Natural fluctuations of populations

ECOTOXICOLOGY

AND

ENVIRONMENTAL

Natural

SAFETY

3,190-203

Fluctuations

(1979)

of Populations1

R. SGLOVER U.K. Natural Environment Marine Environmental Received

Research Research, August

Council, Plymouth,

Institute England

for

16, 1978

INTRODUCTION For the purposes of this paper, I want to take the stance of asserting that a contaminant is not harmful unless it has an effect on wild populations or natural ecosystems. However, I shall largely ignore the effects of incidents such as the grounding of a tanker or an accidental discharge of industrial effluent. Effects from sources of this kind are often detectable with nothing more than trained eyesight and, in most cases, there is a high probability of apparent recovery at some distance in time or space from the source of contamination. Instead, I want to illustrate a difficulty which besets the task of testing the postulation that prolonged exposure to low levels of pollutants may have a significant effect on the performance of ecosystems, in terms of organic production or the abundance, distribution, and composition of communities of animals and plants. The basic task and its fundamental difficulty are obvious: It is the problem of distinguishing changes which are the products of man’s intervention from those which reflect natural variability in populations. It is recognized, for example, that the balances between prey and predators or between primary producers and grazers are dynamic equilibria, altered by intrinsic variability within populations and ecosystems as well as by extrinsic factors such as those which arise from changes in the atmospheric climate. It is less easy than might be expected to demonstrate the patterns of natural variability because most long-term data series relate to exploited natural resources such as fish stocks, cultivated crops such as wheat or rice, husbanded animals such as cows or pigs, or hunted ones such as elephants or whales. It is always difficult, and often impossible, to detect patterns of natural variability from these data because they are subject to major fluctuations which have their origin in changing trends of human fashion or taste, in market demands which reflect financial trends, or in the development of new techniques for catching wild organisms or increasing the yield of cultivated species as, for example, through the introduction of new genetic strains or improved fertilizers. Moreover, although there is an extensive literature on phyto- and zoogeography, it is less easy to find examples of variability with time, in either abundance or * Paper presented at the Symposium of Environmental Chemicals, Vienna, 0147-6513/79/020190-14$02.00/O Copyright 8 1979 by Academic Press. Inc. All rights of reproduction in any form reserved.

on the Scientific Basis August 16-18, 1978. 190

for the Ecotoxicological

Assessment

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distribution, of natural populations. What I want to do is not very profound: I wish merely to provide some illustrations of the scale of variability in populations which are not subject to manipulation by man, for example, through exploitation, and are relatively distant from human impact through the discharge of contaminants. EXAMPLES

OF VARIABILITY

IN THE PLANKTON

I take my examples from the zooplankton of the open sea, using data from a rather unusual kind of survey, operated by merchant ships of eight nations which tow Continuous Plankton Recorders in the course of their normal work. The plankton is sampled, at a constant depth of 10 m, throughout the seasons, year after year, along 20 or more standard routes across the North Sea and in the North Atlantic from the United Kingdom to Canada, the United States, Greenland, and Iceland; for a description of the survey and methods of analysis, see Glover (1967) and Colebrook (1960). The results are used to study the patterns of distribution of more than 300 species of plants and animals (see Edinburgh Oceanographic Laboratory, 1973) and to detect and analyze variability in abundance at monthly intervals in time and 20-mile intervals in space. Although the survey started in 1930, I shall draw my illustrations from the areas of the eastern North Atlantic and North Sea which have been sampled regularly since 1948; see Fig. 1. In part, I shall bring up to date some of the results published by Glover er al. (1972). Figure 2 shows the average numbers per sample of a small but abundant copepod elongatus, in the northeastern North Sea for every crustacean, Pseudocafanus month from 1948 to 1977. The striking seasonal cycle, from low numbers in the winter to high numbers in the summer, is typical of the scale of seasonal variation in temperate latitudes. However, the seasonal cycles are superimposed on a gradual, but considerable, decline in abundance persisting over 30 years. Similar trends are apparent in the numbers of most other species of copepods and several other taxa in the zooplankton throughout the area of Fig. 1 [see, for example, Colebrook (1978)]. In Fig. 3a, which provides an extremely condensed summary of the results, the effects of the seasonal cycle have been removed by

FIG. 1. The Continuous Plankton Recorder survey, 1948- 1977: total numbers (x 10-l) of analyzed samples (left) in the standard rectangles of the seven areas (right) for which data are presented in Figs. 2, 3, and 4.

R. S. GLOVER

DATE -

FIG.

YEARS

2. Continuous Plankton Recorder survey: the abundance, elongatus (average numbers per sample) at monthly intervals in the east-central North Sea (area Cl; see Fig. 1).

at a depth of 10 m, ofPseudocalanus from January 1948 to December 1976

calculating the average abundance per sample for each year. This figure also distinguishes between results from the eastern North Atlantic (areas, C4, C5, and D5 in Fig. 1) and those from the North Sea (areas Dl, D2, Cl, and C2, combined). The numbers of copepods (all species combined) were standardized to permit the combination of results from different areas with different levels of abundance, and to facilitate the comparison between rest& from the North Atlantic and those from the North Sea. It is apparent, from Fig. ?a, that there has been a progressive decline in abundance over a period of 30 years, and that this has occurred in both sea areas. However, the zooplankton includes organisms from many other groups and numerical abundance is not necessarily the best way of summarizing events in an ecosystem. Therefore, an estimate was made of zooplankton biomass; the numbers of organisms in the principal taxa (copepods, euphausiids, hyperiid amphipods, chaetognaths, and gastropod mollusks) were multiplied by their wet weights, using the best available estimates from published records, and summed.2 No attempt 2 For studies of the dynamics of ecosystems, biomass would be expressed in dry weight (or weight or carbon) but there are fewer data for dry weights of these organisms than for wet weights. Current research at IMER is designed to examine regional and seasonal variations in dry weights of these taxa as part of a comprehensive study of the pelagic ecosystem.

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NE ATLANTIC (C4, C5, DS,)

0a

NORTH SEA (CtC2,Dl,D2,)

NUMERICAL

-2~::::::::::::::::.,:::., 50 55

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b5

m

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Ol

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OF COPEPODS

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od::::::::::::::, 1948 DATE - YEARS

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FIG. 3. Continuous Plankton Recorder survey: fluctuations in the plankton at a depth of 10 m in the northeast Atlantic (areas C4, C?, and DS combined; see Fig. 1) and the North Sea (areas Cl, C2, Dl, and D2 combined). The graphs are plotted from means for each year from 1948 to 1977; quartic trend lines are shown. the significance of the fit to the annual data being P < 0.1% with the exception of the graph for biomass in the NE Atlantic (P < 1.0%). (a) The numbers of copepods, all species combined; the results are standardized, about a mean of zero, and the scales of abundance are shown in standard deviation units. (b) An index of biomass of zooplankton; for explanation, see text.

was made to allow for regional variations in weight nor, with the exception of euphausiids, for seasonal changes. Because Continuous Plankton Recorders sample at 10 m only, and because they do not sample young stages as efficiently

R. S. GLOVER NE ATLANTIC

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FIG. 4. Continuous Plankton Recorder survey: annual and monthly fluctuations in the index of zooplankton biomass at a depth of 10 m. The contours are drawn at values of biomass index (see text) of 25, 50, and 75; there are values for every month (horizontally) in all years (vertically) from January 1948 to December 1977. Results for the NE Atlantic, on the left, represent the combination of data from areas C4, C5, and D5 (see Fig. 1) and, for the North Sea, on the right, from areas Cl, C2, Dl, and D2 combined.

as adults, these estimates cannot be regarded as “total biomass” in the strict sense. However, they are indicators of fluctuations in biomass with time, comparable within the CPR survey data. The scales of the graphs in Fig. 3b, and the contour values in Fig. 4, therefore, should be regarded as arbitrary units of a “biomass index.” Despite the crudity of the method used to obtain them, the results in Fig. 3b provide a clear indication of a systematic decline in the biomass of the standing stock of zooplankton at 10 m depth in the North Sea as well as that of the eastern North Atlantic. Another illustration of the complexity of variability, between and within years, is provided in Fig. 4 which shows the values of the biomass index, by months, over the full 30 years of the survey. The seasonal cycle is the most striking and

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persistent feature but there is considerable variability between years, not only in the timing of the seasonal cycle, but also in the levels of biomass achieved at the seasonal peak of biological activity. Nevertheless, the long-term trends summarized in graphical form in Fig. 3b are discernible and, as in those graphs, there are some signs of a reversal in the trends, especially in the North Sea. Long-term trends have also been detected in the phytoplankton [see Glover et al. (1972)]; Reid (1975, 1977) has suggested that numbers of naked flagellates in the North Sea have increased progressively while those of diatoms have decreased. There have also been changes in the geographical distribution of several organisms, including a progressive southerly shift of the planktonic larvae of blue whiting (a fish which is subject to very little commercial exploitation) over deep water to the west of Scotland and Ireland (Bainbridge and Cooper, 1973). A simple illustration of the scale of such changes is provided by Fig. 5. Stomias boa is a small oceanic fish of no commercial importance whose larvae appear in the Plankton Recorder samples; prior to 1968, it was found only over deep water in the open Atlantic but since then it has shifted southward and now occurs over the shallow water of the Celtic Sea and English Channel. INTERPRETATION Obviously, the processes which influence the distribution and abundance of pelagic organisms are such things as growth, fecundity, natural mortality, predation, grazing, migration, and passive transport. It is known that these aspects of performance of organisms are controlled by factors such as sunlight, temperature, salinity, nutrients, and the patterns of the major current systems; to these we should add some of the contaminants, including metallic ions, organochlorines, and petroleum hydrocarbons which are known, from laboratory experiments, to

FIG. 5. Continuous Plankton Records: larvae of Stomias boaferox at a depth of 10 m. The symbols show the presence of larvae in the standard survey rectangles (2” long. by 1” lat.). The boundaries of the sampled area are shown by a line round the limits of the standard rectangles. Redrawn, and brought up to date, from Coombs (1975).

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affect the performance of organisms. But, with the exception of temperature and some aspects of the atmospheric climate, there are no long-term records of these factors in the sea-or none with adequate discrimination and coverage in space and time. For the time being, therefore, attempts to identify factors which are responsible for observed patterns of variability, such as those shown in Figs. 3, 4, and 5, must be based on empirical correlations with those few environmental variables which are sufficiently well documented. The danger, in the context of ecotoxicology, is that any fairly linear trends, such as those illustrated here, could be correlated with almost any activity of man because man’s activities tend to change in a progressive, persistent, or cumulative manner. This is not the place for a detailed account of the research into these topics which is now under way, using the techniques of multivariate statistics and simulation modeling. The changes in the plankton are apparent over a very wide area, affecting many organisms in different taxa. This suggests that we should consider the possibility that they reflect major trends in the oceanic or atmospheric climate, perhaps affecting the whole northern hemisphere. Taylor (1978) and Colebrook (1978) have argued that these trends in the abundance of the zooplankton during the past 2 or 3 decades are related to variability in surface temperatures in the North Atlantic, derived from changes in the strength of the trade and westerly winds through a shift in the North Atlantic current system involving, among other things, changes in the separation of the Gulf Stream from the North American coast, and reflected also in the variations in the position of the northern ice-edge. Southwood er al. (1975) and Dickson et al. (1975) have also related biological changes in the English Channel and North Atlantic to climatic changes. We have to consider the possibility, also, that the variability in the plankton may have a cyclic element. The fitted curves in Fig. 3 do indeed suggest that the trend of declining abundance, in the North Sea at least, has been halted and, perhaps, reversed in recent years. However, straight lines fit the data with about the same level of significance, and, obviously, survey monitoring will be required for several decades to discover whether there will be complete recovery and whether there is a pattern of variability, following a regular or irregular cycle. Colebrook (1976) has drawn attention to trends and cycles in the climate of the North Atlantic Ocean over the past 100 years or so; they are apparent in surface water temperature, the strength of flow of the Gulf Stream, and the frequencies of tropical cyclones which are related to atmospheric circulation over the North Atlantic. Both he and Muir (1977) raised the possibility that a lo- to 11-year cycle in the data might be related to the sunspot cycle. Colebrook (1979) has also detected a 2- to 25year cycle in the plankton data and he has shown that this cycle, as well as the long-term trend, is apparent also in the stratospheric temperatures over Europe [data from Schwentek (1977)]. These findings demonstrate a quandary in this type of research; there is no known mechanism by which sunspots or stratospheric temperatures exert a direct effect on the zooplankton; the correlation of trends and cycles may well be coincidental. However, correlations of this kind may help to narrow down the search for causative mechanisms.

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All we can say at present is that there does appear to be a rational chain of links, from the trade and westerly winds, the changing current system, and the resulting effects on water temperatures, to the variability of the plankton with time. THE QUANDARY The primary lesson to be learned from all this is that there are major systematic trends and, probably, cycles in the long-term patterns of variability of natural populations in an ecosystem which is somewhat distant from, but not necessarily unaffected by, man’s intervention. The persistence of the trends, and their occurrence over such a wide area, give grounds for conjecture that similar fluctuations are probably to be found in populations of estuarine, freshwater, and terrestrial ecosystems, including cultivated crops and husbanded animals. The problems of interpreting the data will not be solved easily or quickly. One of the most promising approaches is simulation modeling of whole ecosystems but models of general application are not yet available, although some models of particular ecosystems, especially in estuaries, are in an advanced state [see, for example, Longhurst (1978); Kremer and Nixon (1978)]; some of these models may be manipulated to examine the possible effects on an ecosystem of proposals for the introduction of contaminants, such as hot water from power stations, or environmental engineering, such as a barrage across an estuary. Until such models are more generally available, the task of predicting variability, whether from natural or anthropogenic sources, will be largely a matter of subjective judgment (or informed guesswork). Another lesson to be learned from these examples is that field monitoring programs are required over very long periods of time and that these programs must include more systematic monitoring of environmental variables, including anthropogenic materials, than has been customary in the past. I might add that this kind of data acquisition is essential, also, for developing and validating simulation models. However, until we do have predictive models, monitoring of this kind will only reveal the effects of natural variability, and any changes resulting from man’s activities, long after the events which gave rise to them. Research and monitoring in these fields is essential for understanding the sources and pathways of processes which affect populations but, until our repertoire of examples and experience has become more extensive than it is today, such research will contribute rather slowly to the formulation of environmental management decisions-or at least to the taking of decisions in advance, designed to prevent possible deleterious effects. AN ALTERNATIVE

APPROACH

For many aspects of environmental management we need immediate indications, rather than historical evidence, of the biological effects of environmental change. In the search for faster methods of detection it seems sensible to start from the proposition that variability in the abundance of populations is the product of systematic changes in the performance of individual plants and animals and, espe-

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cially, changes in growth, reproduction, and mortality, all of which can be investigated and measured in terms, for example, of physiology and biochemistry. I want to end this paper, therefore, with a brief outline of work in these fields, in my own institute, designed to investigate some. of the mechanisms of ecological variability and, particularly, those resulting from environmental changes. Of course, there is nothing new in the concept of dose-response experiments or in the use of living organisms in bioassays of environmental quality. What is new is the refinement of techniques in recent years, particularly in the investigation of effects which are likely to have ecological consequences, and their detection at the very low levels of contaminants which occur in nature. The techniques also lend themselves to the instantaneous monitoring of performance over extended periods of time, as distinct from the historical monitoring of population numbers. Much of the work has been carried out on the common mussel, Mytifus edulis, which is very widely distributed around coasts and estuaries. Its seasonal and annual patterns of growth, feeding, and reproduction, and its principal physiological and biochemical processes, are relatively well known and recent research has revealed the ways in which the rates and pathways of some of these processes change, with detrimental consequences, when the animal is subjected to stress. The objective of the program at IMER, therefore, is to explore the extent to which these rates and pathways can be quantified as indices of condition (of the animals) which could be used as indicators of environmental stress including the presence of contaminants. An essential feature of the work is the evaluation of stress indexes against the known pattern of physiological and biochemical variability which reflects seasonal cycles and annual development. Among the topics which are being investigated are an index of blood sugar, gas exchange efficiency (related to the functioning and morphology of gill tissues), the ratio of aspartate:glutamate as an index of anaerobiosis, and the ratio of taurine:glycine (especially responsive to thermal stress), as well as more general indexes such as growth efficiency, fecundity, and larval quality. A particularly useful index is the ratio of oxygen intake to nitrogen excretion; this reflects the balance between the catabolism of protein, carbohydrate and lipid and is disturbed by stress, such as starvation or extreme temperatures, as well as pollutants [see Widdows (1978)]. An extremely useful ecological index is the “scope for growth” [see Bayne (1975)]; this is the difference between energy intake, as food, and the total energy used or lost in all processes other than growth. In oversimplified terms, it is calculated from measurements, in the field or laboratory, of food consumption and energy losses via feces and respiration. It is highly sensitive to variations in environmental quality and is being used to compare water quality in different sites and to monitor changes over a period of time in a single population (Bayne et al., in press). Gilfillan et al. (1976, 1977) used a similar technique on another bivalve, Myu arena&z, and found a 50% reduction of growth potential in animals from a population exposed to oil compared with those from an unpolluted site. Indexes of this kind may also be used in tests of water quality by transplanting animals, drawn from one population, to several sites under evaluation. Dr. J. Widdows of IMER, in collaboration with American colleagues, exploited this approach in Narragansett Bay. Mussels from the mouth of the bay were transferred in baskets

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to four sites representing a pollution gradient down the bay; after 30-40 days the mussels were recovered for measurements in the laboratory of the scope for growth. The results reflected the pollution gradient precisely with minimum scope for growth at the most polluted site and the maximum in a control sample which had been kept in clean laboratory conditions (Bayne et al., in press). One aspect of this research on stress and pollution has been the detection of the effects of stress within cells of the digestive gland of Myths. Cellular organelles, the lysosomes, are capable of releasing enzymes which digest cytoplasm; under “normal” conditions, the enzymes are latent but if the lysosomal membranes become unstable hydrolases are released, causing autolysis of cellular components. Moore (1976) has shown that the free enzyme activity can be measured precisely by staining techniques; when the scope for growth is negative, there is a marked release of hydrolases into the cytoplasm. Lysosomal destabilization occurs in Myths as a result of exposure to high temperatures (Moore, 1976), combined nutritional and thermal stress (Bayne et al., 1976), and aromatic hydrocarbons (Moore et al., 1978). The value of this, and related work on histochemical methods, is that the techniques are relatively simple, the response of the animals is detectable very shortly after exposure to stress, the range of natural variability within a population is smaller at the cellular level than at the “whole animal” level, and all the evidence so far suggests that these cytological and biochemical responses are extremely sensitive to environmental variability. The intention is to develop a suite of indexes of condition of the animals which can be applied to assessing water quality. A monitoring feasibility study has been carried out for more than a year at seven sites in the United Kingdom, selected to represent a range of environmental conditions, and is continuing at a smaller number of sites, including the vicinity of a major oil terminal. For this work, a minibus has been converted into a mobile laboratory so that disturbance of the animals is minimized and the measurements are made under local ambient conditions of water temperature, salinity, and suspended particulate matter. At the same time, laboratory studies are continuing in order to refine the techniques and investigate responses to particular contaminants. Studies of the effects of water-soluble extracts of North Sea crude oil have revealed biochemical and physiological responses at concentrations as low as 20 ppb; among the effects are an increase in oxygen consumption, with a consequent reduction of the scope for growth, an increase of protein catabolism, so that free amino acids are excreted, and lysosomal changes (B. L. Bayne, J. Widdows, and M. N. Moore, personal communication). A mixed-function oxygenase system is known to function in many animals as a means of metabolizing foreign compounds, including hydrocarbons. Recent work at IMER suggests that there is a similar system in Myths; increased enzyme activity is detectable after mussels have been exposed to water soluble extracts of North Sea crude oil at a dilution of 60 ppb (J. Widdows, personal communication; Bayne et al., in press). A related aspect of the same program is concerned with the use of a sessile colonial hydroid, Campanularia~exuosa, as a bioassay organism (Stebbing, 1976, in press). The hydroids are allowed to grow in the laboratory over a period of about 11 days in water from selected sites. The response of the hydroids may

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be measured in terms of growth (by counting the members of each colony), production of gonozooids, and the curvature of the stolon from which the members of the colony branch off (the stolon branches are normally straight but curve in an anticlockwise direction when exposed to inhibitory agents). All of these measures of performance show clear responses to exposure to metallic contaminants at low concentrations. For example, in sea water to which CuCl, has been added, the growth rate declines sharply and linearly at concentrations of Cu over 10 pg/liter, the numbers of gonozooids reach a maximum at 0.1 pg/liter before falling linearly with increasing concentration of Cu, and the frequency of curved stolons increases from 5 &liter of copper to a maximum at 20 ,ug/liter above which there is an approach to lethal conditions. Although the investigations are incomplete, the detection of free lysosomal hydrolase appears to offer the means 220

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FIG. 6. Bioassay with Companulurinflexuosa. The graphs show the results of experiments in which transplants of the hydroid were maintained for 11 days in seawater to which various levels of Cu*+ had been added. The broken line shows an index of activity of lysosomal hydrolase. The solid line shows the effect on growth, assessed by counting the colony members. In both cases the results are expressed as percentages of the results from controls maintained in seawater to which copper had not been added. Vertical bars mark standard errors (seven replicates at each point). Redrawn from Moore and Stebbing (1976).

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of refining this hydroid bioassay technique. Histological staining for these enzymes reveals response thresholds (depending on the metallic ion being tested) one or two orders of magnitude lower than those determined by measurement of growth of the colonies (Moore and Stebbing, 1976). Figure 6 shows the effect of Cu to which the lysosomal enzyme test was sensitive at about 1.0 pg/liter; this compares with concentrations in Swansea Bay, near an industrialized area of South Wales, reaching about 5.5 Fg/liter. Thus it seems likely that bioassay with colonial hydroids is capable of fulfilling the twin requirements for such tests: (a) that it is capable of revealing effects which have an ecological consequence, and (b) that it is sensitive at the levels of dilution of contaminants which occur in nature. However, these results, like most of the biochemical and physiological investigations of Mytilus, reveal the responses of the organisms to water quality in general terms; they do not necessarily identify the contaminant. Some work now under way is designed to examine the possibility of selective removal of contaminants from seawater samples. Ion exchange resins can be used to remove metallic ions; for example, water from Swansea Bay caused stolon bending in the hydroid bioassay but the response was reduced if the water was passed through Chelex-100 ion exchange resin (Stebbing, in press). The problem of assessing water quality is compounded by the fact that methods of analytical chemistry are sensitive at very great dilutions of contaminants but, until recently, we have lacked the means of determining the lower levels at which contaminants have a deleterious ecological effect (and I started this paper by asserting that a contaminant is harmful only when it does have an effect). But it is not just a question of levels of concentration; the form in which chemical constituents are bound and the presence together of materials which have synergistic effects are also crucial in determining the impact of contaminants on populations; chemical data do not necessarily indicate the biological availability of contaminants. It is well known, for example, that copper is less toxic when it is complexed by organic compounds; in an experiment with Campanularia , the effect of copper on growth was increased by 30% following photo-oxidation which destroys the capacity of organic matter to complex metals (Stebbing, in press). CONCLUDING

REMARKS

In the context of ecotoxicology, the monitoring of population numbers and of environmental chemicals are fraught with difficulties arising from the complexity of natural variability and from uncertainties about the relevance of conventional analytical chemical data in terms of biological effects on populations and production. There is a need for a more enlightened attitude toward environmental monitoring and there are grounds for believing that this could be achieved through techniques for instantaneous monitoring of biological performance. The case was made strongly, and with much supporting evidence, by a working group of the International Council for the Exploration of the Sea (ICES, 1978) which “considered that the possibilities of biological effects monitoring have not been fully explored.” The working group’s proposals for further research, like the few brief examples I have given in this paper, suggest that powerful team effort is needed-

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a carefully planned liaison of ecologists, biochemists, and cytologists.

experimental

biologists,

physiologists,

ACKNOWLEDGMENTS This paper draws extensively on research in the Institute for Marine Environmental Research which is a component of the U.K. Natural Environmental Research Council. The work has been funded by the Development Commission and NERC, and commissioned in part by the U.S. Department of the Navy, Office of Naval Research (Contracts N62558-2834/3612 and F61052-67C-0091), the Ministry of Agriculture, Fisheries and Food, the Department of the Environment (Contracts DGR 480/47 and DGR 480/288), and the European Economic Community (Contract 279-77-4 ENV UK).

REFERENCES BAINBRIDGE, V., AND COOPER, G. A. (1973). The distribution and abundance of the larvae of the blue whiting, Micromesistius poutassou (Risso) in the north-east Atlantic, 1948-1970. Bull. Mar. Ecol. 8, 99- 114. BAYNE, B. L. (1975). Aspects of physiological condition in Myrilus edulis L., with special reference to the effects of oxygen tension and salinity. In Proceedings of the 9th European Marine Biology Symposium (H. Barnes, ed.), pp. 213-238. Aberdeen Univ. Press. BAYNE, B. L., LIVINGSTONE, D. R., MOORE, M. N., AND WIDDOWS, J. (1976). A cytochemical and a biochemical index of stress in Mytilus edulis L. Mar. Pollut. Bull. 7, 221-224. BAYNE, B. L., MOORE, M. N., WIDDOWS, J., LIVINGSTONE, D. R., AND SALKELD, P. Measurement of the responses of individuals to environmental stress and pollution; studies with bivalve molluscs. Phil. Trans. R. Sot. London B. 1015, in press. COLEBROOK, J. M. (1960). Continuous plankton records: Methods of analysis, 1950-1959. Bull. Mar. Ecol. 5, 51-64. COLEBROOK, J. M. (1976). Trends in the climate of the North Atlantic over the past century. Nature (London)

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COLEBROOK, J. M. (1978). Continuous plankton records: Zooplankton and environment, North-east Atlantic and North Sea, 1948-1975. Oceanol. Acta 1, 9-22. COLEBROOK, J. M. (1979) Continuous plankton records: Monitoring the plankton of the North Atlantic and the North Sea. In Monitoring the Marine Environment (D. Nichols, ed.), Symp. Inst. Biol. 24. COOMBS, S. H. (1975). Continuous plankton records show fluctuations in larval fish abundance during 1948- 1972. Nature (London) 258, 134- 136. DICKSON, R. R., LAMB, H. H., MALMBERG, S. A., AND COLEBROOK, J. M. (1975). Climatic reversal in the northern North Atlantic. Nature (London) 256, 479-482. EDINBURGH OCEANOGRAPHIC LABORATORY (1973). Continuous plankton records: A plankton atlas of the North Atlantic and the North Sea. Bull. Mar. Ecol. 7, I-174. GILFILLAN, E. S., MAYO, D., HANSON, S., DONOVAN, D., AND JIANG, L. C. (1976). Reduction in carbon flux in Mya arenaria caused by a spill of No. 6 fuel oil. Mar. Biol. 37, 115-123. GILFILLAN, E. S., MAYO, D., PAGE, D. S., DONOVAN, D., AND HANSON, S. (1977). Effects of varying concentrations of petroleum hydrocarbons in sediments on carbon flux in Mya arenaria. In Physiological responses of marine biora to pollutants (F. J. Vemberget al., eds.), pp. 299-314. Academic Press, New York. GLOVER, R. S. (1967). The continuous plankton recorder survey of the North Atlantic. Symp. Zool. Sot. London 19, 189-210. GLOVER, R. S., ROBINSON, G. A., AND COLEBROOK, J. (1972). Plankton in the North Atlantic-An example of the problems of analysing variability in the environment. In Marine Pollution and Sea Life (M. Ruivo, ed.), pp. 439-445. Fishing News Books for FAO, Rome. ICES (1978). On the feasibility of effects monitoring. Cons. Int. Explor. Mer. Cooperative Research Report No. 75. KREMER, J. N., AND NIXON, S. W. (1978). A Coastal Marine Ecosystem. Pp. vii and 217. SpringerVerlag, Berlin/New York.

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MOORE, M. N. (1976). Cytochemical demonstration of latency of lysosomal hydrolases in digestive cells of the common mussel, Mytilus edufis. and changes induced by thermal stress. Cell Tissue Res. lx,.279-287.

MOORE, M. N., LOWE, D. M., AND FIETH, P. E. M. (1978). Lysosomal responses to experimentally injected anthracene in the digestive cells of Myrilus eduiis. Mar. Biol. 48, 297-302. MOORE, M. N., AND STEBBING, A. R. D. (1976). The quantitative cytochemical effects of three metal ions on a lysosomal hydrolase of a hydroid. J. Mar. Biol. Assoc. U.K. 56, 995-1005. MUIR, M. S. (1977). Possible solar control of North Atlantic oceanic climate. Narure (London) 266,475-476.

REID, P. C. (1975). Large scale changes in North Sea phytoplankton. Nature (London) 257,217-219. REID, P. C. (1977). Continuous plankton records: Changes in the composition and abundance of the phytoplankton of the North-eastern Atlantic Ocean and North Sea, 1958-1974. Mar. Biol. 40, 337-339.

SCHWENTEK, H. (1977). A quasi-biennial J. Interdisc.

Cycl.

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