Climate change, nutrient pollution and the bargain of Dr Faustus



    1. School of Biological Sciences, University of Liverpool, Liverpool, U.K.
      (With an Appendix by David Atkinson & Brian Moss) School of Biological Sciences, University of Liverpool, Liverpool, U.K.
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Brian Moss, School of Biological Sciences, University of Liverpool, Liverpool, U.K. E-mail:


1. The legend of Dr Faustus crops up repeatedly in European literature, drama and music, suggesting that it has profound meaning. In our relationship with the biosphere we have perhaps made a Faustian bargain. In return for unrestrained use of the Earth’s resources, we may have mortgaged a long-term future. Currently we are hoping to renegotiate the bargain, but there is detail in the small-print-clauses about climate change, destruction of ecosystems and consequent release of nutrients to waterways that we have ignored. Natural biomes determine that the biosphere is maintained in a state favourable to our particular biochemistry. Part of the mechanism is regulation of atmospheric gas composition through storage of carbon as biological deposits.

2. Shallow lakes and wetlands, and the tundras and forests of wet soil, store carbon at a much greater rate than the global ocean. The influence, on shallow lake systems, of warming coupled with degrees of eutrophication has been studied in replicated experimental ponds. The first experiment used modest nutrient addition and a 3 °C rise in temperature. Such warming led to some increase in phosphorus availability, takeover by an introduced warm-water species, Lagarosiphon major of the submerged plant community, and an increase in the frequency of severe deoxygenation, with occasional fish kills.

3. The second experiment used a rise of 4 °C against a similar ambient background to that of the first experiment, but a nutrient environment much closer to that of lowland eutrophicated waters. Especially with moderate nitrogen loading, floating duckweeds became very abundant, though submerged plants persisted. Oxygen concentrations fell markedly. Final fish biomass fell by 60% on warming and 80% at the highest nutrient loading used, but the combination of warming and even modest nutrients brought oxygen frequently to zero overnight and killed all the fish. Because the fish used (Gasterosteus aculeatus) were extremely resilient, there are severe implications for many other European fish species.

4. Analysis of oxygen curves allowed calculation of metabolic parameters of the tank systems. Both warming and nutrient addition substantially increased community respiration compared with photosynthesis. Extrapolation suggests that if this phenomenon is widespread, an increase of about 1.8 Gt over the 1990’s net annual atmospheric accumulation rate of 3.2 Gt might result. Since the IPCC models of future climate change do not include such biological feedbacks, they may thus seriously underestimate the future rise in temperature and its consequences.

5. Thematic implications: we do not know if our Faustian bargain can be renegotiated; our political and social institutions are poorly equipped in knowledge and barely accept the importance of biosphere processes, and our scientific establishment is reductionist and conforms to the values of the rest of society. Current approaches to mitigation of climate change attend only to carbon release from human institutions, with little or no reference to natural systems. The future is exceptionally uncertain.


In 1941, perhaps the most perceptive but equally, pragmatic, of conservationists, the academic, forester, administrator and farmer, Aldo Leopold, wrote that:

“One of the penalties of an ecological education is that one lives alone in a world of wounds. Much of the damage inflicted on land is quite invisible to laymen. An ecologist must either harden his shell and make believe that the consequences of science are none of his business, or he must be the doctor who sees the marks of death in a community that believes itself well and does not want to be told otherwise”. (Leopold, 1972).

In a world now with many more ecologists, some of us can still feel similarly alone. Almost daily, the quality newspapers either report some new manifestation of climate change, a government plan to mitigate it, or a commercial proposal to exploit it. Usually it is seen entirely within a context in which human societies have caused the problem mostly by burning fossil fuels, and in which adjustments to human society through the classic economic system of Adam Smith, John Maynard Keynes and Milton Freedman will bring delivery. What are ignored are that the classic economic system is fatally flawed by excluding, as externalities, the costs of environmental damage, and that we as ecologists have been unable or unwilling to convey the concept that humans are only part, indeed a parasitic part at present, of a biosphere that supports us as a host. The economists’ anthropocentric view is that we can simply exploit this system as its controllers and masters and merely need to change the way, but not the extent, in and to which we exploit it. This derives from the traditional view of the sciences that physics and chemistry determine the platform on which biological events take place and that the platform is a feature that cannot ultimately be permanently damaged or removed. It is a manifestation of the view of the middle twentieth century that physics was a vastly superior science to biology, which was categorised by Ernest Rutherford (in Birks, 1962) as merely the collecting of stamps.

The biocentric view is that that the biosphere is maintained in a chemical state, equable to living organisms, through the activities of the organisms themselves and that conditions at the surface of the Earth, although conforming, of course, to the fundamental laws of chemistry and physics, are manifestations of the primacy of biology (Lovelock, 1965, 1979; Margulis & Lovelock, 1974). Such a system is resilient but not necessarily permanent in any one of its possible states. Biospheres are conceivable, and have already existed for very long periods, that are anaerobic, or dominated by microorganisms, or completely lacking vertebrates or mammals, or us. As a scientific community we still cling to the anthropocentric view by adopting its mores in the way that we organise ourselves. Despite our words, our actions betray us; hence my continued feeling of aloneness.

The biocentric view was originally couched in terms of a super-organism whose components deliberately co-operated. The concept was christened ‘Gaia’ by the author William Golding and vigorously attacked by biologists who could not reconcile it with the well-established primacy of natural selection in determining the activities of organisms (Dawkins, 1976, 1986). Altruistic behaviour towards other organisms does not seem to occur unless genes are shared. Couched simply in terms that do not imply super-organism status or deliberate co-operation, which is the present position, the manifestation of biological determination of the nature of the biosphere seems self-evident. We most certainly do have a non-equilibrium composition of the atmosphere and ocean and non-equilibrium states cannot be maintained by simple chemical systems, only by flexible processing systems that use energy to oppose equilibrium by continually opposing a tendency to increased entropy. Such is life.

The bargain of Dr Faustus

If, by suggesting, however inadvertently, mystical status to the biocentric view through a Greek goddess to characterise it, William Golding did it a disservice. It is not the real nature of the arts and sciences to be so polarised as C.P. Snow (1959) argued in his book ‘The Two Cultures and the Scientific Revolution’. Science explains mechanisms, but the arts can give meaning to them. Since 1587, and probably before that, the story of Dr Faustus has repeatedly been adopted in art, music and literature. The latest has been the use by Monbiot (2007) of quotations from the sixteenth century play by Christopher Marlowe to head the chapters of his book on climate change problems and their possible solutions. Faustus, or Faust, is usually portrayed as a learned man who desired to know everything, to enjoy all the delights that the world can offer and to have complete control over them. He enters into a bargain with Mephistopheles, the devil, that he may have these things in return for the devil’s possession of his soul after his death in 24 years. Faust believes that he will not be called upon to meet his share of the bargain for he does not, a mediaeval man, expect to live that long. Faust epitomises all of us, save those of exceptionally rare saintliness. In our relationships with our environment we appear to have entered a Faustian bargain. We have raped the resources of the Earth and expect to carry on doing so, but many indicators now suggest that the metaphorical 24 years are coming to an end and the mortgage must be redeemed.

Items of small print

We have glossed over three interlinked codicils of small print in this mortgage. They are labelled climate change, ecosystem destruction, and nutrient pollution. Together they add up to a loss of biosphere services and it is with their linked consequences that I am particularly concerned here. Climate change needs little introduction following the widespread acceptance of the reports of the Intergovernmental Panel on Climate Change (IPCC) in 2007. Carbon dioxide concentrations have risen from a pre-industrial 260 ppm to a current 380 ppm, alongside recent increases of other greenhouse gases such as methane and nitrous oxide. This has led to a mean global temperature increase of about 0.63 °C, a sea level rise of 20 cm and a reduction in summer north polar ice cover of 5–6%. That the current changes are mostly caused by human activities is little disputed and physical models give some indication of what future temperatures and precipitation are likely to be, given particular scenarios of mitigation by restriction of fossil fuel use by human societies. Restriction of carbon dioxide equivalent concentrations (i.e. including the effects of other greenhouse gases) to around 480 ppm will limit the increase to around 2 °C, which is believed to be problematic but tolerable. However, present proposals for restriction are most unlikely to hold carbon dioxide-equivalent concentrations to lower than 560 ppm, with a 3–4 °C rise. This brings predicted effects to within the range described as catastrophic in a report (Stern, 2006) commissioned by the U.K. Treasury. There is also a major problem that the IPCC (2007) scenarios assume an anthropocentric view of the biosphere. They do not fully allow for biological feedbacks, such as changed rates of photosynthesis or respiration, which might conceivably ameliorate or worsen the consequences predicted by the purely physical models.

The second codicil concerns destruction of ecosystems and clearly has bearing on possible biological feedbacks. Millennium Ecosystem Assessment (2004) quantifies existing and projected destruction of natural ecosystems through agriculture, urbanisation and other forms of exploitation. Apart from the tundra and boreal forest, which remain reasonably intact (courtesy of the consequences of mosquitoes and blackfly for comfortable living) around 70% of all other terrestrial ecosystems will have been destroyed by 2070, together with their abilities to regulate conditions in the biosphere. The oceans will also have been significantly damaged, not least through a rise in pH (Fabry et al., 2008; Guinotte & Fabry, 2008) as a substantial part of the emitted carbon dioxide dissolves. This threatens precipitation of carbon as calcites in corals and planktonic coccolithophorid algae or foraminiferids. Apart from the major loss of biodiversity, we have no idea how much of these systems we can damage without serious consequences for maintenance of the equable non-equilibrium compositions of the atmosphere and oceans. All that can be said is that the remaining systems have been only partly capable of absorbing carbon dioxide released from fossil fuel burning. Of the emissions of 6.4 Gt C year−1 in the 1990s, the oceans absorbed 2.2 and 3.2 Gt C year−1 accumulated in the atmosphere (IPCC, 2007, based on Mikaloff Fletcher et al., 2006 and others). Destruction of forests released 1.6 Gt C year−1 and the budget is balanced by assuming that around 2.6 Gt C year−1 are absorbed in terrestrial ecosystems and stored in wood, soils, sediments and peats. Currently the fossil fuel emissions have risen to 7.2 Gt C year−1 and the net terrestrial sink, estimated as 0.3 in the 1980s and rising to a net 1.0 (2.6−1.6) in the 1990s is believed to be falling and now around 0.9 Gt C year−1 giving a net increase in the atmosphere of 4.1 Gt C year−1 (Reay et al., 2007). We have no idea what the carbon budget of agricultural land is, in comparison with the natural systems it replaced, and the expanding urban areas are inevitably net emitters.

Ecosystem destruction also removes mechanisms that conserve nutrients like nitrogen and phosphorus compounds. In the 1960s, classic experiments at the Hubbard Brook experimental forest (Likens et al., 1970) showed that substantial leakage of soluble ions like Ca, K and NO3 followed clear-cutting, and every survey of rivers and lakes in agricultural and urban areas shows concentrations of N and P orders of magnitude greater than those recorded from catchments with intact natural ecosystems (Smith, Alexander & Schwarz, 2003). Eutrophication is a world-wide problem carrying with it not only reduction in the biodiversity and characteristic biological structure of river and lake systems but also substantial costs to human societies (Pretty et al., 2003b). Increasingly there is concern about the effects of a doubling of the amounts of fixed nitrogen in the biosphere owing to human activities (Vitousek et al., 1997).

If natural systems are destroyed, so too are the regulating mechanisms they provide as ecosystem services. This latter term is now widely used but carries with it, such is the power of words, the implication that the biosphere is there to provide goods and services. A better term is ‘biosphere regulator’. No regulator mechanism can be said to be of greater importance than others in a mutually regulated system, especially when we only modestly understand how the biosphere functions, but in terms of climate change, carbon storage is of obvious importance, for example in maintenance of atmospheric oxygen concentrations. The level of oxygen in the atmosphere appears to be no accident. At concentrations much above 21%, even wet vegetation becomes inflammable (Watson, Lovelock & Margulis, 1978) and much below it, the diffusion rates are inadequate for survival of animals bigger than large insects (Storz & Moriyama, 2008). Oxygen concentrations have been kept up towards 21% by a slight excess of global gross photosynthesis over community respiration, represented by carbon storage in soils and sediments. They are tempered down to 21% by production of reactive gases such as methane, dimethyl sulphide, and methyl iodide, biologically produced, released in very large quantities on a global basis, but with very short residence times in the atmosphere (Beerling et al., 2007). These mechanisms incidentally hold carbon dioxide concentration down to a small fraction of that predicted from chemical equilibrium models (Lovelock, 1979). The large amount of oxygen now in the atmosphere must be balanced by a colossal storage in limestones as carbonate for it cannot be accounted for by an equivalent amount of fossil organic storage. There are about 37.5 × 1018 mol of oxygen in the atmosphere (Charlson & Emerson, 2000), but only about 1.7 × 1012 mol of carbon stored in fossil organic carbon deposits (used, known and projected stocks of oil, gas and coal), and 14 × 1016 in peats and ocean sediments (Holmen, 2000). There are estimated to be 7.5 × 1021 mol of carbon stored as inorganic sediments (Sundguist, 1993). Recently stored organic matter, however, is of great importance in relation to carbon dioxide flux, where comparatively small quantities are involved. The state of stored organic matter is thus a matter of great interest as climate changes and the issues of climate change, ecosystem destruction, nutrient pollution and biosphere regulation have to be seen as a whole, not as separate problems. Shallow lakes and wetlands epitomise this integration.

Shallow lakes and wetlands

Particularly important in carbon storage are the sediments and peats of shallow lakes and wetlands. The naturally deoxygenated interstitial water preserves organic matter more efficiently than in aerated soils. Shallow lakes and wetlands are also extensive, particularly in the boreal zone and wet tropics and of considerable importance in the economies of many traditional peoples through fisheries and wetland products (Dugan, 1994). A very large proportion of the Earth’s lake area is in shallow and small bodies (Downing et al., 2006), far more than in large deep lakes that have received rather more scientific attention. Moreover, the rate of storage of organic carbon in shallow lake and wetland sediments is several orders of magnitude greater than in deeper bodies, including the ocean (Downing et al., 2008). This is presumably because organic matter becomes metabolised on it its lengthy journey through deep and oxygenated waters, whilst it can be rapidly buried in anaerobic sediments in shallow ones. It would seem that the hitherto apparently esoteric area of shallow lake research is not the railway sidings, but the main line.

In recent years, much work has been carried out, based on large-scale surveys, mesocosm experiments and whole-lake experiments in investigating the effects of eutrophication on shallow wetland lakes. These systems have been central to thinking of thresholds and tipping points of change for they may switch rapidly from biodiverse, clear water plant-dominated systems to turbid phytoplankton-dominated systems (Balls, Moss & Irvine, 1989; Irvine, Moss & Balls, 1989; Scheffer et al.,1993). One school of thought sees this as directly a function of increased nutrients acting as drivers (Scheffer, 1998). An alternative sees nutrients as unable alone to cause the switch, but nutrients to influence the magnitude of thresholds at which other drivers such as herbicides, biocides, salinity, grazing by birds or fish, or water level change become effective (Moss, Madgwick & Phillips, 1996; Moss, 2007). Reverse switches, such as deliberate removal of fish for a period may be used to return the system back to clear water and plant dominance, and again, one school sees nutrient reduction as enough to do this, which may be so if the reduction is extreme, whereas the other sees the usually modest levels of reduction possible to be inadequate without other measures such as biomanipulation (Moss et al., 1996) or intrinsic changes in the fish community (Jeppesen et al., 2005). In either case, however, nutrients have a role, so it is of interest to predict what effects global temperature increase might have on systems already under substantial threat of eutrophication.

Such interactions are most easily teased out using controlled and replicated experimental systems; indeed it is difficult to envisage any other way of understanding the mechanisms. Experiments on whole lakes in which temperature is manipulated are inconceivable. The energy costs would be prodigious. Use of mesocosms that are electrically heated within lakes is possible and is a feature of experiments in Switzerland (M. Gessner, personal communication). Tanks, however are much easier to use and two sets of tanks systems, in Denmark (Liboriussen et al. (2005) and the U.K. (Mckee et al., 2000) are currently producing results that illuminate the interactions between temperature increase, nutrient loading and fish population.

U.K. climate tank experiments

Two major experiments have been carried out in the U.K. (Table 1), one in 1998–2000 (McKee et al., 2002, 2003; Moss et al.,2003), the second in 2005–2007 (unpublished data of H. Feuchtmayr, R. J. Moran, D.Atkinson, I. Harvey, K.J. Hatton, L. Connor and B. Moss). In both cases twelve treatments, quadrupally replicated in 3-m3 tanks, were used in a randomised block design and analysed largely by repeated measures anova. Both had fish (sticklebacks, Gasterosteus aculeatus) and no fish treatments. In the first experiment a 3 °C-temperature rise, compared with ambient temperatures, throughout the year, or only in summer, was used. In the second experiment, ambient temperature and a 4 °C increase, all year, were used. Three nutrient treatments in the first experiment reflected no additional nutrients, a very modest enrichment and a moderate enrichment, with a sediment that was low (around 2%) in organic matter. The second experiment used a richer sediment (8% organic matter, though at the lower end of the range for shallow lake sediments, a no-added-nutrient treatment, and two nutrient loadings that straddled that given in the first experiment. In short the first experiment used a relatively lower temperature increase under conditions of low eutrophication, the second a higher increase with greater nutrient loading, but all within expected temperature increases and relevant states of eutrophication.

Table 1.   Summary of experimental conditions in two experiments carried out in temperature-controlled tanks at the University of Liverpool
First experiment (1998–2000)Second experiment (2005–07)
Quadruple replication 3 Warming × 2 Nutrient × 2 Fish treatmentsQuadruple replication 2 Warming × 3 Nutrient × 2 Fish treatments
Ambient max, 24.8°, summer mean 15.5°Ambient max 24.9°, summer mean 15.5°
3 °C experimental rise above ambient4 °C experimental rise above ambient
Nutrient loading: N: 0, or 0.5 mg L−1; P: 0 or 0.05 mg L = 1Nutrient loading: N: 0, 0.25 or 2.5 mg L = 1; P: 0.05 mg L = 1
Sediment 2% loss on ignition (LOI)Sediment 8% LOI
+ or − sticklebacks (Gasterosteus aculeatus) + or − sticklebacks
Investigator-determined plant community (Elodea nuttallii, Lagarosiphon major, Potamogeton natans, Lemna minor)Naturally colonising community (Ceratophyllum demersum, Elodea nuttallii, Lemna trisulca, Potamogeton spp, Lemna minor, Spirodela polyrhiza)

Results from the first experiment (Table 2) suggested that warming would increase the incidence of symptoms of eutrophication. There was more release of phosphorus from the sediments and there were occasional fish kills following deoxygenation in summer (McKee et al., 2003). The plant community did not change in biomass but one member of it, the South African exotic, Lagarosiphon major, increased its growth rate and extended its growth season in the warmed treatments and came to dominate the warmed tanks (McKee et al., 2002, 2003). Effects of nutrient loading and presence or absence of fish were generally greater than those of warming but there was some interaction. Despite both warming and nutrients, a submerged plant community abundantly persisted, in contradiction to predictions made for the effects of climate change on shallow Dutch lakes (Mooij et al.,2005). There was very little effect of warming on the phytoplankton community composition and an expected rise in cyanobacterial abundance did not materialise (Moss et al., 2003).

Table 2.   Summary of effects of warming in two experiments (Table 1) in which temperature rises of 3 and 4 °C were applied to shallow lake communities that were eutrophicated to modest levels
 Warming by 3 °C, low nutrient loadingWarming by 4 °C, moderate nutrient loading
Total plant biomassnsnsIncreased floating, <0.001; no change submergedIncreased floating, <0.001; decr submerged, <0.001
Chlorophyll a concnns<0.001 incr<0.0001 decr<0.0001 decr
Gastropod number0.003 incr<0.001 decrNot availableNot available
Cladocera numberns<0.001 incr<0.01 decr<0.001 incr
Ostracod number<0.001 incr0.011 incr<0.001 incr<0.001 incr
TP concn0.018 incr<0.001 incrnsns
SRP concn0.04 incr<0.001 incr<0.03 incrns
pH0.017 incr<0.001 incr<0.004 incrns
Conductivity<0.001 incr<0.001 incr<0.001 incr<0.0001 incr
Oxygen (%)0.036 decr0.005 decr<0.0001 decr<0.0001 decr

A plant community persisted in the second experiment also, but the combination of a further degree of warming and the slightly raised nutrient loading had dramatic effects. Sticklebacks have been shown in laboratory experiments progressively to abandon male parental care when temperatures were raised from 16–17 °C to around 22 °C in well-oxygenated aquaria (K. Hopkins, B. Moss and A.B. Gill, unpublished data) but the effects of a productive system in causing severe deoxygenation in the mesocosm tanks were more dramatic. Heating markedly reduced fish numbers and biomass but combinations of warming and even the lowest nutrient loading led to death of all fish. The reduced oxygen concentrations were at least partly due to a shift in the composition of the plant community towards greater biomass of floating lemnids that shaded the underlying water, also resulting in reduced phytoplankton growth. Warming did not reduce submerged macrophyte biomass though it increased floating macrophyte biomass. Nutrients significantly increased the floating mass and significantly decreased the submerged mass, though a substantial crop persisted, despite total phosphorus concentrations that averaged over 350 μg L−1. Zooplankton changes were not simply linked to behaviour of the phytoplankton; there was no shift to phytoplankton dominance and turbid water.

The implications of these effects are profound since a 4 °C mean global temperature increase is now likely, and efforts at reducing nutrient loadings from diffuse sources in lowland Europe are showing little success. Sticklebacks are very resilient fish. They are more temperature- and deoxygenation-tolerant than all native British fish (Varley, 1967) bar the crucian carp (Carassius carrasius) and tench (Tinca tinca) and the introduced common carp (Cyprinus carpio). We might thus expect major changes in European fish communities, and those on islands in particular, in future circumstances. On the continental landmass of Europe there are possibilities for warm-tolerant fish and other organisms to shift distribution northwards (Walther et al., 2002), although the rate of movement might be much slower than the rate of temperature change.

For islands like Iceland, the U.K. and Ireland, the only possibility is invasion by new anadromous and catadromous species that can move via the ocean. There are few of these for they tend to be cool-water rather than warm-water fishes, and piscivorous. The incidence of piscivorous fish tends to decline rapidly with decreasing latitude, in favour of omnivores (Fig. 1). The greater likelihood in the U.K. is loss of many species from England but survival of some of them in Scotland, where fish of the coolest waters could become extinct (the coregonids, Coregonus spp, charrs, Salvelinus spp and salmon, Salmo salar) or very rare (brown trout, Salmo trutta). In England, the tolerant cyprinids and particularly the common carp are likely to become dominant, as carp has in many Australian rivers (Kennard et al., 2005). Currently common carp do not reproduce efficiently in the wild in the U.K. but rising temperatures will increase breeding success and the popularity of common carp among many anglers will mean illegal or sanctioned introductions to waters where they are currently absent. Carp are extremely destructive fish (Crivelli, 1983; Moss et al., 1996) because of their habit of disturbing bottom sediment in search of invertebrates and disruption of plant rooting systems, as well as a degree of direct herbivory. Where they become abundant, aquatic plant communities may be destroyed. Although aquatic plant communities in shallow lakes will survive warming per se, even with substantial eutrophication, the secondary effects of changing fish communities may mean their widespread demise. The implications of Fig. 1 for continental areas are that piscivores will decline and be replaced by omnivores, thus increasing the predation pressure on zooplankton and grazing invertebrates through an increase in forage fish. This will allow increase in algal biomass and a consequent loss in macrophyte communities also.

Figure 1.

 Changes in the percentage composition of fish communities by trophic category along a latitudinal gradient in South, Central and North America. Species lists were gleaned from the literature for 120 lake and river sites and food preferences allocated from Fish-Base and other available literature. Trends were very similar for both rivers and lakes so data have been combined. Piscivores means species that primarily feed on other fish as adults; invertivores feed primarily on benthos or zooplankton, herbivores solely on detritus, plant or algal material. Omnivores take food more or less equally from at least two trophic levels. Trends with latitude in piscivores, omnivores and herbivores but not invertivores are statistically significant at < 0.001 (regression analysis).

Metabolic balance

The above results suggest severe effects of a 4 °C rise in temperature for individual water bodies and for regional ecology, but there may be even wider consequences. In the 1950s, H.T. Odum (Odum, 1956, 1957; Odum & Hoskin, 1958) developed methods for measuring the gross photosynthesis and community respiration of whole ecosystems (usually streams and estuaries) by using diel (24-h) oxygen change curves (Seeley, 1969; Swaney & Hall, 2004). He used a graphic areal approach to determining community respiration from the rate during the night and extrapolated this to the light period on the assumption that rates remained the same as at night. From the curve of oxygen exchange rates during the light period, and an extrapolation of it down to the respiration baseline, he determined the gross photosynthesis and showed that most systems were net heterotrophic, feeding on organic matter imported from elsewhere, ultimately from terrestrial systems. This finding has been revived recently as a radical new understanding of aquatic systems (e.g. Cole et al., 2007; Dodds & Cole, 2007).

We have amplified Odum’s method (see Appendix 1) to be able to calculate the separate components of net photosynthesis, gross photosynthesis, heterotrophic respiration, and plant respiration as well as gross photosynthesis and community respiration (D. Atkinson, B. Moss U. Noreen and C. Whitham, unpublished data). We used oxygen probe readings taken every 2 h from the University of Liverpool experimental tanks during three 24-h periods in late June and early July 2007 and corrected the oxygen exchange, using meteorological data taken adjacent to the tanks, with the equations of Jähne et al. (1987) and Wanninkhof (1992). However, conditions were very calm and corrections were very small. Respiration rates at night were often lower than those in the late afternoon and evening, probably because concentrations of dissolved oxygen fell so low that both respiration and photosynthesis became inhibited. We thus used as a measure of community respiration a curve that took the maximum rate recorded as the baseline for the light period, but followed the actual oxygen curve during the evening and night. The results (Table 3) showed that a 4 °C temperature increase significantly reduced both gross and net photosynthesis and plant respiration, but increased heterotroph respiration. The ultimate effects were a substantial increase in the ratio of community respiration to gross photosynthesis and a markedly reduced net ecosystem production (gross photosynthesis−community respiration), meaning that more stored carbon in the systems was being converted to carbon dioxide on warming. Nutrient addition alone also increased heterotroph respiration and the community respiration to gross photosynthesis ratio, so that was an interaction effect between warming and nutrients.

Table 3.   Effects of warming by 4 °C and moderate nutrient loading on ecosystem metabolism in a set of pond mesocosms. between June 27/28 and July 16/17 2007. Effects are shown (= 10) of warming and added nutrients. Values are means ± SD in mg oxygen L−1 h−1 over the entire 24 h period
 Ambient+4 °CPNo nutrient additionAdded nutrientsP
Gross photosynthesis28.3 ± 18.413.2 ± 10.20.00323.0 ± 16.018.4 ± 17.2ns
Net photosynthesis1.15 ± 4.2−0.33 ± 2.49ns−0.23 ± 3.541.05 ± 3.39ns
Net ecosystem production−4.08 ± 2.63−6.73 ± 1.500.0004−4.84 ± 2.47−5.97 ± 2.46 ns
Heterotroph respiration5.26 ± 3.836.41 ± ± 3.67.01 ± 1.92 0.044
Plant respiration27.1 ± 16.613.5 ± 8.990.00323.2 ± 14.817.4 ± 14.7ns
Community respiration32.4 ± 17.019.9 ± 9.50.00727.9 ± 14.524.4 ± 15.6ns
Ratio of community respiration to gross photosynthesis1.41 ± 0.761.85 ± 0.60.0471.40 ± 0.421.86 ± 0.870.044

These were experiments on a limited scale but they were carried out at the height of the plant growth season and the net heterotrophy might be expected to be proportionately even greater at other times of year. There are many caveats to extrapolation of the results to bigger systems. Studies on deep lakes suggest that carbon storage increases with latitude, and this might reflect higher respiration rates at higher temperatures (Alin & Johnson, 2007). On the other hand, synopses of data on European forests indicate that although gross productivity is largely independent of latitude between 35 and 52′N, respiration increases northwards and there is a greater chance of northern forests being net heterotrophic than southern ones (Valentini et al., 2000; Piao et al., 2008). There are indications, however, that forests currently with net uptake of carbon will become net emitters as temperatures increase and the very hot period of 2003 provided evidence for this (Ciais et al., 2005). Moreover, some of the apparent increase in carbon storage measured in northern forests is due simply to re-growth of forest on abandoned cultivated land and much of the rest appears to be driven by increased loads of anthropogenically derived nitrogen (Magnani et al., 2007). Temperate wetland systems with emergent plants seem to be net storers of carbon at present (Bonneville et al., 2008), but there is no guarantee that they will not respire much of the stored material as temperatures increase. Laboratory stream determinations suggest that a 2.5 °C rise in temperature will increase community respiration by 20% (Acuna et al., 2008) and studies on litter decomposition in Canadian forests also suggest that the order of magnitude change in net ecosystem production in our mesocosm tanks is not untoward (Moore et al.,1999).

Conventional wisdom is that warming will increase gross primary production of terrestrial vegetation but evidence appears to be mounting against this and the view may have been conditioned by the need to balance the global carbon budget satisfactorily by attributing to it the 2.6 Gt C year−1 that is released into the atmosphere but is not accounted for by other measurements. If the extensiveness of wetland and saturated soil systems in the northern hemisphere and the wet tropics is borne in mind, our results might suggest that warming could result in a strong positive feedback effect on carbon dioxide release. At the extreme, assuming all ecosystems behaved similarly, the increased release could raise the current net carbon emission to the atmosphere from 4.1 to 5.3 Gt year−1 (Table 4). We do not argue any great precision for this value, but the indications are that the true amount would not be trivial.

Table 4.   Carbon budgets for the biosphere for the pre-industrial period, the 1990s and a future with 4 °C warming. Calculation of the change in the future assumes a steady emission of carbon at current rates from fossil fuels and biomass burning and current rates of exchange in the ocean. The change in future terrestrial sink is based on the percentage change in net ecosystem production in the mesocosm experiments applied to the current estimate of the terrestrial sink. Positive values indicate release to atmosphere, negative values indicate sinks. Units are Gt C year−1. Errors in estimates are believed to be ± 20–25%
 Pre-industrial1990sFuture with 4 °C rise
Fossil fuel burning0+6.4+7.2
Net ocean exchange+0.6−2.2−2.2
Land use change (e.g. burning)0+1.6+1.6
Land sink−0.6−2.6−1.6
Net effect0.0+3.2+5.0

Renegotiation of the Faustian bargain

The consequences of ignoring the three paragraphs of small print in the Faustian bargain could therefore be very substantial. They are not allowed for in the perhaps optimistic assessments made from the physical models by the IPCC (2007) and the assumption of all Governments that the problem can be coped with by application of classical economics to change human behaviour and indeed turn a profit from climate change. All current political approaches assume an anthropocentric rather than a biocentric view. The implications of loss of ecosystems are ignored. The Millennium Ecosystem Assessment Commission need not have bothered to deliberate!

Our anthropocentrism has become more marked as our destruction of ecosystems has increased and indeed as the consequences of that destruction become apparent in disastrous floods, shortage of potable water, disruption of traditional lifestyles, environmental refugees, salinisation of arid lands, soil erosion, famine and loss of existing agricultural land, let alone the apparently esoteric issues of loss of biodiversity and spread of damaging invasive species. Society in general sees the latter two purely as amenity issues. We have behaved in the past like the invasive red fox, whose flexibility is leading to successful expansion even in urban areas far from those in which it evolved (Kamler & Ballard, 2002; Baker & Harris, 2007) but are now being manoeuvred into emulating the giant panda, a highly specialist species so endangered that continuous monitoring and the sophistications of human medical technology must be applied to preserve its numbers (Peng, Jiang & Hu, 2001). But we should be learning instead from the oak, and other forest trees.

We have a western society that is highly centralised and dependent on technology, that profligately uses resources that are not renewable; we are highly educated for business as usual; our expectations for comfort and luxury expand rapidly; our educational emphases are for conformity, training, employability and economic growth; the business and management schools are overflowing; the financial sectors are the most highly rewarded of our economy. We are manipulated by powerful large corporations to want what they find it most profitable to produce; we are increasingly watched and controlled under rationalisations of health, safety and security that may sometimes be true, but often lest we behave or think in ways that might jeopardise the expansion of profits; we have a blame culture that discourages the taking of personal responsibility. We even have toilet rolls, unnecessarily covered with further wrapping that bear the telephone number of a toll-free helpline (Fig. 2)! Nature deficit syndrome is now recognised as a malady in the young (Louv, 2008). Increased urbanisation in the western world has led to a reduced understanding and acknowledgement of how humans depend on natural systems and therefore a reduced comprehension of the very nature of life itself in favour of a cloud- cuckoo-land in which economics and technology will solve all problems at the push of a computer button. We are inward-looking and less and less fitted to cope with the problems posed by warming and its combined threats with many other environmental stresses.

Figure 2.

 Toilet roll photographed in the Republic of South Africa in 1998.

Moreover, in the organisation of our scientific activities we follow the rest of society in our approach, with performance indices, rewards, business plans, and competitiveness. We co-operate in trivial habitat restoration schemes (Ormerod, 1999, 2004; Moss, Carvalho & Plewes, 2002; Pretty et al., 2003a,b) that pay lip-service to the purported importance of ecology but which, deep-down, I suspect, we know to be tokens of no ultimate significance. We are manoeuvred to help undermine the provisions of water legislation that could be far-reaching but is being manipulated to achieve far less (Moss, 2008) and our conventional approach to science is failing to do much that is of real consequence in averting an uncomfortable future (Ehrlich & Pringle, 2008). We are sleepwalking into paying the final instalment of our bargain with Mephistopheles and our future is more than usually uncertain. We are the doctors who see the marks of death in a community that believes itself well and does not want to be told otherwise. But nor do we.


This paper was prepared under the auspices of EU Contract GOCE-CT-2003-505540 (EUROLIMPACS). The experimental design involving fish was approved by the Home Office Inspectorate as not requiring a licence. I am grateful to Tom Popplewell for assembling the raw data on which Fig. 1 is based and to the Freshwater Biological Association for granting the H. Cary Gilson Award in 2007, which allowed the carrying out of the diel experiments in the mesocosm tanks.

Conflicts of interest

The author has not declared any conflicts of interest.


Appendix 1. Modification of the Odum method

Odum’s diel oxygen change method for standing water sites depends first on regular recording of oxygen concentrations over a 24-hr period and then conversion of the data to rates of change in oxygen concentration, corrected for exchange with the atmosphere using meteorological data or, more recently, measurements of diffusion of alien gases such as propane added to the water. The curve (Fig. A1) generally shows a rise in rate of production during the light period and a fall at night. Seeley (1969) summarises the method of subsequent calculation (Fig. A2). The community respiration is taken as the area ABHJ, assuming that the hourly rate of uptake at night (FGHJ) is the same as that by day (ABFG) and is shown by a red line in Fig. A2. The light period curve is projected down to the baseline respiration rate to give an estimate of gross photosynthesis (green line, ACDEF in Fig. A2. The ratio of community respiration to gross photosynthesis or the net ecosystem production (gross photosynthesis – community respiration) can then be calculated.

We have modified the calculations as shown in Figs A3 and A4. Using the following symbols (units are in mg O2 per unit volume and time):

Phg24 hr is Gross photosynthesis per 24 hr

Phn24 hr is Net photosynthesis per 24 hr

Rhetlight is Heterotrophic respiration (animals and microorganisms plus plant material not producing oxygen for whatever reason) in the daylight hours

Rhet24 hr is respiration of the heterotrophs, as defined above per 24 hr

Rplant24 hr is respiration of the photosynthesisers per 24 hr

Rcom24 is the total respiration of the community, photosynthesisers and heterotrophs per 24 hr

NEP is net ecosystem production, equal to Phg24 hr–Rcom24

The area shown in green in Fig. A3 (ABCDEGF) gives the gross photosynthesis plus the rate of heterotroph respiration during the light period (Phg24 hr + Rhetlight).


The area shown by a red line (ABHJ) is taken as the community respiration (Rcom24 hr during 24 hr as in the original method.


The areas indicatively shaded in blue in Fig. A4 allow the net ecosystem production (Phg24 hr- Rcom24) to be calculated through addition of area CDE (which is positive) to the areas ABC and EFJHG (which are negative).


Thus: (c) + (b) = Phg24 hr

(a) −Phg24 hr = Rhetlight

Rhetlight × 24/light period hours = Rhet24 hr

(b) −Rhet24 hr = Rplant24 hr

Phg24 hrRpl24 hr = Phn24 hr