. Thus to obtain figures for the annual 14C production in the Baltic Sea one has to have a large number of stations sampled 26 times per year, an enormous effort. Using structural properties of communities it may be possible to reduce the sampling effort considerably, but only if one is interested in the long-term year-to-year changes that occur. Plankton is monitored in some sampling programmes such as the Continuous Plankton Recorder (CPR) programme in Britain. Plankton nets are towed behind commercial vessels on runs across the North Sea and Atlantic and by laboriously counting the animals and identifying them to species, trends in the data over decades have been established. The plankton net has a unique advantage over benthic samplers in that it tows through small scale patchiness and thus trends over large areas are easier to ascertain. One could not conceive of benthic sampling to indicate the health of the North Atlantic, whereas the CPR programme can do this admirably. It is very important to remember however, that the CPR programme did not start out as a monitoring programme but as a means of predicting fish stocks from the eggs and larval stages. Now that the data stretch over decades it is a vital long-term data series which must continue. However, if the same arguments about cost-effectiveness had been applied to the programme in its early stages that are applied to other forms of monitoring today, the CPR programme would have been stopped ages ago. Most pollution occurs in coastal areas and here local hydrographical conditions render plankton monitoring impractical. Thus the non-motile benthos is largely used since it is sessile and must tolerate the pollution or die. Rocky shore monitoring is the commonest of all but has rarely stretched over long time periods being largely geared to the three or four years of a Ph.D. study. Since J.R. Lewis has adequately covered approaches to rocky shore monitoring I will not deal with the rocky intertidal further. The great advantage of studying hard substrata is that one can return to exactly the same place and monitor by nondestructive methods. We are using an excellent technique, stereo-photography, subtidally. Not only can species be identified from photographs but the under-canopy fauna and flora can also be seen and growth rates measured since the third dimension can be studied. Subtidally there are not the large variations in climatic ~¢ariables that one finds intertidally. Ours and other studies do indicate, however, that the community structure is determined by variations in larval settlement and chance predation. The changes in community structure are apparently unpredictable on a local scale, that of the 0.25 m -2 used in individual photographs. Over larger areas however, when several photographs are pooled together then consistent patterns occur. Investigations of the rocky subtidal are fairly recent and we do not have the basic knowledge that we have for the

intertidal, but the system suggests that here is a potentially ideal monitoring habitat where changes can be followed with great precision. Sediment covers by far the greatest part of the floor of the ocean and the infauna of sediments are probably the most widely used in ecological monitoring programmes. The fauna are, however, sampled blind and destructively and at most statistical estimates of abundance are obtained. Whilst much attention has been given to such problems as how many samples should be taken, based on the speciesarea curve and the size of sieve to be used the most important aspect of sampling strategy is often neglected. Stratified random sampling can greatly improve the efficiency of most programmes over regular or random sampling especially when different depths or/and sediment types are used for the stratification. Whatever community is sampled there will be a few common species and many rare species represented by only one or a few individuals, except perhaps in polluted areas where there may be only a few common species. This rareness is, therefore, a key ecological property of communities from unpolluted areas. Monitoring programmes which only deal with the ten most common species are neglecting perhaps the most important facet of ecological monitoring. The problem with rare species however, is that one seldom knows why they are rare. They may be rare because of random settlement over a large area, the centre of the population is elsewhere, predation has removed many individuals, mortality has been variable, etc. Thus although rareness is a key property it is nearly impossible to explain since there will be countless explanations varying with each species. So how can we use this property? One way is to combine number of species and individuals per species into a diversity index. Diversity indices do vary along pollution gradients in both space and time but in my experience they are not particularly sensitive. I have used another method which in benthic communities from sediments seems to work. If a large sample is taken from a heterogeneous community from an unpolluted area a log-normal distribution of individuals among species generally occurs (see Gray & Mirza, 1979; Gray, 1979, for details). There is nothing magic about the log-normal, in fact it is merely a distribution that fits large numbers. There is no single underlying principle. A series of normal distributions lumped together will give a log-normal (e.g. species distributed along an environmental gradient), or a series of random variables acting on a population will produce a lognormal distribution. The important thing is that the sample size must be large so that there is a chance to sample most of the species in the area. I believe that the log-normal in this case is a good statistical description of how the individuals are distributed among the species. I interpret the fit as representing an equilibrium community where immigration and emigration of species has stabilized and niche space has been partitioned giving the said distribution. If one moves along a pollution gradient such as a gradient of eutrophication in the Oslofjord one finds that suddenly the log-normal distribution on longer fits the data, the community has gone out of equilibrium. If one continues into the highly polluted area there is a return to the equilibrium community but with quite a different structure to the unpolluted area. Here a few species dominate and numbers increase greatly per unit area compared with the 63

Marine Pollution Bulletin

unpolluted area. The same trend also seems to occur over time at one fixed site. The grounds for believing the lognormal represents an equilibrium community can be substantiated by the fact that in north temperate latitudes in summer the plots of the log-normal indicate that the community goes out of equilibrium when seasonal recruitment occurs. In the autumn when mortality has taken place the community returns to equilibrium. The method above should not be regarded as anything more than a quick and dirty method indicating that something has changed. Use of the method must be accompanied by comparative studies and a follow up study of change is indicated. The really interesting question is why has there been a change? Analysis of the log-normal plots show that along eutrophic gradients, when the community goes out of equilibrium some species become more common, rare species remain and are not eliminated. As pollution increases some rare species are eliminated and some species become very common returning to an equilibrium state but with a structure quite different to that in the unpolluted area. Along gradients of eutrophication in the most polluted areas there are two species which dominate, the polychaetes Capitella capitata and Polydora ciliata. Most people would suspect that the reason for these two species dominating is because they are the most tolerant species, in fact this does not appear to be the case. Under severe eutrophication most of the oxygen is used up and tolerance to low oxygen would be the most obvious adaptive strategy. Yet Capitella is not particularly tolerant of low oxygen and there are many other species which tolerate lower oxygen concentrations yet it is Capitella which occurs in the most polluted areas. I believe that the answer lies in the life-history characteristics of Capitella rather than in the tolerance. Capitella produces both planktonic larvae and also has direct development. It can therefore find new areas to colonize and then rapidly build up the population by reverting to brooding. It has been known to build up populations from 0 to 200000 m -2 in only 2 months. In highly eutrophic areas, such as off a sewage pipe outfall, particles sediment out continuously and smother most species killing them. Capitella with its constantly available larvae can recolonize the sediment again and again and rapidly build up a large population. Polydora also has a planktonic larva and can brood within the tube. In Oslofjord the populations at the most polluted areas breed throughout the year whereas at less polluted areas breeding only occurs for 3 months of the year. Here again is a lifehistory strategy ideally suited for coping with continuous sedimentation of sewage particles. The animals are adapting to a continuous disturbance and not to low oxygen tolerance. For many years Capitella was regarded as a 'universal indicator of organic pollution', since where there was heavy pollution it occurred in large numbers. Then people became suspicious since large populations were found following excavations for a pipeline where the sediment had been disturbed or following an oil spill where most of the fauna had been destroyed. The common factor with all these cases is that where the sediment was disturbed Capitella increased in abundance. If the disturbance is temporary then Capitella returns to its normal low numbers and is outcompeted by other species (e.g. following the oil spill and excavation). Thus pollution effects should not be considered as simply a chemical stress effect but also a disturbance. 64

Under slight pollution stress the reason that species increase in abundance along a eutrophic gradient is that they probably have the life-history characteristics that enable them to increase where other species cannot. Unfortunately there is little biological data on the species that show increased abundance under slight pollution but a programme of research is under way in Oslo. The interesting fact however, is that the 9-10 species that give rise to the departure from the equilibrium log-normal distribution in Oslofjord are very similar to those found in Sweden and Scotland. Thus the log-normal technique objectively gives us a list of species that have been found to be sensitive to small increases in abundance along eutrophic gradients. It is not, however, known if the same will be true for other forms of pollution. The strategy for ecological monitoring of a potentially serisitive area would therefore be to take samples along a pollution gradient and find the point where there is a departure from the log-normal and concentrate on monitoring these 9-10 species. The monitoring programme has been simplified from the possibly 100-odd species found in the initial sampling programme and rationalized to species which do indicate trends. The species in question will vary from one geographical area to another and with sediment type, but the strategy is the same. Some of the species may well be bivalves where monitoring of growth rates can be done retrospectively and more information gained on the history of the specific site. Surely these are the species that should provide the basis for a biochemical, physiological and ecological monitoring programme? In fact there are indications that this approach is a highly promising one. One of the polychaetes that increases in abundance under slight pollution is Chaetozone setosa. Preliminary biochemical studies at the Scottish Marine Biological Association's Oban Laboratory show that a number of enzyme systems increase in activity before the population responds by increasing in abundance. Some of the enzymes are also those commonly used as genetical markers. It is planned to study this species from genetical, biochemical and population dynamical aspects since it looks to be a highly sensitive indicator of effects of eutrophication. If I am correct in my hypothesis that most species adapt to pollution by means of varying their life-history and not by tolerance of stress then there is little to be gained from laboratory toxicity tests. The results of such tests will not predict the ecological consequences of a given concentration of effluent discharge since tolerance does not dictate where the species will be found along a pollution gradient. Again a closer coupling of ecological knowledge in the design of the tests and particularly the selection of organisms is called for. Whilst I can understand the desire for a standard universal toxicity test as a preliminary screening of new chemicals, the prediction of what is a safe concentration to discharge must be related to an appropriate set of local species which cannot be expected to be the same even within one country where there may be many geographical provinces. Much more information is needed on how species adapt to pollution. For too long ecologists have produced long lists of which species occurs where along a given pollution gradient and have ignored the important questions of why a particular species is found at a certain place along the gradient. It will undoubtedly prove to be a whole complex of factors and no simple overall rule can be expected.

Volume I 1/Number 3/March 1980 The most important question concerning ecological monitoring has yet to be posed and that is what do we understand and mean by ecological monitoring? I have used monitoring here as goal orientated towards measuring effects of pollution along a known gradient. This is a very common form of monitoring but is relatively simple since the spatial extent of the monitoring programme is governed by the dispersion of the effluent(s). A more difficult form of monitoring is that concerned with chronic effects over long time periods where one has to be concerned with natural variability in the data. If one is interested in long-term variability over many years then with benthic monitoring it may well be quite sufficient to sample merely once per year. In north temperate latitudes with the massive recruitment in summer (leading to the departure from an equilibrium community indicated by the log-normal plots) monitoring can reasonably be confined to the winter period only. A programme of this type is being done in Northumberland by Dr Buchanan (Buchanan et al., 1978) and has produced excellent results for relatively little effort. This is only possible if one is interested in year-to-year variations and in this case counting and identifying all the newly settled spat in summer would be pointless in relation to the overall aim. Thus the monitoring strategy must be related to the question being asked. Too often the aim of the monitoring is not clearly defined and results in the waste of time and money mentioned at the beginning of this article. Ecological monitoring does not have to be extremely costly if the strategy outlined here is followed. The questions

being asked must be clearly defined and then after an initial investigation a rationalized programme can be followed. Such a programme is likely to be based on intensive studies of a few species from an ecological standpoint measuring growth rates, fecundity, recruitment and general life-table data. On these same species a suite of biochemical and physiological techniques could be applied. The important and new data on stress physiology could then be applied to the ecologically important species and the best of all combinations found. Physiological and biochemical approaches are based on the individual and it is the effects of the population that are important ecologically. Whereas the physiological and biochemical approaches predict effects on populations it is the ecological monitoring that is the only test of whether these predictions are correct. Here, then, is the answer to the question posed in the title. Ecological monitoring is thus essential but the ideal is a combination of biochemical, physiological and ecological monitoring on the same species not the fragmented and competing approaches that seem to be the rule today.

Buchanan, J. B., Sheader, M. & Kingston, P. F. (1978). Sources of variability in the benthic macrofauna off the south Northumberland coast, 1971-76.J. mar. biol. Ass. U.K., 58, 191-210. Gray,J. S. (1979).Pollutioninducedchangesin populations.Phil. Trans. R. Soc. Ser. B., 286,545-561. Gray, J. S. & Mirza, F. B. (1979).A possiblemethod for the detectionof pollution-induced disturbance on marine benthic communities. Mar. Pollut. Bull., 10,142-146.

Marine Pollution Bulletin, Vol. 11, pp. 65-68 © Pergamon Press Ltd. 1980. Printed in Great Britain.

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Dissolved Petroleum Hydrocarbons in some Regions of the Northern Indian Ocean R. SEN GUPTA, S. Z. QASIM, S. P. FONDEKAR and R. S. TOPGI National Institute o f Oceanography, D o n a Paula, Goa 403 004, India

Dissolved petroleum hydrocarbons were measured in some parts of the Northern Indian Ocean using UV absorbance technique with a clean up step. The concentration of oil ranged from 0.6 to 26.5 pg I_ i Higher values were recorded along the oil tanker route compared, with the coastal region From surface to about 10 m depth the oil appeared to he well mixed with water.

According to the reports of NAS (1975), the total global oil (petroleum and its products) shipped in 1971 was 1355 million tonnes (MT). Of this, 755 MT or 55.7% of the total was shipped across the Arabian Sea. From the Gulf countries, there are two main oil tanker routes through the Arabian Sea - one across the Mozambique Channel via the

South African waters to the western hemisphere and the other across the Laccadive Sea (Lakshadweep), via Sri l_anka (Ceylon), the southern Bay of Bengal and through The Malacca Strait to Far Eastern countries and Japan. The bulk of the crude is carded along the former route whereas through the latter only about 295 MT oil has been reported to be transported in 1971. In 1977, the global marine transport of oil increased to 1724 MT (B.P. Statistical Review of the World Oil Industry, 1977), thus recording an increase of 27% from 1971. In the same way, the total quantity of oil shipped across the Arabian Sea increased to 1024 MT; of which the transport to the countries in the eastern hemisphere was 334 MT. The two oil tanker routes in the Arabian Sea are of direct concern to India, as about 750-1000 tonnes of tar-like 65