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Climate and change in oceanic ecosystems: The value of time-series data
TREE vol. 5, no. 9, September
7990
The consequences of climaticchange for the structure and function of oceanic ecosystems are of considera6le current interest. A predictive, mechanistic model of these consequences based on our scanty knowledge of the dynamics of the systems’ con+ ponents seems unlihely: a complex set of simultaneous partial differential equations depicting population interactions and transfer rates of energy and materials would be necessary. A second approach is simply to measure the phenomenologg of variations in both climate and ecosystem components, for the purpose of detecting shared patterns. Two studies of the latter type have 6een done. Both have been successful in revealing relationships Getween climatic variation and large-scale, largeamplitude, low-frequency Giological variability. Both sets of results can provide models for the prediction of consequences, and 60th can serve as Gaselines for the definition of ‘change’.
Populations of pelagic organisms vary on many time-space scales, and much effort has been devoted to describing these variations and to determining their causes. Haury et al.‘, using all available data, constructed a diagram of biomass variability in which both time and space were considered (Fig. I). It shows that oceanic population changes on a small spatial scale are of short duration, and that larger spatial events last longer. There is a rough 45” slope of biomass variability on the log-log plot of time and space. This diagram matches quite well a similar one of physical environmental events in the ocean*. Since this match can hardly be a coincidence, it strongly implies that different biological events happen on different scaies for different physical reasons, and that the izger ones are associated with atmospheric and oceanographic climate. It has become increasingly evident that we must understand these relationships between climate and biota in order to anticipate the consequences of climatic change. There seems to be no question now that humanity has altered the mix of atmospheric gases by increasing those that are active in the process of radiative heating of john McGowan is at the Scripps Institute of Oceanography, University of California, La folla, CA 92093, USA.
fQ 1990
E se”iei
Science Publishers
i!d
IUKi 0169.5347!90602
Climateand Changein Oceanic Ecosystems:The Value of Time-seriesData John A. McGowan Earth. It is predicted that this alteration will change the climate at rates exceeding those of past natural variations. Although there are many uncertainties, it is also likely that the warming will not be uniform but will show significant geographic variation3,4. The warming should change the large-scale general circulation of the atmosphere and the oceans, but the geographic variation should result in numerous and perhaps intense episodic regional and mesoscale perturbations as well. Such events will probably be evident as large and significant nonseasonal positive and negative anomalies from regional means of environmental conditions and, therefore, result in numerous ecosystem disturbances on many scales. The consequences of such disturbances will be very difficult to predict on the basis of our current
knowledge of the structure of food webs and the functional relationships between the components of these webs. These systems are complex, especially in such a mobile environment as the ocean, and are not necessarily at steady state when we measure them. The numerous nonlinear functional relationships between system components may make it impossible to model such systems for arbitrarily long forecast times. Further, the mechanisms by which climatic variations affect many aspects of population biology and the transfer of energy and materials between populations are not well known. All of this makes it unlikely that models based on functional interrelationships of numerous, individual system components can be used soon for the study of ecosystem change. Even the very definition of the word
ICE-AGE VARIATIONS
Fig. I. A conceptual model of the time-space scales of variations in zooplankton biomass, and an indication of the factors contributing to them. A, ‘micro’ patches. B, swarms. C, upwelling. D, eddies and rings. E, island effects. F, ‘El Nitio’ type events. G, small ocean basins. H, biogeographic provinces. I, currents and oceanic fronts - length. I, currents-width. K, oceanic fronts-width. Adapted from Ref. I.
00
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TREE vol. 5, no. 9, September
Gauze,
Formalin
Gauze’ Fig. 2. The Hardy plankton recorder is towed behind ‘ships of opportunity’ at speeds of 12-18 knots, sampling at a depth of about IO m. The mouth opening is I3 mm square. Plankton is collected on bands of silk mesh (mesh aperture 285 pm by 3 I5 urn 1that pass across the throatoftherecorder.In IOnauticalmilesl18km),about 3 m’ of water is filtered. The common large species of phytoplankton and zooplankton are identified and Redrawn from Ref 16. counted.
NE ATLANTIC
NORTH
SEA
Fig. 3. Space-averaged seasonal and interannual variations in the abundance of zooplankton in two sectors of the North Atlantic. Logarithmic contour intervals are indicated by increasing density of stipple. There are strong interannual differences in the magnitude of the seasonal cycle of abundance, as well as regional differences. The trend for a shorter season of abundance, shown here. has since reversed. Redrawn from Ref 19.
294
‘change’ is uncertain in the context of oceanic ecosystems. One obvious way to define ‘change’ is by the use of time series of measurements, from which trends, frequencies, amplitudes and directions of significant departures from long-term means of population sizes and other system components may be calculated. Spectral analyses of such data can give us further insight, as can crossspectral correlations between properties. That is, the behavior of the system in general can be quantitatively described without knowing all of the details of the intermediary mechanisms. If multiple components of physical-chemical-biological systems interact to influence one another’s magnitude and temporal rates of change, and if this happens in a patterned way, there should be detectable statistical relationships between them. Determining such patterns, especially those involving climatic variables (both atmospheric and oceanic) and populations, can give us insight into such questions as ‘which types of atmospheric or hydrographic perturbation affect biotic systems, and which do not?’ There are many kinds of disturbance or perturbation in the ocean ranging from micro-scale turbulence to El Nines (Fig. I) - and almost all of them have been implicated, one way or another, in influencing populations. But some atmosphereocean events seem to result in severe disturbances to species structure, biomass and trophic function, while others do not. Which ones, then, are which? For example, does a single large storm have greater effects on primary and secondary production than, say, a month or two of merely ‘bad’ weather? How long do the effects of El Nina last? How and in what direction do systems respond to different kinds of climatic events5? It seems likely that the mean state of an ecosystem is set by the cumulative effects of environmental variability on many scales, rather than a single one; but if there are multiple steady states, how are shifts between them brought about? That is, is it necessary for driving forces to change on all scales for a shift from one system ‘steady’ state to another? Can we ever pre-
1990
diet the direction and amplitude of such shifts? Have we even described these patchy, oceanic systems sufficiently well to describe their responses to disturbances or to detect change? Time series, especially those where some space averaging is possible, are clearly helpful in the resolution of many of these questions. Only a few such studies have been carried out over the decades necessary to establish baseline means, and to reveal frequencies of oscillation and amplitude of anomalies. Curiously, these studies are limited to the higher trophic levels, such as commercial fish and the larger zooplankton. A few of the larger phytoplankton species have also been studied, but only those that happened to be caught along with zooplankton or those from very nearshore locales6,7. Thus, complete ‘ecosystem’ structure has not been followed through time. There appear to be no comparable time series for phytoplankton nutrients or biomass, for bacteria, protozoa or other microplankton, nor for dissolved organic matter or detritus. We must therefore use limited-size fractions of oceanic communities, chiefly the larger zooplankton. as proxy measures of system states and to detect changes of state. Data from commercial harvests There are long-term data on the catches of commercially valuable fish, and estimates of the sizes of these populations can be derived. But such information cannot be utilized very easily to study the interactions of fish with other populations as they are affected by climate. Furthermore, Garrod and Colebrook have cross-correlated a long series of data on many species and stocks of fish in the North Atlantic, and found that while year-toyear variability in recruitment was great, most of the stocks were uncorrelated with each other. That is, if cooccurring fish populations were responding to climatic variations, they were not doing it in a similar way. In the Pacific there has been a well-documented systematic decline, over four or five decades, in the abundance of the Pacific sardine (Sardinops sagax). Early in this period (about 1942) a very similar, co-occurring fish, the northern an-
TREE vol. 5, no. 9, September 1990
chovy (Engraulis mordax), also began to decline, but by 1953 or so it was evident that the two populations were beginning to behave differently9. The sardine continued its secular decline, while the anchovy began a long-term increase. Neither the sardine’s decrease nor the anchovy’s increase over this period are paralleled by any direct or indirect measure of physical environmental change. Analyses of annual indices of larval abundance, between 195 1 and 1958, for four other species of California Current fish with strongly overlapping distributions - Pacific mackerel (Scomber japonicus), jack mackerel (Trachurus symmetricus), saury and Pacific hake (Co/o/a& saira and Merluccius productus) - show them to be in broad disagreement with one another and with both the sardine and anchovy as to population trendslO. Radovich” has reviewed some of this research on Pacific fishes and reaches the ‘inescapable’ conclusion that it is man’s harvesting that is the chief determinant of sardine population variability, and it seems unlikely that such an effect can be limited to this species alone. Shepherd et af.12, in a review of the many time-series studies of the role of climate in influencing recruitment of young fish to populations, conclude that ‘there is strong evidence, from the long history of fluctuations in abundance and the existence of fairly well defined geographical ranges, that an important relationship must exist between recruitment and climate. Determining the nature and magnitude of the relationship and elucidating the mechanisms involved is, however a most difficult problem.’ The effects of harvesting are complex and basically not well understood, but they may seriously confound our efforts to determine the effects of climate change on these populations. The failures clearly to relate fish population variations to measures of climatic variation were based on ‘modern’ quantitative catch statistics, most of which cover only the past 70 years or so. Cushingls and later Southward eta/.14, using many historical accounts such as The Housekeeper3 Guide to the Fishmarket for Each Month of the Year: and an Account
of the Fisheries
of
Devon and ComwalP5, have pieced together much longer records (1660-1980). They found that ‘the harengusl fishery herring I &pea flourished better in really cold periods and then extends farther to the west along the south coast’ (of Devon and Cornwall), ‘while the warm period in the middle of the present. century saw a great impoverishment of the South Devon Herring Fishery.’ The herring were often replaced by pilchard (Sardina pilchardus) and ‘The hypothesis that pilchards and herring alternate in abundance off the south west, in response to minor fluctuations in climate, is still a reasonable explanation of a large part of the changes since the Sixteenth century.’ Perhaps harvested populations do respond to climatic cycles of very low frequency (about 20-90 years). But it is difficult to obtain frequency spectra, amplitudes of anomalous departures from the mean, or even the means, from the older historical accounts. Therefore relationships with environmental shifts, which are themselves poorly measured, cannot be easily quantified. There are, however, other timeseries studies of oceanic organisms that are not commercially harvested. These series are of high enough frequency and long enough duration to allow some useful statistical interpretations. Atlantictime series The continuous plankton recorder (CPR) surveys of zooplankton and phytoplankton species abundance in the North Atlantic between Scotland and Iceland began in 1939. After World War II, routes to and from the Atlantic Ocean weather ships were added. This survey was extended progressively until by 1965 a large part of the North Atlantic, north of 45”N, was sampled monthly by 20 merchant ships and 16 weather ships (Fig. 2)16J7.In that year, II2 000 miles of continuous sampling was done18. Three early, main results of this effort have been: composite biogeographic maps of spatial variations in species abundance and patterns of diversity in the northern North Atlantic, based on thousands of observations; the derivation of species assemblages and their spatial and temporal trends (i.e. the
1950
1960
1970
1980
Cyclonic weather
,
Ceratium furca
Ceratium horridum
I
L
1960
n
I
1970
n
J
1980%%%%%30
Fig. 4. (a) The low-pass filtered CPR data on total zooplankton and net phytoplankton. There are obvious similarities between trophic levels in long-term trends of abundance. Adapted from Ref. 21. (bl Four species of dinoflagellates showing good agreement among species as to long-term trends in abundance. There are clear relations to climatic variations. Adapted from Ref.
22.
outlines of community structure); and the analysis of temporal variations in the plankton (Fig. 3)19.The power of the latter analyses is greatly enhanced by the availability of so many samples and the ability to space average the data. Much of the more recent work on temporal changes has been done in an area ( IO’E to 2O”w, 45”N to 65”N) in the northeastern Atlantic, the North Sea and the English Channel. This later effort has emphasized the relationships between environmental variations and plankton abundance. The earlier studies of the CPR group were impeded by the lack of physical-chemical data on commensurate scales of sampling. But as time-series information accumulated, it became evident that it was the larger time-space scales that showed the greatest variations (Fig. 4120.Interannual variations were evident and in some cases dominated Continued
on p. 298 295
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by Mike Ashmore Imperial College Centre for Environmental Technology, 48 Prince’s Gardens, London SW7 2PE, UK
There is a balar ce between tk the longwave r, ldiation thsl ii absorbed by ai nospheric ga vapour. Concet I has grown trations of othe radiatively ac as a result of hi man activit e: and intensive a
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Relative Contribution The pie chart illustrates : Environmental Protectio. contribution of the majc global warming over the of individual gases on t-i calculated from a know! concentration of the gas a relationship between cot absorption for that gas, a absorption bands overlap generally agreed that CO, current warming, and tha are the most important of. it should be emphasized estimates, as are man) boxes.
ion received by the earth and of this longwave radiation is most important of which is water years that atmospheric concennhouse’, gases are increasing rgy production, deforestation concentrations may enhance significant changes in the
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Blake, D.R. and Rowland, F.S. (1988) Science 239,112s1131 [tropos@eric CHJ Balin, B., Doos, B.R., Jager, J. and Warrick, R.A., eds (1saS) The GreedhouseEiiFect,C/JmsticChs~gestd ;, John Wiley nd Graedel, T.E. (1986) in Sustdnabie Devekpment of the BirJsphsmn (Clark, W.C. and e Univeit;ity Press [atmospheric chm&tryI 1)ScientJfJcAssessmentofCJimate Change:Reporito Mxking Group 1,WMCVUNEP and Rasmussen, K.A. (1988) Ann. GJscioJ.10,73-79 [N20] nd Ahuja, DR. (lX4g) MS&&e344,KXb531 Id Tirpak, D.A. eds (7989) hi& Opt&w for StabJiizingGlobal CJJmst&Erwirenmentel rrommon Agency, Washington UNEP (1987) The Gmeohouse Gssss, UNEP Wiiey, T.M.L. (l%B) hdptftrne 335,333~335 [CFCsl WuebbteS, D-J., Grant, KX., ConneM,P.S. and Penner, J.E. (1989) J. Air &J/M. Con& Assoc. 39,22-28 -atmosoheric chernietrvl
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3
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TREE vol. 5, no. 9, September 125” I
’
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1990
110
’ may contribute change.
to the process of
Pacific time series
The systematic decline of the Pacific sardine led to the establishment of a large environmental study of the California Current in 1949: the California Cooperative Oceanic Fisheries Investigations (CalCOFI) (Fig. 5). This study resembles the CPR work in some important ways. Both allow for the (all-important) space averaging of time series, both cover large areas and are of over 40 years duration, thus allowing frequencies of change from monthly to decadal to be resolved. Both targeted the larger and more efficiently sampled zooplankton. They differ in that CalCOFl 25” 25” measured physical properties along with biological ones, and did so over a substantial depth range, thus adding another dimension to the study. I “‘I ’ “1 1 ” ” ” ’ “1 J As in the CPR study, species bio110 115 120” 125” geographic patterns and seasonal Fig. 5. The California Cooperative Oceanic Fisheries Investigations (CalCOFI) sampling plan. Since 1949, cycles have been described25. There cruises have covered the area reaching from San Francisco to mid Baja California and about 400 miles is a strong north-south gradient seaward. Each dot represents a station where data were collected: weather observations were made, a in biomass and tin offshore, midhydrographic cast measured physical
TREE vol. 5, no. 9, September
1990
currently being compared to one another and to the background mean, for they serve as one model of what the consequences of largescale warming may be. In both cases there were substantial changes in the upper 100 m or so of the entire system. Both the thermocline and the nutricline deepened, and productivity was greatly diminished. Although some tropical species were transported to the north very near shore, this was not generally true over the entire system. Rather, warm, high-salinity water and its inhabitants intruded from the westsouthwest. This normally occurs in most summers but during the two El NiAos it was greatly exaggerated. In addition to these two great positive temperature anomalies called El Nirios, there were other large, nonseasonal departures from mean conditions; these had other ecosystem signatures. Sorting out the patterns of these climatic events and their ecosystem consequences is not an easy task. But repeatable patterns, as opposed to randomness, do seem to exist, and therefore regulation is strongly implied and prediction a possibility. Conclusion These two time series-one in the Atlantic, the other in the Pacific - do provide bases for the definition of
Satellite measurements and the development of new techniques have confirmed the importance of ocean biology in controlling the carbon dioxide (CO,) content of the atmosphere. The marine sedimentary record shows that climate change and the ocean carbon cycle are closely linked: during glacial periods, marine productivity was enhanced and atmospheric CO, levels were reduced. Global warming may have the oppositeeffect, with reduced uptake of CO, exacerbating the problems of climate change. Marine photosynthesis is responsible fora worldwide annual conversion of 30-50 Gt (billion metric tons: 10’~ g) of carbon from dissolved, inorganic substrates to particulate, Phillip Williamson and Patrick Holligan are at the NERC Plymouth Marine Laboratory, Prospect Place, Plymouth PLI 3DH, UK.
‘change’. Departures from long-term mean conditions can be defined; further, the response of the biota to climatic anomalies can be described in terms of direction, magnitude and frequency. To the degree that large zooplankton can serve as a proxy for the state of the rest of the system, we have achieved some real insight into how climate affects oceanic ecosystems.
Wiley & Sons 12 Shepherd, I.G., Pope, I.G. and Cousens, R.D. (19841 Rapp. P-V. Reun.. Cons. Int. Expior. Mer 185, 255-267 I3 Cushing, D.H. (1982) Climate and Fisheries. Academic Press I4 Southward, A.!., Boalch, C.T. and Maddock, L. ( 1988) /. Mar. Biol. Assoc. UK 68,423-445 I5 Bellamy, l.c. (I8431 The Housekeeper’s Guide to the Fishmarket for Each Month of the Year: and an Account of the Fisheries of Devon and Cornwall, E. Nettleton, Plymouth I6 Hardy, A. (I9561 The Open Sea - Its Natural History - The World of Plankton, Collins
References
I Haury, L.R., McGowan, I.A. and Wiebe, P.H. II9781 in Spatial Patterns in Plankton (Steele, J.H., ed.), pp. 277-327, Communities Plenum Press 2 Stommef, H. (1963) Science 139.572-576 3 Dickinson, R.E. and Cicerone. R.I. 119861 Nature319,109-II5 4 Ramanathan, V. (1988) Science 240, 293-299 5 Wiebe, P.H., Miller, C.B., McGowan, j.A. and Knox, R.A. II9871 Eos 68, 1178-l 190 6 Tont, S.A. II9891 Geophys. Monogr., Am. Geophys. Union 55, 161-163 7 Maddock, L., Harbour, D.S. and Boalch, G.T. ( 1989) /. Mar. Bio/. Assoc. UK 69, 229-244 8 Garrod, D.]. and Colebrook, I.M. (19781 Rapp. P-V. Reun.. Cons. Int. Expior. Mer 173, 128-144 9 Smith, P.E. (1972) Fish. Boll. 70, 849-874 IO MacCall, A.D. and Prager, M.H. (1988) Calif. Coop. Oceanic Fish. Invest. Rep. 29, 91-101 I I Radovich, I. ( 1981 I in Resource Management and Environmental Uncertainty: Lessons from Coastal Upwelling Fisheries IGlanz. M.H. and Thompson, I.D.. edsl, pp. 107-135, john
I7 Oceanographic Laboratory, Edinburgh (1973) Bull. Mar. Ecoi. 7, I-174 I8 Clover, R.S. ( I9671 Symp. Zooi. Sot. London 19, 189-2 IO I9 Colebrook, I.M. (1982) /. Plankton Res. 4, 435-462 20 Dickson, R.R., Kelly, P.M., Colebrook, I.M.. Wooster, W.S. and Cushing. D.H. ( 1988) 1. Plankton Res. IO, 151-169 21 Colebrook. I.M. et ai. ( 1984) 1. Cons. Int. Explor. Mer 4 I, 304-306 22 Colebrook, I.M. and Taylor, A.H. (19841 Rapp. P-V. Reun., Cons. Int. Expior. Mer 183, 20-26 23 Colebrook, j.M. ( 1982) Oceanoi. Acta 5, 473-480 24 Radach, G. II9841 Rapp. P-V. Reun., Cons. lnt. Expior. Mer 185, 234-254 25 Brinton, E. (1976) fish. Bull. 74, 733-762 26 Chelton, D.B., Bemal, P.A. and McGowan, LA. (198211. Mar. Res. 40, 1095-I 125 27 Chelton, D.B. (I981 I Caiif Coop. Oceanic Fish. Invest. Rep. 22, 34-48 28 Bernal, P.A. ( 1979) Caiif Coop. Oceanic Fish. invest. Rep. 20, 89-101 29 Sette, O.E. and Isaacs, I.D. ( 1960) Caiif. Coop. Oceanic Fish. Invest. Rep. 7, l-2 I7 30 McGowan, I.A. ( 1985) in Ei Nifio North (Wooster, W.S. and Fluharty, D.L., edsl, pp. 166-184, University of Washington
OceanProductivityand Climate Change Phillip Williamson and Patrick M. Holligan organic material. As a result of such biogenic carbon fixation in the sunlit surface waters, there is an oceanic drawdown of CO, from the atmosphere of similar magnitude: an amount at least five times greater than the quantity of carbon released to the air by fossil fuel combustion and other human activities’,2. All but a tiny fraction of the organic carbon in marine biomass is subsequently reconverted to CO, (the fate of all life on Earth), adding to the pool of around 35 000 Gt of inorganic carbon within the oceans. Balance is achieved by the release
of a proportion of that carbon pool to the atmosphere, through ocean circulation processes; the nearexactness of that equilibrium is shown by the stability of atmospheric CO, levels over the period IO 000-100 years before present. But many of the factors controlling biologically driven CO, uptake and physically driven CO, release are only loosely coupled, and will be affected in different ways by climate change. There is therefore a strong likelihood that perturbations in the ocean carbon cycle will have a future influence on profound 299
7990
The consequences of climaticchange for the structure and function of oceanic ecosystems are of considera6le current interest. A predictive, mechanistic model of these consequences based on our scanty knowledge of the dynamics of the systems’ con+ ponents seems unlihely: a complex set of simultaneous partial differential equations depicting population interactions and transfer rates of energy and materials would be necessary. A second approach is simply to measure the phenomenologg of variations in both climate and ecosystem components, for the purpose of detecting shared patterns. Two studies of the latter type have 6een done. Both have been successful in revealing relationships Getween climatic variation and large-scale, largeamplitude, low-frequency Giological variability. Both sets of results can provide models for the prediction of consequences, and 60th can serve as Gaselines for the definition of ‘change’.
Populations of pelagic organisms vary on many time-space scales, and much effort has been devoted to describing these variations and to determining their causes. Haury et al.‘, using all available data, constructed a diagram of biomass variability in which both time and space were considered (Fig. I). It shows that oceanic population changes on a small spatial scale are of short duration, and that larger spatial events last longer. There is a rough 45” slope of biomass variability on the log-log plot of time and space. This diagram matches quite well a similar one of physical environmental events in the ocean*. Since this match can hardly be a coincidence, it strongly implies that different biological events happen on different scaies for different physical reasons, and that the izger ones are associated with atmospheric and oceanographic climate. It has become increasingly evident that we must understand these relationships between climate and biota in order to anticipate the consequences of climatic change. There seems to be no question now that humanity has altered the mix of atmospheric gases by increasing those that are active in the process of radiative heating of john McGowan is at the Scripps Institute of Oceanography, University of California, La folla, CA 92093, USA.
fQ 1990
E se”iei
Science Publishers
i!d
IUKi 0169.5347!90602
Climateand Changein Oceanic Ecosystems:The Value of Time-seriesData John A. McGowan Earth. It is predicted that this alteration will change the climate at rates exceeding those of past natural variations. Although there are many uncertainties, it is also likely that the warming will not be uniform but will show significant geographic variation3,4. The warming should change the large-scale general circulation of the atmosphere and the oceans, but the geographic variation should result in numerous and perhaps intense episodic regional and mesoscale perturbations as well. Such events will probably be evident as large and significant nonseasonal positive and negative anomalies from regional means of environmental conditions and, therefore, result in numerous ecosystem disturbances on many scales. The consequences of such disturbances will be very difficult to predict on the basis of our current
knowledge of the structure of food webs and the functional relationships between the components of these webs. These systems are complex, especially in such a mobile environment as the ocean, and are not necessarily at steady state when we measure them. The numerous nonlinear functional relationships between system components may make it impossible to model such systems for arbitrarily long forecast times. Further, the mechanisms by which climatic variations affect many aspects of population biology and the transfer of energy and materials between populations are not well known. All of this makes it unlikely that models based on functional interrelationships of numerous, individual system components can be used soon for the study of ecosystem change. Even the very definition of the word
ICE-AGE VARIATIONS
Fig. I. A conceptual model of the time-space scales of variations in zooplankton biomass, and an indication of the factors contributing to them. A, ‘micro’ patches. B, swarms. C, upwelling. D, eddies and rings. E, island effects. F, ‘El Nitio’ type events. G, small ocean basins. H, biogeographic provinces. I, currents and oceanic fronts - length. I, currents-width. K, oceanic fronts-width. Adapted from Ref. I.
00
293
TREE vol. 5, no. 9, September
Gauze,
Formalin
Gauze’ Fig. 2. The Hardy plankton recorder is towed behind ‘ships of opportunity’ at speeds of 12-18 knots, sampling at a depth of about IO m. The mouth opening is I3 mm square. Plankton is collected on bands of silk mesh (mesh aperture 285 pm by 3 I5 urn 1that pass across the throatoftherecorder.In IOnauticalmilesl18km),about 3 m’ of water is filtered. The common large species of phytoplankton and zooplankton are identified and Redrawn from Ref 16. counted.
NE ATLANTIC
NORTH
SEA
Fig. 3. Space-averaged seasonal and interannual variations in the abundance of zooplankton in two sectors of the North Atlantic. Logarithmic contour intervals are indicated by increasing density of stipple. There are strong interannual differences in the magnitude of the seasonal cycle of abundance, as well as regional differences. The trend for a shorter season of abundance, shown here. has since reversed. Redrawn from Ref 19.
294
‘change’ is uncertain in the context of oceanic ecosystems. One obvious way to define ‘change’ is by the use of time series of measurements, from which trends, frequencies, amplitudes and directions of significant departures from long-term means of population sizes and other system components may be calculated. Spectral analyses of such data can give us further insight, as can crossspectral correlations between properties. That is, the behavior of the system in general can be quantitatively described without knowing all of the details of the intermediary mechanisms. If multiple components of physical-chemical-biological systems interact to influence one another’s magnitude and temporal rates of change, and if this happens in a patterned way, there should be detectable statistical relationships between them. Determining such patterns, especially those involving climatic variables (both atmospheric and oceanic) and populations, can give us insight into such questions as ‘which types of atmospheric or hydrographic perturbation affect biotic systems, and which do not?’ There are many kinds of disturbance or perturbation in the ocean ranging from micro-scale turbulence to El Nines (Fig. I) - and almost all of them have been implicated, one way or another, in influencing populations. But some atmosphereocean events seem to result in severe disturbances to species structure, biomass and trophic function, while others do not. Which ones, then, are which? For example, does a single large storm have greater effects on primary and secondary production than, say, a month or two of merely ‘bad’ weather? How long do the effects of El Nina last? How and in what direction do systems respond to different kinds of climatic events5? It seems likely that the mean state of an ecosystem is set by the cumulative effects of environmental variability on many scales, rather than a single one; but if there are multiple steady states, how are shifts between them brought about? That is, is it necessary for driving forces to change on all scales for a shift from one system ‘steady’ state to another? Can we ever pre-
1990
diet the direction and amplitude of such shifts? Have we even described these patchy, oceanic systems sufficiently well to describe their responses to disturbances or to detect change? Time series, especially those where some space averaging is possible, are clearly helpful in the resolution of many of these questions. Only a few such studies have been carried out over the decades necessary to establish baseline means, and to reveal frequencies of oscillation and amplitude of anomalies. Curiously, these studies are limited to the higher trophic levels, such as commercial fish and the larger zooplankton. A few of the larger phytoplankton species have also been studied, but only those that happened to be caught along with zooplankton or those from very nearshore locales6,7. Thus, complete ‘ecosystem’ structure has not been followed through time. There appear to be no comparable time series for phytoplankton nutrients or biomass, for bacteria, protozoa or other microplankton, nor for dissolved organic matter or detritus. We must therefore use limited-size fractions of oceanic communities, chiefly the larger zooplankton. as proxy measures of system states and to detect changes of state. Data from commercial harvests There are long-term data on the catches of commercially valuable fish, and estimates of the sizes of these populations can be derived. But such information cannot be utilized very easily to study the interactions of fish with other populations as they are affected by climate. Furthermore, Garrod and Colebrook have cross-correlated a long series of data on many species and stocks of fish in the North Atlantic, and found that while year-toyear variability in recruitment was great, most of the stocks were uncorrelated with each other. That is, if cooccurring fish populations were responding to climatic variations, they were not doing it in a similar way. In the Pacific there has been a well-documented systematic decline, over four or five decades, in the abundance of the Pacific sardine (Sardinops sagax). Early in this period (about 1942) a very similar, co-occurring fish, the northern an-
TREE vol. 5, no. 9, September 1990
chovy (Engraulis mordax), also began to decline, but by 1953 or so it was evident that the two populations were beginning to behave differently9. The sardine continued its secular decline, while the anchovy began a long-term increase. Neither the sardine’s decrease nor the anchovy’s increase over this period are paralleled by any direct or indirect measure of physical environmental change. Analyses of annual indices of larval abundance, between 195 1 and 1958, for four other species of California Current fish with strongly overlapping distributions - Pacific mackerel (Scomber japonicus), jack mackerel (Trachurus symmetricus), saury and Pacific hake (Co/o/a& saira and Merluccius productus) - show them to be in broad disagreement with one another and with both the sardine and anchovy as to population trendslO. Radovich” has reviewed some of this research on Pacific fishes and reaches the ‘inescapable’ conclusion that it is man’s harvesting that is the chief determinant of sardine population variability, and it seems unlikely that such an effect can be limited to this species alone. Shepherd et af.12, in a review of the many time-series studies of the role of climate in influencing recruitment of young fish to populations, conclude that ‘there is strong evidence, from the long history of fluctuations in abundance and the existence of fairly well defined geographical ranges, that an important relationship must exist between recruitment and climate. Determining the nature and magnitude of the relationship and elucidating the mechanisms involved is, however a most difficult problem.’ The effects of harvesting are complex and basically not well understood, but they may seriously confound our efforts to determine the effects of climate change on these populations. The failures clearly to relate fish population variations to measures of climatic variation were based on ‘modern’ quantitative catch statistics, most of which cover only the past 70 years or so. Cushingls and later Southward eta/.14, using many historical accounts such as The Housekeeper3 Guide to the Fishmarket for Each Month of the Year: and an Account
of the Fisheries
of
Devon and ComwalP5, have pieced together much longer records (1660-1980). They found that ‘the harengusl fishery herring I &pea flourished better in really cold periods and then extends farther to the west along the south coast’ (of Devon and Cornwall), ‘while the warm period in the middle of the present. century saw a great impoverishment of the South Devon Herring Fishery.’ The herring were often replaced by pilchard (Sardina pilchardus) and ‘The hypothesis that pilchards and herring alternate in abundance off the south west, in response to minor fluctuations in climate, is still a reasonable explanation of a large part of the changes since the Sixteenth century.’ Perhaps harvested populations do respond to climatic cycles of very low frequency (about 20-90 years). But it is difficult to obtain frequency spectra, amplitudes of anomalous departures from the mean, or even the means, from the older historical accounts. Therefore relationships with environmental shifts, which are themselves poorly measured, cannot be easily quantified. There are, however, other timeseries studies of oceanic organisms that are not commercially harvested. These series are of high enough frequency and long enough duration to allow some useful statistical interpretations. Atlantictime series The continuous plankton recorder (CPR) surveys of zooplankton and phytoplankton species abundance in the North Atlantic between Scotland and Iceland began in 1939. After World War II, routes to and from the Atlantic Ocean weather ships were added. This survey was extended progressively until by 1965 a large part of the North Atlantic, north of 45”N, was sampled monthly by 20 merchant ships and 16 weather ships (Fig. 2)16J7.In that year, II2 000 miles of continuous sampling was done18. Three early, main results of this effort have been: composite biogeographic maps of spatial variations in species abundance and patterns of diversity in the northern North Atlantic, based on thousands of observations; the derivation of species assemblages and their spatial and temporal trends (i.e. the
1950
1960
1970
1980
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,
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Ceratium horridum
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L
1960
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1970
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Fig. 4. (a) The low-pass filtered CPR data on total zooplankton and net phytoplankton. There are obvious similarities between trophic levels in long-term trends of abundance. Adapted from Ref. 21. (bl Four species of dinoflagellates showing good agreement among species as to long-term trends in abundance. There are clear relations to climatic variations. Adapted from Ref.
22.
outlines of community structure); and the analysis of temporal variations in the plankton (Fig. 3)19.The power of the latter analyses is greatly enhanced by the availability of so many samples and the ability to space average the data. Much of the more recent work on temporal changes has been done in an area ( IO’E to 2O”w, 45”N to 65”N) in the northeastern Atlantic, the North Sea and the English Channel. This later effort has emphasized the relationships between environmental variations and plankton abundance. The earlier studies of the CPR group were impeded by the lack of physical-chemical data on commensurate scales of sampling. But as time-series information accumulated, it became evident that it was the larger time-space scales that showed the greatest variations (Fig. 4120.Interannual variations were evident and in some cases dominated Continued
on p. 298 295
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There is a balar ce between tk the longwave r, ldiation thsl ii absorbed by ai nospheric ga vapour. Concet I has grown trations of othe radiatively ac as a result of hi man activit e: and intensive a
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ion received by the earth and of this longwave radiation is most important of which is water years that atmospheric concennhouse’, gases are increasing rgy production, deforestation concentrations may enhance significant changes in the
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Blake, D.R. and Rowland, F.S. (1988) Science 239,112s1131 [tropos@eric CHJ Balin, B., Doos, B.R., Jager, J. and Warrick, R.A., eds (1saS) The GreedhouseEiiFect,C/JmsticChs~gestd ;, John Wiley nd Graedel, T.E. (1986) in Sustdnabie Devekpment of the BirJsphsmn (Clark, W.C. and e Univeit;ity Press [atmospheric chm&tryI 1)ScientJfJcAssessmentofCJimate Change:Reporito Mxking Group 1,WMCVUNEP and Rasmussen, K.A. (1988) Ann. GJscioJ.10,73-79 [N20] nd Ahuja, DR. (lX4g) MS&&e344,KXb531 Id Tirpak, D.A. eds (7989) hi& Opt&w for StabJiizingGlobal CJJmst&Erwirenmentel rrommon Agency, Washington UNEP (1987) The Gmeohouse Gssss, UNEP Wiiey, T.M.L. (l%B) hdptftrne 335,333~335 [CFCsl WuebbteS, D-J., Grant, KX., ConneM,P.S. and Penner, J.E. (1989) J. Air &J/M. Con& Assoc. 39,22-28 -atmosoheric chernietrvl
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TREE vol. 5, no. 9, September 125” I
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The systematic decline of the Pacific sardine led to the establishment of a large environmental study of the California Current in 1949: the California Cooperative Oceanic Fisheries Investigations (CalCOFI) (Fig. 5). This study resembles the CPR work in some important ways. Both allow for the (all-important) space averaging of time series, both cover large areas and are of over 40 years duration, thus allowing frequencies of change from monthly to decadal to be resolved. Both targeted the larger and more efficiently sampled zooplankton. They differ in that CalCOFl 25” 25” measured physical properties along with biological ones, and did so over a substantial depth range, thus adding another dimension to the study. I “‘I ’ “1 1 ” ” ” ’ “1 J As in the CPR study, species bio110 115 120” 125” geographic patterns and seasonal Fig. 5. The California Cooperative Oceanic Fisheries Investigations (CalCOFI) sampling plan. Since 1949, cycles have been described25. There cruises have covered the area reaching from San Francisco to mid Baja California and about 400 miles is a strong north-south gradient seaward. Each dot represents a station where data were collected: weather observations were made, a in biomass and tin offshore, midhydrographic cast measured physical
TREE vol. 5, no. 9, September
1990
currently being compared to one another and to the background mean, for they serve as one model of what the consequences of largescale warming may be. In both cases there were substantial changes in the upper 100 m or so of the entire system. Both the thermocline and the nutricline deepened, and productivity was greatly diminished. Although some tropical species were transported to the north very near shore, this was not generally true over the entire system. Rather, warm, high-salinity water and its inhabitants intruded from the westsouthwest. This normally occurs in most summers but during the two El NiAos it was greatly exaggerated. In addition to these two great positive temperature anomalies called El Nirios, there were other large, nonseasonal departures from mean conditions; these had other ecosystem signatures. Sorting out the patterns of these climatic events and their ecosystem consequences is not an easy task. But repeatable patterns, as opposed to randomness, do seem to exist, and therefore regulation is strongly implied and prediction a possibility. Conclusion These two time series-one in the Atlantic, the other in the Pacific - do provide bases for the definition of
Satellite measurements and the development of new techniques have confirmed the importance of ocean biology in controlling the carbon dioxide (CO,) content of the atmosphere. The marine sedimentary record shows that climate change and the ocean carbon cycle are closely linked: during glacial periods, marine productivity was enhanced and atmospheric CO, levels were reduced. Global warming may have the oppositeeffect, with reduced uptake of CO, exacerbating the problems of climate change. Marine photosynthesis is responsible fora worldwide annual conversion of 30-50 Gt (billion metric tons: 10’~ g) of carbon from dissolved, inorganic substrates to particulate, Phillip Williamson and Patrick Holligan are at the NERC Plymouth Marine Laboratory, Prospect Place, Plymouth PLI 3DH, UK.
‘change’. Departures from long-term mean conditions can be defined; further, the response of the biota to climatic anomalies can be described in terms of direction, magnitude and frequency. To the degree that large zooplankton can serve as a proxy for the state of the rest of the system, we have achieved some real insight into how climate affects oceanic ecosystems.
Wiley & Sons 12 Shepherd, I.G., Pope, I.G. and Cousens, R.D. (19841 Rapp. P-V. Reun.. Cons. Int. Expior. Mer 185, 255-267 I3 Cushing, D.H. (1982) Climate and Fisheries. Academic Press I4 Southward, A.!., Boalch, C.T. and Maddock, L. ( 1988) /. Mar. Biol. Assoc. UK 68,423-445 I5 Bellamy, l.c. (I8431 The Housekeeper’s Guide to the Fishmarket for Each Month of the Year: and an Account of the Fisheries of Devon and Cornwall, E. Nettleton, Plymouth I6 Hardy, A. (I9561 The Open Sea - Its Natural History - The World of Plankton, Collins
References
I Haury, L.R., McGowan, I.A. and Wiebe, P.H. II9781 in Spatial Patterns in Plankton (Steele, J.H., ed.), pp. 277-327, Communities Plenum Press 2 Stommef, H. (1963) Science 139.572-576 3 Dickinson, R.E. and Cicerone. R.I. 119861 Nature319,109-II5 4 Ramanathan, V. (1988) Science 240, 293-299 5 Wiebe, P.H., Miller, C.B., McGowan, j.A. and Knox, R.A. II9871 Eos 68, 1178-l 190 6 Tont, S.A. II9891 Geophys. Monogr., Am. Geophys. Union 55, 161-163 7 Maddock, L., Harbour, D.S. and Boalch, G.T. ( 1989) /. Mar. Bio/. Assoc. UK 69, 229-244 8 Garrod, D.]. and Colebrook, I.M. (19781 Rapp. P-V. Reun.. Cons. Int. Expior. Mer 173, 128-144 9 Smith, P.E. (1972) Fish. Boll. 70, 849-874 IO MacCall, A.D. and Prager, M.H. (1988) Calif. Coop. Oceanic Fish. Invest. Rep. 29, 91-101 I I Radovich, I. ( 1981 I in Resource Management and Environmental Uncertainty: Lessons from Coastal Upwelling Fisheries IGlanz. M.H. and Thompson, I.D.. edsl, pp. 107-135, john
I7 Oceanographic Laboratory, Edinburgh (1973) Bull. Mar. Ecoi. 7, I-174 I8 Clover, R.S. ( I9671 Symp. Zooi. Sot. London 19, 189-2 IO I9 Colebrook, I.M. (1982) /. Plankton Res. 4, 435-462 20 Dickson, R.R., Kelly, P.M., Colebrook, I.M.. Wooster, W.S. and Cushing. D.H. ( 1988) 1. Plankton Res. IO, 151-169 21 Colebrook. I.M. et ai. ( 1984) 1. Cons. Int. Explor. Mer 4 I, 304-306 22 Colebrook, I.M. and Taylor, A.H. (19841 Rapp. P-V. Reun., Cons. Int. Expior. Mer 183, 20-26 23 Colebrook, j.M. ( 1982) Oceanoi. Acta 5, 473-480 24 Radach, G. II9841 Rapp. P-V. Reun., Cons. lnt. Expior. Mer 185, 234-254 25 Brinton, E. (1976) fish. Bull. 74, 733-762 26 Chelton, D.B., Bemal, P.A. and McGowan, LA. (198211. Mar. Res. 40, 1095-I 125 27 Chelton, D.B. (I981 I Caiif Coop. Oceanic Fish. Invest. Rep. 22, 34-48 28 Bernal, P.A. ( 1979) Caiif Coop. Oceanic Fish. invest. Rep. 20, 89-101 29 Sette, O.E. and Isaacs, I.D. ( 1960) Caiif. Coop. Oceanic Fish. Invest. Rep. 7, l-2 I7 30 McGowan, I.A. ( 1985) in Ei Nifio North (Wooster, W.S. and Fluharty, D.L., edsl, pp. 166-184, University of Washington
OceanProductivityand Climate Change Phillip Williamson and Patrick M. Holligan organic material. As a result of such biogenic carbon fixation in the sunlit surface waters, there is an oceanic drawdown of CO, from the atmosphere of similar magnitude: an amount at least five times greater than the quantity of carbon released to the air by fossil fuel combustion and other human activities’,2. All but a tiny fraction of the organic carbon in marine biomass is subsequently reconverted to CO, (the fate of all life on Earth), adding to the pool of around 35 000 Gt of inorganic carbon within the oceans. Balance is achieved by the release
of a proportion of that carbon pool to the atmosphere, through ocean circulation processes; the nearexactness of that equilibrium is shown by the stability of atmospheric CO, levels over the period IO 000-100 years before present. But many of the factors controlling biologically driven CO, uptake and physically driven CO, release are only loosely coupled, and will be affected in different ways by climate change. There is therefore a strong likelihood that perturbations in the ocean carbon cycle will have a future influence on profound 299