Progress in Oceanography 58 (2003) 175–191
www.elsevier.com/locate/pocean
Use of Continuous Plankton Recorder information in support
of marine management: applications in fisheries,
environmental protection, and in the study of ecosystem
response to environmental change
K.M. Brander a,∗, R.R. Dickson b, M. Edwards c
b
a
International Council for the Exploration of the Sea, Palaegade 2–4, Copenhagen, DK-1261, Denmark
The Centre for Environment, Fisheries and Aquaculture Science, Lowestoft Laboratory, Pakefield Road, Lowestoft, NR33 0HT,
UK
c
Sir Alister Hardy Foundation for Ocean Science, The Laboratory, Citadel Hill, Plymouth, PL1 2PB, UK
Abstract
The Continuous Plankton Recorder (CPR) survey was conceived from the outset as a programme of applied research
designed to assist the fishing industry. Its survival and continuing vigour after 70 years is a testament to its utility,
which has been achieved in spite of great changes in our understanding of the marine environment and in our concerns
over how to manage it. The CPR has been superseded in several respects by other technologies, such as acoustics and
remote sensing, but it continues to provide unrivalled seasonal and geographic information about a wide range of
zooplankton and phytoplankton taxa. The value of this coverage increases with time and provides the basis for placing
recent observations into the context of long-term, large-scale variability and thus suggesting what the causes are likely
to be. Information from the CPR is used extensively in judging environmental impacts and producing quality status
reports (QSR); it has shown the distributions of fish stocks, which had not previously been exploited; it has pointed
to the extent of ungrazed phytoplankton production in the North Atlantic, which was a vital element in establishing
the importance of carbon sequestration by phytoplankton.
The CPR continues to be the principal source of large-scale, long-term information about the plankton ecosystem
of the North Atlantic. It has recently provided extensive information about the biodiversity of the plankton and about
the distribution of introduced species. It serves as a valuable example for the design of future monitoring of the marine
environment and it has been essential to the design and implementation of most North Atlantic plankton research.
 2003 Elsevier Ltd. All rights reserved.
Keywords: Continuous Plankton Recorder survey; Climate change; Marine management; Fisheries change; Eutrophication; Biodiversity; Long term
∗
Corresponding author. Tel.: +45-33154225; Fax: +45-33934215.
E-mail address: keith@ices.dk (K.M. Brander).
0079-6611/$ - see front matter  2003 Elsevier Ltd. All rights reserved.
doi:10.1016/j.pocean.2003.08.003
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Contents
1.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 176
2.
The growth of understanding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177
3.
Support for fisheries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178
4.
The issue of eutrophication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 181
5.
Biodiversity and global change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 186
6.
The role of the CPR within biological oceanography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189
1. Introduction
In the summer and autumn of 1921 and spring of 1922, an advanced multidisciplinary study in fisheries
oceanography took place in the west-central North Sea. In three issues of the ICES Publications de Circonstance (Nos. 78, 79 and 80), we read of a curiously modern attempt by Hardy (1923); Carruthers (1923)
and Lumby (1923) to explain the relative failure of the English herring fishery in that year as the joint
effect of abnormal conditions in the plankton, currents and hydrography. In the end, the attempt was almost
bound to fail. As E. S. Russell notes in his Introduction to this paper: “Conclusions as to the effects of
hydrographic conditions in any one year can be drawn with complete confidence only when the extent of
their departure from normal conditions can be determined; and the period over which regular observations
have been made in the North Sea on a large scale is at present insufficient to furnish a norm”.
The inadequacies of the data set on which the 25-year-old Hardy was compelled to depend on that
occasion—sparse tow-net hauls and no adequate baseline—do much to explain the applications for which
the CPR was subsequently conceived and justified. And the CPR was plainly an applications-led development, designed from the start to provide improved scientific support for the fishing industry. First, in his
earliest description of the ‘New Method of Plankton Research’, Hardy (1926) is concerned to resolve the
highest time-space scales of plankton variability (‘patchiness’) which were obscuring his view of largerscale and longer-term variability: “For a long time I have felt the need of an instrument which by giving
a continuous record, … would enable one to study and compare the uniformity or irregularity of planktonic
life in different areas, to measure the size, varying internal density and frequency of patches and to indicate
… whether any correlation exists between different species”. Then, 3 years later, in his Civic Week lecture
at the University College Hull, Hardy returns once more to the original aim of his 1921 study—the provision
of interpretative and predictive support for the fishing industry on the scales important to them (Hardy,
1930): “The experiment I want to make from this College consists of running a number of these instruments
on definite steamship routes across the North Sea ... When these charts are examined and the results
compared with the positions of herring shoals from year to year, we shall know whether or not we can
forecast the position of the fish from the distribution of the plankton ... These varying movements of fish
must have a definite ascertainable cause, and once ascertained, forecasting cannot be difficult”.
In seeking financial support from the Industry, Hardy was prudent enough not to promise results, yet
confident enough to suggest that “If it fails to yield useful results, it will not be science that has failed; it
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177
will be because the experiment is not big enough, bold enough, for the problem concerned”. He got his
money, though the enthusiasm of the Hull Fishing Vessel Owners Association was expressed no bolder
than £100 per year, with £50 from the Fishmongers’ Company.
By the time the first of the familiar ‘Hull Bulletins’ began to appear in 1939, his focus was firmly and
appropriately on the largest scales of variability, using the technique to develop a baseline against which
anomalies in plankton distribution and abundance might be recognised and explained. “The similarity of
the methods to those of meteorology has already been stressed: we are aiming at producing, month by
month, charts of the broad changes in the distribution of the more important plankton forms. It is then our
aim to correlate these changes with the fluctuations in the fisheries, both the drift-net herring fisheries and
the trawl fisheries, and also with hydrological and climatic changes. The correlation with the herring fisheries was one of the first economic results that was expected from such a survey ”. (Hardy, 1939:6).
Hardy was clearly far ahead of his time in realising the significance of spatial differences in the kinds
and abundance of plankton and in devising the means to study them. As Platt and Stuart (1997) remind
us: “Until the advent of satellite remote sensing, the CPR provided the only means of collecting plankton
data at large spatial scales: it was the remote sensing of the day. Further, by recognising [from an overflight
of the English Channel from Plymouth to the western mackerel grounds in the early 1920s] that colour
differences in the ocean contained important biological information that could be surveyed rapidly with
aircraft … he became a true pioneer of remotely-sensed ocean-colour science”.
However, although enthusiasm, optimism and foresight can initiate concepts, they can rarely sustain
them. Duarte, Cebrian and Marba (1992) show that: “long-term monitoring programs are, paradoxically,
among the shortest projects in marine science: many are initiated but few survive a decade”. As Grove
(1992) concludes in his review of the ‘Origins of Western Environmentalism’, survival comes with utility:
“If a single lesson can be drawn from the early history of conservation, it is that states will act to prevent
environmental degradation only when their economic interests are shown to be directly threatened. Philosophical ideas, indigenous knowledge and people and species are, unfortunately, not enough to precipitate
such decisions”.
The implication is clear: that to survive for seven decades, the CPR dataset must have had some continuing utility for marine resource management or policy. In the remainder of this chapter we aim to describe
both our increasing understanding of variability in the marine ecosystem with time as the CPR record has
lengthened and the changing preoccupations that have justified its continued survival. Four main applications develop with time: the issues of fisheries, eutrophication, biodiversity and global change.
2. The growth of understanding
It is increasingly difficult to fund long period measurements. The quotation above from Duarte et al.
(1992) still applies. One reason for this may be the mistaken perception of ‘diminishing returns’ from
long-term monitoring and it is worth making the case that there is in fact an increasingly valuable and
complex scientific return with time.
When the major papers based on the CPR record are classified by type and date (arrowed in Fig. 1),
we find that the elaboration of our understanding of the Atlantic plankton and its ecosystem grows steadily
with time. Initially, these papers provide description. Then the samples become adequate to contribute to
the systematics of the plankton; then successively to comment on variability at increasing time scales, from
seasonal change through seasonal dynamics to interannual change and lastly to ecosystem change, involving
a complex of variability across decades and trophic levels. Papers anticipating the planktonic signature of
global change have begun to appear. Thus, over seven decades, the value of the time series has grown in
terms of the breadth of understanding that we can mine from it.
It is as well that it is so. As Fig. 2 also shows, the management issues supported by these data have
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Fig. 1. Types of scientific understanding dealt with by papers written about the CPR. Based on the post-war bibliography by Dickson
(1995).
Fig. 2.
Management issues become more complex.
also become more elaborate and complex with time as a range of actual or potential anthropogenic impacts
begin to affect our thinking. In each case, the requirement has been—in advance of their onset—to anticipate
the likely chain of responses that will arise through the marine environment and its ecosystem, to deploy
unambiguous and practical means of detecting these impacts, and to develop appropriate policies for managing them. To develop such criteria and policies in ignorance of the ‘natural’ envelope of variability in both
the ecosystem and its environment is to risk implementing measures that are costly and do not work.
The longest time series give us access to the broadest spectrum of ocean variability. That, in short, is
why a 70-year record of the planktonic ecosystem is of importance and why its value has increased with
time. The following sections are intended to illustrate this point.
3. Support for fisheries
Hardy’s aim in setting up the CPR survey was to provide a service, similar to that provided by meteorologists for the atmosphere, which would enable fishermen to locate their target species and eventually have
some predictive capability. He was a realist and he recognised that this would be a long haul:
It must take many years before we have enough knowledge of this changing plankton to establish what
may be considered the normal state of distribution for any one time of year; only when this has been
done can we see in which particular ways the different years have been abnormal. Not until then can
we safely think of trying to predict the effects of such changes on a fishery.
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179
The aim of providing fishermen with operational information from the CPR to locate target species and
improve their catches has not been realised in the way in which Hardy intended, or rather it has not been
attempted for several reasons. For one thing the time lag between sampling by the CPR and the availability
of the information makes short-term application impossible. For another, new technologies, particularly
acoustics, proved to be highly effective for real-time location and tracking of herring shoals. These techniques have made fishing operations for pelagic species, such as herring, so efficient, that there is far more
concern now about how to restrain catches than enhance them.
The CPR has however proved useful in locating significant fishery resources, e.g. blue whiting, which
have subsequently been explored and developed. The CPR showed the location of the blue whiting stock
west of the British Isles (Fig. 3) at a time when only Spain recorded any landings of blue whiting and
these were from areas south of 52°N (average 13,500 tonnes from 1958–1966). After 1967 the international
fishery increased to over one million tonnes in 1979–1980 (average 465,400 tonnes from 1967–1998).
Another example is the redfish stocks in the Irminger Sea (Henderson, 1964b).
The utility of surveying plankton was based not only on what it was expected to reveal about the
distributions of zooplankton and their fish predators, but also on the insight it would give into the dynamics
of lower levels of the food chain leading to fish, with the expectation that changes in plankton production
must have consequences for the higher trophic levels. Hardy’s investigations resulted in a very detailed
Fig. 3. Average distribution of early life stages of blue whiting Micromesistius poutassou March–May 1948–1962. Dots indicate
absence; crosses are numbers up to 0.1 m⫺3; circles are numbers up to 0.3, 1.0 and over 1.0 m⫺3 successively. From Henderson
(1964a).
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and complex food web for herring (Fig. 4) and now, with a 60-year time series of variability in both the
herring stock and their major prey items, we can see remarkable correlations between them (Reid, Battle,
Batten, & Brander, 2000). The rich detail of processes and interactions between all the components of the
food chain and the influence of physical and biological factors at many stages make it difficult to distinguish
between possible and actual causal relationships that give rise to the observed correlations between fish
and plankton. Even the basic question of whether correlations between predators and prey demonstrate
top-down or bottom-up control cannot be resolved unequivocally (Reid, Battle, Batten & Brander, 2000)
and both types of control probably occur at different times and ecosystem states.
The CPR has provided immensely valuable information concerning the scale and nature of the processes
affecting fish stocks. One of the first attempts to analyse the large-scale impact of environmental change
on seasonal and interannual patterns of biological variability in the North Atlantic (Garrod & Colebrook,
1978) concluded:
Convincing as these are, the mechanisms of the link between climatic/hydrographic changes and their
biological effects has in most cases, yet to be established. This paper does not come any closer to
defining such links but shows that similar variation in plankton and fish communities are contemporary
and on a geographic scale which suggests a common origin in pan-Atlantic environmental effects rather
than in strictly localized phenomena.
Subsequent analysis of the spatial scales of variability in cod (e.g. Myers, Mertz, & Barrowman, 1995)
confirms the importance of this work and many recent studies (e.g. Corten, 1998; Fogarty, Myers and
Bowen, 2001; Ottersen, Planque, Belgrano, Post, Reid and Stenseth, 2001; Brander, in press) have confirmed the conclusion concerning large-scale geographic pattern. We continue to study the processes and
to develop tools for making use of the information about large-scale variability in relation to fisheries management.
CPR data have been applied in many specific studies of recruitment variability, with results, which are
Fig. 4.
The food web of herring Clupea harengus. From Hardy (1924).
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181
tantalising, encouraging, but so far incomplete. For example, Cushing (1984) tested the match–mismatch
hypothesis on North Sea cod, using data on Calanus in the NE North Sea from the CPR survey to show
both the interannual variability in abundance and also in the timing of spring production. He obtained a
significant correlation between number of cod recruits and Calanus timing and abundance, but the relationship did not hold up in a later analysis (Brander, 1992) using more years and more information on Calanus.
The relationship being modelled here may be fundamentally correct, but it depicts only a part of the
dynamics needed for adequate representation of Calanus variability. Other case studies have shown both
positive and negative relationships between zooplankton abundance from the CPR and recruitment of cod,
haddock and herring (Drinkwater, Frank, & Petrie, 2000; Reid, Battle, Batten & Brander, 2000). Thus
empirical analyses and biological reasoning give us good grounds for expecting that the information from
the CPR will become useful in understanding and assessing variability in fish stocks, but it is not clear
whether the utility will derive mainly from the long-term, large-scale overview of ecological ‘regime shifts’
which it provides, or from direct operational application at short time scales for improved year-to-year
forecasting (Brander, in press).
Fisheries management has become more concerned about the impact of fishing on the marine ecosystem
as a whole and this is now articulated in the FAO Code of Conduct for Responsible Fisheries and in
numerous ministerial declarations about future fisheries policy. Turning this general concern into an operational process, with measurable indicators, against which progress towards ecological objectives and compliance with statutory instruments can be measured, is by no means simple. It is evident that plankton is
a key part of the marine ecosystem in this respect, since trophic calculations show that the fish removed
by fisheries consume a very significant proportion of the production of phytoplankton and zooplankton
(Pauly & Christensen, 1995) and that fisheries therefore have a major impact on plankton (Reid, Battle,
Batten & Brander, 2000). Quantifying this effect, providing observational evidence, evaluating whether the
effects are deleterious and designing procedures for mitigating such effects are in their infancy. Here the
CPR has a special role to play, not least because it provides a unique example of the problems and payoffs which such a spatially, temporally and taxonomically detailed time series gives rise to. The rationale,
history and operation of the CPR over 70 years provides many useful lessons for the design of any future
monitoring which is intended to provide ecosystem indicators.
4. The issue of eutrophication
The early 1970s saw the beginning of a series of measures on either side of the Atlantic designed to
detect the potential eutrophication of coastal seas. In the US, the Clean Water Act has included such
responsibilities since 1972. In waters of the European Community, the health of our coastal seas has been
regulated through a series of Directives [Surface Water Directive (1975), Dangerous Substances Directive
(1976), Shellfish Waters Directive (1979), Urban Waste Water Directive (1991), and Nitrate Directive
(1991)], many of which assign responsibilities for the nutrient status of our seas, the nutrient inputs to
these seas or the activities and practices that give rise to them. From December 2003, a new Water Framework Directive will begin the process of rationalising, modernising and in some cases replacing the existing
regulatory structure. Yet the common thread of assessing the nutrient balance and eutrophic status of our
coastal waters will remain a fundamental issue for the science and policy that underpin marine management.
By the end of 2002, for example, the eutrophication status of all parts of the OSPAR Maritime Area has
to be established using the OSPAR ‘Common Procedure’. However as the QSR (OSPAR, 2000) states
“The situation concerning nutrients and associated eutrophication effects is rather complex”.
Though the concept of eutrophication may seem clear enough, a consensus definition has proved elusive.
That adopted by the QSR of the 1987 Ministerial North Sea Conference might seem unexceptionable: “the
process of enrichment of sea water with nutrients, especially of nitrogen and phosphorus, leading to
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increased production of phytoplankton”. Yet the Urban Waste Water Treatment Directive of 1991 adds
the idea also that eutrophication must imply some undesirable change, thus making a clear distinction
between a cause—nutrient enrichment (not in itself an ecological problem)—an effect—increased plant
growth—and a consequence—some undesirable change in organisms or water quality. Much the same
definition was adopted by OSPAR in 1998.
Developing agreement on whether particular areas of shelf are actually or potentially eutrophic is, of
course, the vital point and in the absence of any direct measure, nations have differed as to which proxy
criteria might be appropriate to determine the issue. Possible criteria on the input side include increase in
nutrient inputs or increase in nutrient concentrations in coastal waters. On the uptake or effects side, they
include exceptional algal blooms, oxygen deficiency, fish and shellfish kills, changes in macrophyte growth,
scum on beaches, etc. However, although these considerations are not irrelevant to the problem, they (or
any similar mix) suffer two main defects. First they may arise from ‘natural’ as well as anthropogenic
causes. Second, even as proxies, their space–time resolution tends to be poor, weighted towards observations in particular rivers or at isolated points around the ocean margin.
Thus we have a situation where (to quote Longhurst, Colebrook, Gulland, Le Brasseur & Smith, 1972)
“Man’s chemical invasion of the ocean does, we believe, pose a real threat to marine life despite the great
volume of the oceans, despite their chemical buffering systems, and despite the probable elasticity of their
complex food webs”; where, accordingly, we have introduced a regulatory framework to guard against the
undesirable types of change in the marine ecosystem or its environment that fit our definition of ‘eutrophication’. Whereas the penalties for non-compliance are real enough, e.g. the large cost of moving to tertiary
treatment (nutrient stripping) to restore normal water status under the Urban Waste Water Directive, or
the imposition of Good Agricultural Practice where nitrate-vulnerable zones are defined, but where, in
the changeable waters of our estuaries, coast and shelf, almost any of the defining criteria may have
arisen naturally.
In such a situation, if ambiguity and contention are not to be perpetuated, the need is as much for the
long time series that will resolve the natural space—time variability of the shelf and its ecosystem as for
the inventories and trends of anthropogenic inputs. Longhurst et al. (1972) reached this conclusion three
decades ago in their review of ‘The instability of ocean populations’: “This review demonstrates several
basic principles that have to be understood if man is to measure his influence on the ocean environment.
Perhaps most important, it is evident that the ocean is a restless and changing environment and that its
changes may either be sudden and dramatic, or covert and sustained for very long periods; it is also obvious
that, by their nature, these changes can only be revealed and measured by deliberately mounted and wellsustained ocean monitoring operations. ... there seems to be a real lack of understanding that pollution
monitoring schemes, in the ocean or elsewhere, can only succeed if the natural effects of the changing
physical environment are both understood and monitored continuously and indefinitely. Natural fluctuations
in animal populations have already been ascribed incorrectly to the effects of pollutants, and it would be
easy for a serious impact on the environment to pass unnoticed through ignorance of natural population
instability or a lack of monitoring...”.
This quotation neatly explains the special nature of the CPR contribution to the eutrophication debate.
Though still a proxy and still a partial measure (limited, for example, in its fixed-depth coverage; myopic
in the near-shore zone; partial in not recording elements of the micro- and macro-plankton), the CPR
dataset is nonetheless unique in its length of record, in its (largely) unchanging technique, in its monthly
time-resolution, in its full ocean coverage, in the spatial resolution of that coverage (18.5 km of tow, but
traditionally aggregated into 1° × 2° rectangles) and in its ecological scope (over 400 separate planktonic
species or entities recorded). The fact that the new Water Framework Directive will draw a particular focus
on the issue of ‘good ecological quality’ can only enhance the value of its contribution even though this
criterion will initially be restricted to the near-shore zone.
Once again it is worth stressing that the CPR data set cannot referee the eutrophication debate, but it
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can most usefully help to tip a balance of probabilities. Two examples, one general, one more specific,
will illustrate these capabilities in action.
The first, one of the clearest and most useful conclusions from the entire CPR programme, was instrumental in persuading UK government departments of the value of continuing to fund the survey in the late
1980s, when its existence was threatened. The result was a simple one, namely that a single long-term
trend of zooplankton abundance has affected all areas of the eastern Atlantic and European shelf since
1948, but it represents the painstaking distillation by the CPR team, of thousands of route-miles of tow
over four decades. This result is illustrated in Fig. 5 for a single band of latitudes from Rockall to the
German Bight. The full result is described by Colebrook (1986), augmented with data on seabird abundance
by Colebrook (1989) and is the basis for the first description of parallel long-term trends across four trophic
levels by Aebischer, Coulson and Colebrook (1990).
Since this long-period change was found to be present, with variations, in all 12 CPR Standard Areas,
this was taken as a strong indication that the trend was real, not merely some artefact of the CPR method.
Since the common trend extended into the eastern Atlantic, where no significant anthropogenic influence
could be claimed, its cause was accepted to be large-scale and natural, rather than simply a local factor,
such as increased nutrient input.
We continue today to use CPR data from the eastern Atlantic as an open-ocean benchmark or point-ofreference for plankton conditions in the inner shelf. Edwards, Reid, & Planque (2001a), for example, report
a range of remarkable and widespread changes in the phytoplankton of the European shelf over the last
decade which at first sight would seem to offer clear evidence of eutrophication: a considerable increase
in phytoplankton biomass to 3–4 standard deviations above the long-term (1950–1995) mean, from CPR
Fig. 5.
Long-term trends in plankton from 1950 to 1985 for the areas outlined in bold. From Colebrook (1986).
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‘colour’ data; a change in the timing of primary production, with many species occurring 1 or 2 months
earlier than their normal seasonal cycle and a decrease in the ratio of diatoms to dinoflagellates.
However since “the exact same pattern and increase was also seen in oceanic waters to the west of the
British Isles” the conclusions are quite different: “that a strong overriding climatic signal is apparent in
the phytoplankton data recorded by the CPR survey, which is not only evident in regional areas of the
north-east Atlantic, but also in coastal areas of the North Sea. Even in restricted areas of the North Sea
close to the coastal zone, where adverse effects associated with elevated nutrient concentrations are believed
to occur, the over-riding long-term signal also appears to be climatic in origin ... from the virtually identical
trends in phytoplankton biomass from all regional areas of the North Sea, including the coastal zone of
the Danish coast and the German Bight”. On the basis of this analysis and these conclusions, they suggest
it is essential that natural hydro-climatic variability and wider Atlantic influences on regional seas are fully
taken into account when developing the criteria and methods to be applied to the OSPAR Common Procedure.
The above example relies on the comparison of changes at the largest scale between ocean and shelf.
Valuable insights into the eutrophication debate have also been derived from more localised and more
specific comparisons within an area of shelf, and this forms our second example. In 1987–1988, the CPR
recorded remarkable and unprecedented changes in the summer plankton of the North Sea (Dickson, Colebrook, & Svendsen, 1992). The main change was an increase in the abundance of certain Ceratium spp.
(C. furca, C. fusus and C. tripos) by ⬎+2 SD (Fig. 6). There was no obvious change in their time of
production, but a parallel increase was observed in the neritic copepods Acartia and Temora, and in the
cladocerans Evadne and Podon.
This change was of interest for two main reasons. First the Ceratia are dinoflagellates whose shape and
relatively large size (Fig. 7) allow them to be collected quantitatively by the CPR, unlike many of the
smaller dinoflagellate species. Although not toxic themselves, they are part of the same order of plankton
as many of the nuisance bloom species that affect our waters, giving some expectation that their fluctuations
might provide insight into the causes of such blooms. Second, the unprecedented scale of the increase was
itself of interest. There had already been some speculation (e.g. Frank, Perry, Drinkwater, & Lear, 1988)
that ‘global warming’ in temperate and subarctic waters would act to favour components of the summer
plankton, particularly dinoflagellates, in view of their strong preference or requirement for stable stratified
conditions (explained by Dickson, Colebrook & Svendsen, 1992). And since the time of their peak occurrence coincided with the summer minimum in inorganic nutrient concentrations, it was also suspected that
this dramatic increase in the plankton might reflect the relief of nutrient-limited growth through anthropogenic nutrient inputs, in other words, that it was a result of eutrophication.
Had our observations of this change been restricted to the near-shore margins of the German Bight
where the Ceratium increase was between three- and four-fold, this viewpoint might well have prevailed.
However, when the CPR dataset for the whole North Sea was examined to identify the site of maximum
change, it was immediately apparent that such a cause was unlikely. This analysis showed that the locus
of maximum increase (17-fold compared with the long-term mean) lay east of the Shetlands with a tongue
of lesser increase running south-eastward into the German Bight (Fig. 8). As these authors conclude,
“Plainly, although it is possible to identify some components of the plankton which exhibit some increase
further south, we are dealing with a phenomenon of the northern North Sea, remote from the zone of
maximum anthropogenic nutrient loadings along the continental coast of the German Bight”. The role of
eutrophication was discounted. Instead, the close correspondence between the distributions of near-surface
(0–30 m) salinity anomaly and increased Ceratium abundance across the northern North Sea (Fig. 8) confirmed clearly enough that the cause was the reinforcement of haline stratification in the summer of 1987,
caused by the extreme westward spread of fresh water from the Norwegian (and Jutland) coasts. The
cladocerans showed a parallel increase because they eat Ceratium.
It is easy to overlook the features of the CPR data set that have contributed to this outcome. We have
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Fig. 6. Seasonal cycles and trends in abundance (1958–1988) of three species of Ceratium in the North Sea. From Dickson, Colebrook and Svendsen (1992).
used its length of record to define the norm and identify the amplitude of the change. Its species discrimination showed which classes of plankton were affected and which were not, thus providing clues as to the
types of environmental change that were likely to be important. Its space–time discrimination defined the
locus of change and provided enough detail on distribution to match against hydrography. And finally, the
CPR record showed a reversion to normal Ceratium abundances in the northern North Sea during the
following summer—the clearest confirmation that this remarkable change was the local effect of short-
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Fig. 7.
Line drawing of Ceratium tripos. Redrawn after Lebour.
Fig. 8. Anomaly in abundance of Ceratium spp. (heavy lines) as a multiple of the long term mean and near-surface (0–30 m)
salinity–anomaly (light lines and shading). From Dickson et al. (1992), their Figure 4a.
term climatic ‘noise’, not the result of slow shifts in global climate or regional contamination. Where these
features are important to the eutrophication debate, the CPR is still the only observing system capable of
providing them.
5. Biodiversity and global change
In some instances, Hardy’s initial ideas and methods have been overtaken by events. The advent of
satellite remote sensing in the late 20th century, for example, has permitted the study of plankton patchiness
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187
on a space and a time-scale inconceivable to Hardy. However, we have other examples in which the
usefulness of the CPR technique has expanded to meet actual or potential problems, which did not exist
in Hardy’s day.
One such problem is the warming caused by the increase in greenhouse gases. Plankton play a significant
role in this because they fix carbon, which may subsequently be transported into the deep ocean and remain
there for very long periods of time. The CPR provided the first spatially and temporally extensive pictures
of the timing of spring phytoplankton and zooplankton blooms in the North Atlantic and, on the basis of
these distributions, Colebrook (1979) suggested that phytoplankton were not fully grazed, resulting in “a
surplus of phytoplankton in the open ocean for most of the summer”. This established the existence of a
large quantity of fixed carbon, which might be exported down the water column.
A second problem is the threat to ‘biodiversity’ that seems an increasingly likely outcome of global
change, and which has prompted a number of attempts to find appropriate global solutions. A Convention
on Biodiversity was one of the main outcomes of the UN Conference on Environment and Development
in Rio de Janeiro in 1992, and a global initiative known as DIVERSITAS will include marine biodiversity
as a special target area, aimed at understanding how marine biodiversity is affected by the broadest range
of human impacts including fisheries operations, eutrophication, alteration of physical habitat, invasion of
exotic species, etc. The coastal marine environment seems particularly vulnerable to man’s activities and
has become a priority issue in global ecology: at the beginning of the 21st century, 60% of the world’s
population was living in or dependent on the coastal zone, and this population and its impacts seem set
to increase rapidly.
While there are obvious socio-economic and perhaps ethical reasons for the protection of biodiversity,
there is also a growing body of legislation requiring compliance. These legal obligations stem from the
global Conventions on Biological Diversity and the Law of the Sea, regional conventions, such as those
of the Council of Europe or the Directives of the European Union, and national laws regulating fisheries
and nature conservation. Of particular relevance to marine biodiversity in European shelf seas is the socalled ‘Habitats Directive’ for the conservation of natural habitats and wild fauna, which inter alia, requires
member states to ‘monitor biodiversity’ and ‘promote the maintenance of biodiversity’ as a means of
assessing the health of ecosystems, and particularly with identifying habitat degradation caused by Man’s
activities. In providing information on around 450 taxonomic entities of zooplankton and phytoplankton
over many decades, the CPR is the only survey capable of defining the baseline for the planktonic ecosystem
and thus of providing a monitor of changes in regional planktonic diversity in both the open ocean and
the shelf. Thus, although Hardy can scarcely have conceived of this particular application, it is unsurprising
that the CPR survey was identified as a ‘major biodiversity monitoring programme’ in EU/EEA (European
Environment Agency) member states (Warwick, Goni, & Heip, 1996).
The utility of the CPR dataset has thus evolved in line with current environmental concerns from a
fisheries and biological oceanographic perspective to a wider ecological one. Present evidence is that planktonic populations respond extremely sensitively and quickly to ocean variability (Roemmich & McGowan,
1995). The temperature tolerance range of many species may also delimit the geographical distribution of
a species, with populations shifting latitudinally in response to shifting climatic zones. Some points of
detail may be guessed. Since components of the plankton, especially copepods, are more diverse further
south, a warming ocean may lead to an increase in plankton diversity in temperate waters. Such an increase
may not be considered desirable as it could lead to a reduction in the productivity of fisheries. The CPR
has already identified both a rapid rise in the incidence of sub-tropical plankton species in the North Sea
over the last decade and a strong biogeographic shift in all copepod assemblages, with a northward extension
by more than 10° in the latitude of warm-water species, associated with a decrease in the number of colderwater species. These biogeographical shifts in plankton diversity are correlated with northern hemisphere
temperature, suggesting that global warming may be causally involved (Beaugrand, Reid, Ibañez, Lindley, & Edwards, 2002). Phenological changes are also evident in the CPR data, with some species reaching
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their seasonal peak up to 2 months earlier in the 1990s compared to the long-term seasonal mean
(unpublished data). Changes in biodiversity, physiology, phenology and geographic distributions of plankton will inevitably alter competitive interactions between species and trophic levels and may radically alter
food-web structures, carbon fluxes and nutrient recycling processes, but these interactive and emergent
properties are too complex to predict.
The trans-ocean transfer of nuisance species in ship’s ballast water is a particular and extreme example
of a change in planktonic biodiversity due to Man’s activities. As Showstack (2001) reports: “The IMO
estimates that 10 billion tonnes of ballast water are transferred globally each year, and that 3000 species
of animals and plants may be transferred daily around the world. Among the suspected hitchhikers are
toxic dinoflagellates that have threatened shellfish farming in Australia, the American comb jelly that helped
in the collapse of the Black Sea anchovy fishing industry and the tropical green alga Caulerpa taxifolia
that is replacing native sea grasses in the Mediterranean. With faster ships, more trade agreements, and
more shipping, problems associated with ballast water could worsen unless the situation is addressed”.
(The spread of Caulerpa taxifolia is most probably facilitated by attachment to the anchors of yachts.) The
US National Invasive Species Act of 1996 is due for re-authorisation in 2002 by Congress, but in advance
of national or international agreement, California, Hawaii, Maryland, Virginia and Washington have already
moved to enact ballast regulations to protect their own waters.
Each such introduction is unpredictable. However, CPR data have provided a unique case history of an
invasive plankton species (Coscinodiscus wailesii), from its initial introduction into European shelf seas
through its subsequent geographical spread over the period of a decade, to its persistence as a significant
member of the plankton community (Fig. 9, from Edwards, John, Johns, & Reid, 2001b). This analysis
Fig. 9.
Distribution of Coscinodiscus wailesii. From Edwards, John, Johns & Reid (2001b).
K.M. Brander et al. / Progress in Oceanography 58 (2003) 175–191
189
suggests that measuring the pattern and rate-of-spread of non-indigenous species in the marine environment
is essential if we are to establish the effectiveness of any management strategy that we may deploy to
limit such invasions. Analysing the effect of invasive species on the marine biodiversity of European shelf
seas will therefore remain a part of ongoing CPR research.
Recent marine management strategies have stressed the importance of an integrated ‘ecosystem approach’
to the management of marine resources and with it an assessment of the ecological ‘health’ of the regional
system under management (Sherman & Duda, 1999). Though the assessment of patchiness by the CPR
survey may have been superseded by satellite imagery (see earlier), the assessment of ecological health
requires data on the plankton community, which cannot be assessed remotely. Accordingly, one of the
primary parameters for assessing ecological health is suggested to be the system’s biodiversity (Sherman
and Duda, 1999). With the collection of over 70 years of community data by the CPR survey, it is now
in a position to act as a baseline for changes in marine biodiversity, to monitor the marine response to
climate forcing and its extension into global change, and to provide managers with an index for the assessment of the general health of European regional seas.
If global change proceeds at anything like the projected rate during the 21st century, it seems likely that
the CPR survey will continue to encounter and report evidence of rapid and radical changes in planktonic
populations and in the plankton community. Without such programmes, we will simply have no knowledge
of change in ecological health over large areas of the ocean and hence no means of assessing the appropriateness, or effectiveness, of measures designed to protect the marine ecosystem from anthropogenic impacts.
6. The role of the CPR within biological oceanography
Although this paper is primarily about the utility of the CPR in relation to issues of marine management,
one should not exclude the part, which it has played and continues to play in the development of science
and more specifically in biological oceanography. The utility may be indirect in this case, but the CPR
has undoubtedly helped to strengthen and focus the application of marine science to the wider concerns
of society.
Results from the recently completed Trans-Atlantic Study of Calanus (TASC) are an example of the
application of CPR information. The first paper in the TASC Symposium volume on Population Dynamics
of Calanus in the North Atlantic, by Planque and Batten (2000) provides the long-term large-scale context,
within which the more detailed, short-term studies making up the bulk of the programme results can be
framed. They show that the abundance of Calanus finmarchicus has declined and by 1997, which had been
designated the “year of Calanus” and in which much of the research took place, it was at the lowest level
in the 40-year record for the NE Atlantic. Many of the papers in the symposium volume use information
from the CPR and most refer to results from it. The national and regional research programmes, which
follow on from the TASC programme, have relied heavily on CPR information for their geographic coverage and sampling design. Without this background information there would have been large (probably
infeasible) additional survey costs for the field programmes, just to establish the basic seasonal and geographic distributions and even then there would be no knowledge of how these compared with other years.
Reliance on the CPR to provide the geographic and seasonal frame for plankton populations throughout
much of the North Atlantic is almost taken for granted. It would be unthinkable to produce reports on the
status and changes in the marine environment, such as the quality status reports, without including CPR
information, where it is available. The danger in being taken for granted is that it is often accompanied
by the assumption that no effort is needed for the activity to continue. The history, current operation and
funding of the CPR shows how far this is from reality and that even successful monitoring programmes
such as this can quickly come to a halt unless individuals and teams are prepared to make extraordinary
efforts to keep them going.
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There is growing awareness of the need for informed, timely and appropriate adjustment of many aspects
of human activity in relation to our natural environment. A prerequisite for such action is awareness of
the variability, which natural systems undergo and some understanding of their interrelationships and
responses to change. This does not come quickly and a long, consistent, uninterrupted time series is of
great value, particularly when it is taxonomically as detailed as the CPR. The future of the CPR must be
considered in the context of other marine monitoring and ‘operational oceanography’—it must be a sustained, temporally open-ended commitment, which is not immune from change and improvement, provided
that comparison across the whole of the time span is maintained. There can be little doubt that Alister
Hardy would applaud this aim, since it follows the goals, which he set in establishing the survey 70
years ago.
In 1956, he wrote: “No doubt before long the old recorder will be obsolete, as it is superseded by a
new invention”. We must honour his commitment to technological progress, while preserving the continuity
of the remarkable time series, which he established.
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