Special Issue: Long-term ecological research

Multi-decadal oceanic ecologicaldatasets and their application inmarine policy and managementMartin Edwards1,2, Gregory Beaugrand3, Graeme C. Hays4, J. Anthony Koslow5 andAnthony J. Richardson6,7

1 Sir Alister Hardy Foundation for Ocean Science, Citadel Hill, The Hoe, Plymouth PL1 2PB, UK2 Marine Institute, University of Plymouth, Drake Circus, Plymouth PL4 8AA, UK3 Centre National de la Recherche Scientifique, Laboratoire d’Oceanologie et de Geosciences UMR LOG CNRS 8187, Station Marine,

Universite des Sciences et Technologies de Lille – Lille 1BP 80, 62930 Wimereux, France4 Department of Pure and Applied Ecology, Swansea University, Swansea SA2 8PP, UK5 Scripps Institution of Oceanography, 9500 Gilman Drive, University of California, S.D. La Jolla, CA 92093-0218, USA6 Climate Adaptation Flagship, CSIRO Marine and Atmospheric Research, Cleveland, QLD 4163, Australia7 School of Mathematics and Physics, The University of Queensland, St Lucia, QLD 4072, Australia

Review

Long-term biological time-series in the oceans are rela-tively rare. Using the two longest of these we show howthe information value of such ecological time-seriesincreases through space and time in terms of theirpotential policy value. We also explore the co-evolutionof these oceanic biological time-series with changingmarine management drivers. Lessons learnt fromreviewing these sequences of observations provide valu-able context for the continuation of existing time-seriesand perspective for the initiation of new time-series inresponse to rapid global change. Concluding sectionscall for a more integrated approach to marine observa-tion systems and highlight the future role of oceanobservations in adaptive marine management.

The rarity of multi-decadal biological oceanic datasetsWhile there are a number of long-term biological time-series on land, there are relatively few in marine environ-ments. This is highlighted by the fact that the IPCC(Intergovernmental Panel on Climate Change) FourthAssessment Report noted 28 586 significant biologicalchanges in terrestrial systems, but only 85 from marineand freshwater systems [1–2]. Of the marine biologicaltime-series, most are coastal, often associated with theproximity of a convenient marine laboratory [3–4]. Long-term (multi-decadal) open-ocean biological datasets arenotoriously rare, especially those that monitor multipletrophic levels over a broad spatial scale. This is undoubt-edly a consequence of the difficulty in sampling this remoteenvironment on a continuous and routine basis, the obvi-ous financial constraints of maintaining such an undertak-ing, and the technical difficulty and expense of measuringbiological variables beyond bulk indices. For these reasons,few global repositories of oceanic biological data collectedfrom the oceans of theworld exist, and themajority of these

Corresponding author: Edwards, M. (maed@sahfos.ac.uk).

602 0169-5347/$ – see front matter � 2010 Elsevier Ltd. All rights res

are riddled with numerous spatial holes and temporal gapsdue to funding cycles.

Because of the rarity of long-term ocean biologicaltime-series, we focus here on two, one from the NorthAtlantic and the other from the North Pacific, that havebeen in operation for more than 60 years and that overthat period have been intimately connected with manage-ment decisions. The California Cooperative Oceanic Fish-eries Investigations (CalCOFI) in the North Pacific andthe Continuous Plankton Recorder (CPR) survey in theNorth Atlantic have the longest record of sustained oceanobservations. These two oceanic surveys are similar insome important ways: both cover large spatial areas andboth provide long time-series allowing for the establish-ment of baseline means that can reveal frequencies ofoscillations and the amplitude of anomalies over manydecades (Box 1).

The waxing and waning of historical time-seriesIn this period of rapid environmental change, ecologicalmonitoring now forms the basis of many long-term scien-tific strategies for marine ecosystem management. How-ever, this has not always been the case and many time-series have been initiated but few survived even a decade[5]. Until recently, long-term ecological monitoring wasoften considered a dispensable funding option until societybecame aware of the rapidity of anthropogenic changes inthe biosphere and the need to monitor and evaluate thesechanges in reference to long-term established baselines(Figure 1).

How did the CalCOFI and CPR surveys survive manydecades before this recent appreciation of their value? Inthe case of CalCOFI, the range and frequency of samplinghas contracted considerably since its inception and in thecase of the CPR survey, it was weakened on a number ofoccasions throughout the survey’s history, often teeteringon the edge of financial collapse. However, both these

erved. doi:10.1016/j.tree.2010.07.007 Trends in Ecology and Evolution 25 (2010) 602–610

Box 1. Multi-decadal sampling by the CPR survey and CalCOFI.

The Continuous Plankton Recorder (CPR) survey is operated by the Sir

Alister Hardy Foundation for Ocean Science (SAHFOS), an interna-

tionally funded charity operating in the North Atlantic and North

Pacific. The survey, initiated by Sir Alister Hardy in 1931, has evolved

into a marine monitoring programme that measures plankton

communities (�500 planktonic taxa are routinely recorded, many to

species level) on an oceanic scale using cost-effective voluntary ‘ships

of opportunity’. It is now one of the longest and most geographically

extensive ecological datasets in the world with �100 million plankton

records and has sister surveys in the Southern Ocean, Australian

waters, NW Atlantic and South Africa. CalCOFI, operating off the

Californian coast since 1949, is a partnership between federal and

state fishery agencies [the National Marine Fisheries Service (NMFS/

NOAA) and California Department of Fish and Game] and the Scripps

Institution of Oceanography. The government agencies have been

concerned primarily with fishery management, and Scripps has

focused on the marine environment, in particular, climate science

and oceanography. The CalCOFI program has sampled phytoplank-

ton, zooplankton and fish distributions with species-level resolution,

associated physical variables, primary production and nutrients over

the course of its lifetime. These longstanding surveys provide

invaluable insights into keeping such long-term observation pro-

grammes operating despite the vagaries of funding and evolving

management objectives (Figure I).[(Figure_I)TD$FIG]

Figure I. Left figure: Continuous plankton recorder sample distribution in the Northern Hemisphere. Right figure: CalCOFI station positions off the southern Californian

coast.

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surveys continue to survive: the CPR survey continues tooperate throughout the world’s oceans with routine sam-pling of �10 000 nautical miles of open-ocean systemsevery month, and the CalCOFI survey has undergone agreat expansion in the range of oceanographic param-eters now routinely monitored as part of it. The mainreason the CPR and CalCOFI surveys still exist is thatthey not only provide invaluable scientific knowledgeabout change in pelagic ecosystems, but they have alsodemonstrated continuing utility for marine environmen-tal management and policy over the many decades oftheir existence.

Both CalCOFI and the CPR survey were set up as eco-logical monitoring programmes that would have immediatevalue with regard to the management of natural resources.CalCOFI was initiated in 1949, with the primary aim ofunderstanding the recruitment variability of the Pacificsardine and its systematic decline at that time in theCaliforniaCurrent. Similarly, theCPRsurveywasdesignedto monitor the distribution and movements of plankton inthe North Sea with the objective of relating these studies tofishpopulationdynamics.Bothof these studiesuseplankton(predominately phytoplankton, zooplankton and ichthyo-

plankton) to monitor ecological changes. Planktonic ‘indica-tor species’ are highly sensitive to environmental variabilityand have a long history in ecological monitoring of themarine environment [6]. They represent a relatively quickand easy way to monitor different water masses, definemarine habitats and to observe changes in food-web struc-ture. Over the past decade, these applications have beenrefined and used as management tools by developing ap-plied ecological indicators to support specific, evolving ma-rine management issues and to provide evidence-basedinformation for policy [7–9]. Examples include specific poli-cies and legislation that monitor fluctuations in climatechange impacts, fisheries and marine wildlife, pollution,Harmful Algal Blooms, invasive species and marine biodi-versity (Figure 2).

The value of marine ecological time-series withincreasing space and timeAs the length of the time-series and the range of spatialscales addressed increases, so does the number of manage-ment issues that can be tackled. This is a key reasonbehind the longevity of time-series and can be illustratedby the CPR survey (Figure 3). By traversing many space

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[(Figure_1)TD$FIG]

Figure 1. Start of sustained open-ocean biological time-series and records (temporally broken and coastal time-series are not included) plotted along the global mean SST time-

series from 1900 (Hadley Centre). While some records are taxonomically rich and sampled at a monthly frequency, many time-series are only annually or seasonally collected at

single point stations and only contain bulk biological indices such as chlorophyll. Note that the majority of time-series are less than 30 years long and many were initiated when

temperature records began a monotonic rise. Many biogeographical and phenological observations may therefore be biased because most studies were performed during a

period of monotonic climate warming with no prior established baseline. Station P (North Pacific), RYOFU line (west Pacific transect), VICM (Vancouver Island Continental

Margin time series), NMFS (National Marine Fisheries Service collection), BATS (Bermuda Atlantic Time series Study), HOT (Hawaii Ocean Time series program), BD Zoo (North

Coast of Spain), SO CPR survey (Southern Ocean CPR survey), AMT (Atlantic Meridional Transect), and AZMP (Atlantic Zone Monitoring Program).

Review Trends in Ecology and Evolution Vol.25 No.10

and time scales these surveys can address a multitude ofmanagement issues as well as emerging issues (e.g. oceanacidification [10]). The dominant external force on marineecosystems depends on the scale of study. For example, insmall-scale studies, biological patterns could be driven bybiological forcing (e.g. predation), whereas in large-scalestudies patterns could be predominantly forced throughhydro-climatic variability. For example, climate changehas a macro-scale impact encompassing virtually all spaceand time scales, while eutrophication may only manifestitself locally or at the meso-scale. Many long-term studiesfrom single-point stations in the North Sea have initiallyinterpreted abrupt changes in the biology of the North Seaas signs of nutrient enrichment; however, when regionalcomparisons were taken into consideration the biologicalpatterns that emerged were found to be part of far-fieldNorth Atlantic hydro-climatic changes [11]. These findingsstress the need not only for an ecological approach tomonitoring human impacts but for incorporating amulti-scale approach in future monitoring strategies thatquantifies some degree of natural variability from theregional scale down to the local scale. A technique nowtypically employed by the CPR survey to address marineenvironmental policy issues for assessment purposes is theadoption of a macro-scale downscaling approach. Startingat the CPR survey’s maximum spatial-temporal extentwhere climate oscillations dominate biological signals,there is a systematic working down of the scales to assessheterogeneous biological signals and spatial responsesthat appear at smaller scales.

Writing in the 1980s, Colebrook [12] summarised theexpansion of the CPR time-series through space and timeand perceptively argued that it yieldedmore and different

604

information as a consequence. Coherent patterns of spe-cies in eco-regions were definable with 12 years of data[13]; a long-term quasi-linear trend was identified with 20years of data [14]; the 3-year periodicity, using spectralanalysis, was first noticed with 26 years of data; and after36 years of data, reliable relationships between planktondata and large-scale weather systems were identified (inthis case a relationship between copepods and westerlyweather showed a high level of coherence at the longestwavelengths). In the following decades, many other hy-dro-climatic signals were identified, such as the relation-ship between the North Atlantic Oscillation (a naturaldecadal atmospheric oscillation) and phytoplankton [15]and zooplankton [16], as well as multi-decadal regimeshifts across many trophic levels [7,17]. As a monitoringprogramme expands through time and includes multiplespatial scales, therefore, its value increases as it capturesmore and more spatio-temporal structures and naturalphenomena, as well as shifting decadal and multi-decadalbaselines and regimes. This provides the best way toseparate anthropogenic and natural biological signalsand address the extent and severity of various anthropo-genic impacts. Surveys that traverse multiple-scales pro-vide both the larger-scale and finer-scale perspectivesthat are missed by point time-series. Here we use somerecent policy-driven questions regarding the ecologicalstate of the marine environment to illustrate how thesequestions can be answered through having a long-termbiological time-series. Our intention here is not to create acomprehensive review of the history and results fromoceanic time-series but to highlight some case-studiesrelevant to marine management and policy (see alsoBox 2).

[(Figure_2)TD$FIG]

Figure 2. Recent examples of plankton ecological indicators providing evidence-based research for policy and marine ecosystem management to address issues ranging

from climate change impacts to non-indigenous species. Many new questions and policy issues (e.g. eutrophication, biodiversity, climate change impacts, pollution and

acidification) have emerged over the past few decades, following the realisation that the marine environment has become progressively perturbed by human impacts. This

has increasingly led to the use of applied ecological indicators to monitor and assess these impacts.

Review Trends in Ecology and Evolution Vol.25 No.10

Case-studies of applied ecological indicators forassessing and monitoring change in oceanicecosystemsPolicy-driven question: Is there evidence that climate

change is having an impact on oceanic ecosystems and

can it be distinguished from natural low-frequency

climate variability?

There is a large body of observed evidence to suggest thatmany oceanic ecosystems are responding, both physicallyand biologically, to changes in regional climate causedpredominately by the warming of sea surface temperatures(SST) and modification of ocean currents and atmosphericpressure systems. Biological manifestations of warmingSST take the form of biogeographical, phenological, biodi-versity, physiological and species abundance changes, aswell as whole ecological regime shifts [18]. What particu-larly stands out from these oceanic studies is the rapidity ofthe pelagic and planktonic responses, be it biogeographicalor phenological, to climate warming and global changecompared to their terrestrial counterparts [1,18]. For ex-ample, plankton shifts of up to 200 km per decade [19] havebeen observed in the North East Atlantic, compared with ameta-analytic terrestrial average of 6 km per decade [20].Similarly, changes in phenology of up to six weeks have

been observed in pelagic ecosystems [21], compared witha mean phenological change of 2.3 days collectivelyobserved for 172 species of plants, birds, insects andamphibians [20].

Any observed change in the marine environment asso-ciated with climate change, however, should be consideredagainst the background of natural variation on a variety ofspatial and temporal scales. Recently, long-term decadalobservational studies have explored natural modes of cli-matic oscillations with similar temporal scales such as theEl Nino-Southern Oscillation (ENSO) and the Pacific De-cadal Oscillation (PDO) in the Pacific and the North At-lantic Oscillation (NAO) in theNorth Atlantic in relation topelagic ecosystem changes [22–24]. Both the CalCOFI andCPR surveys have revealed that oceanic time-series arestrongly affected by low-frequency climate oscillations.Many of the biological responses observed have been asso-ciated with warming temperatures. However, assessingeffects of anthropogenic climate change embedded in nat-ural modes of variability, particularly multi-decadal oscil-lations such as the Atlantic Multidecadal Oscillation(AMO) [25], is extremely difficult and evidence of changesattributable to anthropogenic climate change must betreated with some degree of caution. Even after 80 years

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[(Figure_3)TD$FIG]

Figure 3. The relationship between the focus of CPR research and types of understanding (a), coupled with changing marine management issues (b) and the expansion of

the CPR survey in space and time and spatio-temporal ecosystem structures (c). Understanding large-scale environmental change in the marine environment for example,

can only be addressed by monitoring on similar space and time scales. Over the course of many decades, the science of a long-term monitoring programme evolves in

response to policy issues to guarantee financial survival and it must continue to act as a utility for marine resource management and policy. For example, a recent emerging

issue is ocean acidification, with the CPR survey and CalCOFI already providing in situ data for calcareous organisms. However, the CPR survey has not only proved an

invaluable tool by providing direct empirical evidence to inform policy makers, but throughout its history has provided new insights into natural and anthropogenic

changes and in many cases influenced policy change. In this way, changing policy drivers and the CPR survey can be considered co-evolved.

Review Trends in Ecology and Evolution Vol.25 No.10

of operation, the CPR survey is only now capable of takinginto account the longer frequency of natural variability inthe North Atlantic temperature records. However, therecent discovery of a Pacific diatom species in the NorthAtlantic may provide some biological evidence that we areactually witnessing unprecedented change in the NorthAtlantic even beyond the scale of ice-age variations withthe first documented trans-Arctic migration of a species for800 000 years [26].

Policy-driven question: How do we manage our

fisheries? A move towards ecosystem-based

management

CalCOFI was initiated to study the relative influence ofenvironmental change and overfishing on the decline of thePacific sardine fishery, the largest fishery in the westernhemisphere, in the 1940s. Since 1984, the survey hasconsisted of quarterly cruises that cover the extensivespawning grounds of the anchovy, sardine and hake offsouthern California. This has provided fishery-indepen-dent data on the anchovy and sardine populations basedon the daily egg-production method [27] derived fromquantitative tows for fish eggs and larvae along withancillary data on adult fecundity and proportion spawning.The CalCOFI ichthyoplankton sampling has been integralto stock assessment of anchovy and sardine and hasallowed these populations to be tracked even when theywere not commercially exploited, including the several

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decades between the collapse of the Pacific sardine fisheryin the 1950s and its recovery in the 1980s.

By counting eggs and larvae of approximately 400 taxaof fish and invertebrates from the CalCOFI zooplanktontows, most of which are not commercially exploited, it hasbeen possible to distinguish impacts of natural and an-thropogenic forcing on the fish community of the CaliforniaCurrent. Commercial exploitation has been shown to in-crease the variability of fish populations [28,29], and long-term trends and phenological shifts are evident in bothexploited and unexploited components of the fish commu-nity [30,31]. All these long-term measurements have en-abled researchers to recognise the importance of oceanicclimate conditions (such as the PDO and ENSO) on theproductivity of marine fisheries and various components ofthe California Current System [32,33]. This recognitionthat environmental fluctuations on the inter-annual andinter-decadal timescales have far reaching consequenceson fishery science and management was instrumental inthe motivation for ecosystem-based management. For in-stance, ecosystem-based management manages fisheriesin the context of the whole ecosystem and includes ecosys-tem-level factors such as climate oscillations that interactwith fishing to impact stocks. In contrast, traditional stockmanagement approaches focused on only single species.Lessons learnt from CalCOFI have been instrumental indeveloping the theory of ecosystem-based managementand data from the survey continue to be integrally involved

[(Figure_I)TD$FIG]

Figure I. (a) Cod (Gadus morhua). Time-series of fish abundance are used globally to inform fisheries management, as well as identify over-exploited populations.

These time-series are derived from dedicated fisheries surveys or catch per unit effort data. (b) A dog whelk (Nucella lapillus). Coastal zone time-series are often

associated with marine biological laboratories and influence, for example, policy on managing pollution. As an example increasing incidence of imposex (a condition

where male sexual characteristics are superimposed on females) in gastropod molluscs was linked to the use of tributyltin (TBT) in anti-fouling paints used on the hulls

of ships and helped to drive international law to ban these paints. (c) A green turtle (Chelonia mydas). Time-series for endangered species are used to designate the

conservation status which drives international conservation policy. For example, long-term changes in the abundance of green turtles has led to their designation by the

International Union for the Conservation of Nature (IUCN) as endangered and, consequently, this species is listed on Appendix 1 by the Convention on International

Trade in Endangered Species of Wild Fauna and Flora (CITES), meaning that international trade in green turtle products (e.g. green turtle soup) is prohibited. (a)

Reproduced with permission from The Rooms Provincial Archives, St Johns; (b) Graeme Hays; and (c) Caroline S. Rogers.

Box 2. Policy questions and marine biological time-series.

While marine plankton are the focus of some of the longest-standing marine biological time-series, the value of other time-series is widely

recognised, as illustrated by the examples in Figure I.

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in the development of the next generation of ecosystem-based marine management in the California Current.

The role of ocean observations in adaptive marinemanagementThe mixed success of conventional management of ouroceans, in particular fisheries management [34], and thecontinuing human threats posed, have necessitated inno-vative approaches to the management of our oceans [35].The ecosystem approach to management (EAM) has beenproposed as a more effective and holistic approach formanaging and maintaining healthy marine ecosystemsand the goods and services they produce by addressingsome of the consequences of human use [36,37]. However,while EAM considers the effect of fishing at the ecosystemlevel, whenmoving beyond its impact on the target species,it may in some cases underestimate climate-driven envi-ronmental variability that can exert bottom–up control onfish stocks. Results using the CPR survey emphasise thateffective EAM must also consider the position of a stockwithin its ecological niche, the direct effects of climate andthe influence of climate on the trophodynamics of theecosystem [38–40].

Robust EAM needs an ecosystem approach to oceanobservation, beyond simply the physical and chemicalenvironment. The foundation of a sound EAM is reliableinformation on the distribution, abundance and interac-

tions of species at multiple trophic levels. Increasingly,ocean time-series observations are being used to supportmanagement decisions within an adaptive managementframework for EAM. The adaptive management cyclerequires a phase of determining management objectives,implementing actions, evaluating the success or otherwiseof management strategies, and adjusting the strategy forthe next cycle in order to better meet objectives. Time-series observations are useful to the adaptive managementcycle in three main ways. First, monitoring programs areneeded, so that once ecological or performance indicatorscross over a threshold, management actions are triggered.

Second, ocean observations are also needed for evalu-ating the efficacy of management actions and for learningabout how the system functions in order to improvefuture management. An emerging pillar of EAM is Inte-grated Ecosystem Assessments, which provide the basisfor reviewing the status and trends of ecosystems. In theUS, for example, the California Current has been chosenby NOAA as the proof-of-concept for an Integrated Eco-system Assessment, primarily because of the extensivelong-term monitoring data collected by the CalCOFIprogram [41]. As a research-vessel-based program, Cal-COFI measures a range of physical, biogeochemical andbiological parameters at each station, including temper-ature, salinity, oxygen, nutrients and chlorophyll withdepth, as well as zooplankton and ichthyoplankton. In

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addition, while underway between stations, seabirds andmammals are surveyed and acoustic observations of mid-trophic levels are carried out. These measurements haveenabled researchers to assess the impacts of El Nino anddecadal-scale climate variability (the Pacific Decadal Os-cillation and North Pacific Gyre Oscillation) on variouscomponents of the California Current ecosystem [32,33].Ship-based sampling is now supplemented by mooringsand glider deployments along several CalCOFI transectlines. CalCOFI data underpin annual Integrated Ecosys-tem Assessments of the California Current. Further,sampling of the coastal ichthyoplankton in CalCOFIhas been proposed as a cost-effective means to evaluatethe benefits of the new network of Marine ProtectedAreas on nearshore fish communities.

Last, observations from CalCOFI are increasingly beingused to underpin process studies and to validate andcalibrate ecosystem models and for near real-time assimi-lation. The US National Science Foundation selected theCalifornia Current for a process-oriented Long-Term Eco-logical Research study, based on the program’s close col-laboration with CalCOFI. The close interaction of long-term observations and process studies with ecosystemmodelling is viewed as a most effective means to advanceecosystem understanding. Such data–model fusion is beingused to underpin decision-making and for managementstrategy evaluation by choosing the optimal managementdecision from a suite of possible actions based on theoutputs from the ecosystemmodel and management objec-tives. CalCOFI data are being used to parameterise andvalidate a biophysical model which will extend from oneend of the California Current to the other, and which willinclude fish [42]. As ecosystem models increase in theirrealism and include higher trophic levels and more func-tional groups, marine biological observations will becomeincreasingly necessary.

The way forward: integrated observing systemsWith the realisation that ocean ecosystems are vulnerableto human threats such as overfishing, climate change,eutrophication, habitat destruction, pollution and speciesintroductions (e.g. [43]), there is an increasing imperativeto observe our ocean biology in amore integrated fashion inorder to provide the long-term baselines needed for man-agement actions and research. However, most currentocean observation programs focus on only one or fewtrophic levels, with none being integrated across multipletrophic levels, from bacteria to whales. Further, there isgrowing evidence that responses to climate change areusually manifested at the species level and that this taxo-nomic resolution is often needed to interpret many ob-served changes [9,21,44]. For example, some of the mosteffective ecological indicators used for assessment pur-poses in European seas are constructed at the species level.

Observation of biological variables at a high taxonom-ic level, however, is technologically challenging, timeconsuming, requires considerable skill and is expensive.Further, the identification of species becomes more diffi-cult in tropical systems where diversity is higher andspecies are more likely to be found at low abundancethroughout the year. The CPR and CalCOFI surveys

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both employ large numbers of skilled taxonomists toidentify plankton samples to the species level whereverpossible. By contrast, automated methods for physicaland chemical variables make measuring these ecosystemcomponents relatively easy. However, monitoring of atleast some biological components can be semi-automatedand these techniques are ripe for inclusion in futuremarine observing systems to make them truly integrat-ed, although many provide useful information at a func-tional group level rather than at the species level.Functional group approaches to biological observationprovide some baseline of ecosystem change and cancertainly be useful when setting up modelling studieswith an aim to simplifying large and complex problems.One useful semi-automated technology is the sensing ofphytoplankton functional groups from fluorescence atmultiple wavelengths [45]. Additional technologies thatare being used extensively for animal tracking includeactive acoustics and satellite telemetry. These allowresearchers to investigate the distribution, migrationroutes, and spawning and feeding aggregations of ma-rine animals and how these are influenced by climatevariability and change. The technology poised to trulyrevolutionise biological observing systems is molecularbiology and microbial metagenomics. For example, theCensus of Marine Life project’s Barcode of Life will helpus to identify all species, including species difficult toidentify, and life stages that are currently impossible toidentify. With the massive decrease in cost per observa-tion predicted for genomic methods, this approach islikely to become cost-effective in the near future.

A truly integrated marine biological observing programshould be tightly coupled to physical and chemical obser-vations. This increases its scientific usefulness by facilitat-ing new interpretations of biological time-series. Forexample, the strong link between physical and biologicaloceanography in the CalCOFI program ensures there is acritical mass of researchers enabling greater political andscientific influence, and means that there is a diversity ofresearch themes as priorities change.

Ultimately we need a multinational observing networkfor marine organisms. Fortunately, the basis for such anobserving system already exists in the Global Ocean Ob-serving System (GOOS), which was endorsed by the Inter-governmental Oceanographic Commission (IOC) in 1991.However, this is primarily focused on physical and chemi-cal monitoring. Nevertheless, GOOS is moving towardmore biological observations, facilitated by the recentadvances in biological observation technology. A trulyintegratedmarine observing system needs to have a strongbiological component; otherwise it will run the risk of beingable to detail future physical and chemical changes but willremain unaware of biological consequences. We can nowconceive of biological observing systems across ecosystems,equal to and complementing the existing physical–chemi-cal observing system.

The lessons learnt and future recommendationsThe focus of this article has been on distilling some ofthe lessons learnt from maintaining and positioning thetwo longest and largest oceanic time-series containing

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ecological data. It is clear that successful marine biologicalobserving programmes have a number of characteristics,one of the most important being that they have to con-stantly evolve to inform ever-changing marine policy andmanagement objectives. From the experiences gained frommaintaining multi-decadal time-series and from the con-sideration of a marine management perspective, severalkey recommendations for present and future ocean time-series can be identified:1. Existing ocean ecological time-series, particularly

multi-decadal surveys, need to be maintained, andwhere possible expanded into new areas to guaranteeconsistent methodology for regional comparisons. Thesampling of additional biological properties should takeadvantage of new technological advancements forroutine counting procedures (e.g. molecular techni-ques) while maintaining traditional methods of identi-fication and assessment. Integration with physio-chemical programmes would also be highly beneficial.

2. New ocean time-series should include major experi-mental and process components, have integratedmodelling studies and act as a platform for opportunis-tic and supplementary programmes. These new sur-veys should also consider an applied ecologicalindicator approach for marine management assess-ment purposes and policy transfer. Becoming anindispensable part of ongoing management and policydecisions maximises the programme’s chance of sur-vival.

3. An ecosystem approach to management also needs touse a multi-scale spatial and temporal design. Thisshould quantify some degree of natural variabilityfrom a regional scale down to a local scale as well asmonitor multiple trophic levels where possible. It isonly when these wider-scale, low-frequency influ-ences have been taken into consideration that we canbe confident in any assessment of environmentalimpacts on oceanic systems. Using integrated moni-toring programmes, it is suggested that a macro-scaledownscaling approach is a particularly useful tool forassessment purposes.

4. New ocean time-series observations should be initiatedin under-sampled ocean regions and those regions thatare considered to be particularly sensitive to climatechange such as the Southern Ocean and the Arctic.These new time-series observations should also takemore advantage of ‘ships of opportunity’ as a cost-effective mechanism for extending observations inspace and time.

5. Currently the ocean biological monitoring surveys thatdo exist around the globe are in disparate form and arecollectively unintegrated. There is a need to develop amore systematic data management approach to ensurethe public availability of similar data products and to actas a shared international resource for time-series data.

6. Future biological monitoring of these open-oceanecosystems, through an integrated and sustainedobservational approach, will be essential in under-standing the continuing impacts of climate andenvironmental change on oceanic systems. This inturn may allow us through international collaboration

to mitigate and adaptively manage some of their moredetrimental impacts.

AcknowledgementsWe thank Abigail McQuatters-Gollop for constructive comments on thetext and David Mackas, Todd O’Brien and Mike Sinclair for provinginformation on oceanic time-series. Some of the figures use symbols fromthe Integration and Application Network (ian.umces.edu/symbols),University of Maryland Center for Environmental Science.

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