Science of the Total Environment 434 (2012) 130–142

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Science of the Total Environment

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Review

Cogs in the endless machine: Lakes, climate change and nutrient cycles: A review

Brian MossSchool of Environmental Sciences, University of Liverpool, Liverpool, UK

E-mail address: brmoss@liverpool.ac.uk.

0048-9697/$ – see front matter © 2011 Elsevier B.V. Alldoi:10.1016/j.scitotenv.2011.07.069

a b s t r a c t

a r t i c l e i n f o

Article history:Received 5 April 2011Received in revised form 23 July 2011Accepted 29 July 2011Available online 29 September 2011

Keywords:NitrogenPhosphorusCarbonHeterotrophyGlobal warmingEutrophicationMesocosms

Lakes have, rather grandly, been described as sentinels, integrators and regulators of climate change(Williamson et al., Limnol. Oceanogr. 2009; 54: 2273–82). Lakes are also part of the continuum of the watercycle, cogs in a machine that processes water and elements dissolved and suspended inmyriad forms. Assessingthe changes in the functioning of the cogs and themachinewith respect to these substances as climate changes isclearly important, but difficult. Many other human-induced influences, not least eutrophication, that impact oncatchment areas and consequently on lakes, have generally complicated the recording of recent change in sedi-ment records andmodern sets of data. The least confounded evidence comes from remote lakes inmountain andpolar regions and suggests effects of warming that include mobilisation of ions and increased amounts of phos-phorus.A cottage industry has arisen in deduction and prediction of the future effects of climate change on lakes, but theresults are very general and precision is marred not only by confounding influences but by the complexity of thelake system and the infinite variety of possible future scenarios. A common conclusion, however, is thatwarmingwill increase the intensity of symptoms of eutrophication.Direct experimentation, though expensive and still unusual and confined to shallow lake and wetland systemsis perhaps the most reliable approach. Results suggest increased symptoms of eutrophication, and changes inecosystem structure, but in some respects are different from those deduced from comparisons along latitudinalgradients or by inference from knowledge of lake behaviour. Experiments have shown marked increases incommunity respiration compared with gross photosynthesis in mesocosm systems and it may be that themost significant churnings of these cogs in the earth–air–water machine will be in their influence on the carboncycle, with possibly large positive feedback effects on warming.

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Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1302. Parameters of the Review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1313. Approaches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1334. Questions 1 and 2: Current Effects of Changing Climate on Nutrients in Lakes and Implications for Future Warming . . . . . . . . . . . . . . 133

4.1. Ocean and atmosphere . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1334.2. Catchment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1344.3. Internal Lake Processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135

4.3.1. Experimental Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1364.3.2. Exacerbation of Eutrophication Symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1364.3.3. Carbon Exchange . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1374.3.4. Internal Adjustments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137

5. Questions 3 and 4: Importance of Likely Future Effects and their Mitigation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 138

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131B. Moss / Science of the Total Environment 434 (2012) 130–142

1. Introduction

An endless machine, the water cycle, drives everything of impor-tance on Earth, from the survival of the smallest essential bacteriumto the rather less obvious need for futures trading in the bankingsystem. Sometimes, during a glaciation, the machine slows; at othertimes, during the Carboniferous period for example, high temperaturesquicken evaporation, and it turns faster. Only during the Hadean, whentemperatures were too high for water to condense, was the machinenearly at rest. Raisewell et al. (1980, latest edition, Andrews et al.,2004) christened it the earth–ocean–atmosphere system and used itto integrate the entire subject of biogeochemistry, for, as the cycleturns, it drives also the cycles of every other element. The slightlypolar but still largely covalent nature of the water molecule gives itproperties of dissolution, sought, but missed, by the alchemists of themediaeval period in their quest for a universal solvent.

As the cycle takes in the land surfaces, the machine runs through acontinuous mesh of freshwater cogs, from headwater streams, pud-dles, ponds, swamps and marshes, soils and groundwater, rivers,lakes and more rivers to estuaries, and eventually the ocean, whereit gathers much of its running energy from the sun and starts toturn again. None of the cogs is isolated; all have inflows and outflows,either direct to the atmosphere as evaporation, or as liquid throughthe next cog to the next but one. And as the water flows, a huge work-force of living organisms removes and adds raw materials, indeed bydoing so maintains the conditions in the biosphere by which themachine can continue to function and not relapse into Hadean immo-bility (Lovelock, 1979). It was therefore complete folly for me to agreeto review current knowledge on the effects of climate change onnutrient cycling in lakes, even out of respect for the considerable con-tributions Colin Neal has made to knowledge of the processing ofnutrients and major ions in the freshwater system. It was to masquer-ade as aDaVincianpolymath in aworldwhose complexity even Leonardocould not imagine, and no such review could ever be complete.

There is some logic, however, in isolating just one set of cogs, thelakes, for review (George, 2010;Williamson et al., 2009). They respondrapidly to changes in thewater cycle through the changes in their levelsand in their chemical composition. They also, in their sediments, retain arecord, if incomplete, of such changes. They are ubiquitous and althougheach is individual, they retainmany commonprocesses that canbe com-pared across latitudes. They are also temporary, few being older thanfifty thousand years, and some annually disappearing and reappearingin response to dry and wetter years, thus recording a changing climatein a particularly graphicway. They arewell understood as systems, for re-tention of a large body of water renders them less vulnerable to the sto-chastic processes of weather that plague hydrologists and streamecologists; and, like all freshwater systems, they have great importanceto humans, as water storages, sources of fish and other products likereed and clay, as settlement sites, and for recreation andvisual inspiration.They are, at least, obvious and identifiable cogs in the endless machine.

They have also been studied as integrated systems through a longtradition of limnology (Moss, 2010a). River systems, in contrast, havelong been studied separately by hydrologists and by stream ecolo-gists, and only now is it seen that these disciplines should be broughttogether (Vaughan et al., 2007); the study of terrestrial systems hasbeen even more schismatic (Levin, 2009), even to a long periodwhen animal ecology was studied separately from plant ecology. Incontrast, limnologists have understood since the early twentiethcentury that catchments and freshwaters are mutually dependent.Ever since Stephen Forbes' famous paper on ‘The Lake as Microcosm’

(1887), though he underestimated the importance of the catchment,lake science has been holistic in concept, whilst supported by anintense set of reductionist specialisations. Many of the key conceptsof ecology, from energy flow and nutrient cycling to niche and foodwebs, have been initiated in lakes and limnology laboratories(McIntosh, 1985).

Climate, weather andwater chemistry have always been pre-eminentin lake studies. Local communities have long recorded the dates onwhichice formed on adjacent lakes, and finallymelted, because of the economicimplications for transport and navigation (Magnuson et al., 2000). Theserecords now document the immediate effects of global warming. Lakelevels, and hence the net balance of inflow and evaporation, likewisehave many long records. For large lakes especially, storminess and itseffects on seiches that might swamp lakeside villages have been noted(Hutchinson, 1957). But it has been the seasonal changes in inflow, andthe nutrients, brought in and accumulated during the winter and spring,in temperate lakes, that have been an enduring theme. These nutrientsfuel the growth of phytoplankton and in turn the stocks of zooplanktonand the annual recruitment of fish. The Plankton Ecology Group (PEG)model (Sommer et al., 1986) of seasonal change that describes the mainfeatures is a widely quoted and used summary of this.

Over lengthier periods, the concept of lake development has alsobeen a theme that integrates climate, water chemistry, and, in turn,changes in the productivity of lakes. Huge numbers of lake basinswere created by the bulldozing action of moving ice, the deposition ofmoraine dams, the plucking of rock from corrie walls and the meltingof icebergs buried in glacial drift, during and just after the last glaciation.The provision of large amounts of fresh-ground rock in the catchmentsmeant that the lakes, when they formed, were rich in ions derived fromrockweathering (Mackereth, 1965), but deprived of those elements likenitrogen that must be accumulated from the atmosphere by biologicalprocesses. Progressive leaching of the catchment soils, coupled withaccumulation of land vegetation that evolved mechanisms to retainelements in short supply, then led to establishment of nutrient deficien-cies and a progressive oligotrophication of natural lakes (Engstromet al., 2000;Haworth, 1969; Round, 1961). This contrastswith thewide-ly held eutrophication myth that lakes naturally accumulate nutrientsand becamemore fertile with time. Lakes do sometimes increase in fer-tility, particularly when aridity leads to erosion and then concentrationof nutrients (Haworth, 1972) but eutrophication almost always is asso-ciated with human disturbance.

In warmer regions, concepts that link climate, nutrients and lakeproduction have been fewer, for studies have been scarcer, but the‘endless summer’ of Kilham and Kilham (1990) offered a start. Lakesin the dry tropics receive much less in the way of nutrients washedin from the land and become much more isolated from their catch-ments than those in wetter regions, such that internal recycling ofnutrients becomes their permanent state, as it often does temporarilyin the summer in temperate lakes.

2. Parameters of the Review

Thus there are both difficulties and good reasons for looking at theeffects of climate change on lake nutrients but some boundaries haveto be drawn. I have drawn two sets. The first is encapsulated in Fig. 1,which defines the scope of this review. Superimposed on it are twofurther layers. The first is the range of elements considered; the sec-ond is the scope of climate change. There are about twenty elementsprobably absolutely needed by living organisms (C, H, O, N, P, S, Fe,Mn, Na, K, Cu, Mg, B, Cl, Zn, Ca, Co, Mo, I, V and possibly Se) andone, Si, absolutely needed by a few groups of algae. Some of these el-ements are very abundant in available forms in natural waters, othersare scarce, but the important ratio is that of supply by the environ-ment to that of need by organisms. This is high for most elementsand if the ratio is normalised to unity for P, the value is greater than1.0 for all other lithospheric elements (Hutchinson, 1973). It may belower than 1.0 for nitrogen in many habitats, for although nitrogenis immensely abundant in the atmosphere, it becomes naturally avail-able only though biological fixation and the products of its minerali-zation are very vulnerable to bacterial conversion back to nitrogengas. Nitrogen or phosphorus or both (Elser et al., 2007; Lewis andWurtsbaugh, 2008) may then be limiting to the accumulation of

AtmosphereChanges in circulation and changing precipitation. Changes in gases, C, N

Internal Lake processesChanged seasonality, ice free period, change

in stratification, changed seasonality and match/mismatch, changed retention time. Changed water balance and salinisation.

Changing biota and invasive species

OceanProvision of spray.

Salinisation of coastal lakes

CatchmentWeathering rates of lithospheric elements.

Leaching rates, hydrology of transfer as dissolved and particulate matter. Influence of humans by removing natural ecosystem.

Indirect influence by changed activities (more intensive agriculture, more biofuels)

Changing weatherIncreased

storminess, sea level rise

Sea spray effects Nutrient leaching,changed hydrologyChanged land use

Changed temperatureprecipitation

Greenhouse gasrelease

Fig. 1. Scope of this review.

132 B. Moss / Science of the Total Environment 434 (2012) 130–142

biomass or the rate of growth of primary producers in lakes, and areof especial importance.

Carbon, and silicon (for diatoms and a very few other groups)are very abundant but needed in large quantities so may becometemporarily short on either a daily or seasonal basis. Carbon is readilyre-supplied from the atmosphere and many lake waters are apparentlyover-saturated with it from import in stream waters that have drainedsoils with very active decomposer processes, or through decompositionof imported organic matter by the bacterial community in the lake(Cole, 1999; Sobek et al., 2003). In recent years a hypothesis that mostlakes are net heterotrophic has become popular (Reynolds, 2008)but has the potential flaw that there is no current means of knowingwhether the imported carbon comes from the terrestrial vegetation ofthe catchment or the emergent swamp vegetation that surrounds, andis part of, most lakes. In the latter case it might be possible to talk of aheterotrophic plankton community, but not of a net heterotrophiclake. Carbon is, however, a driver for climate change, so must also beconsidered in this review.

Silicon is essential for diatoms, and diatoms are particularlyprominent in freshwater communities and thus should also be in-cluded, though information is very scarce. Other needed elementsfall into three groups: the lithospherically-derived major ions Na,K, Ca, Mg, the atmospherically-derived major ions S and Cl andthe largely lithospherically-derived trace elements (Fe, Mn, Cu, B,Zn, Co, Mo, V). Except in very unusual circumstances, the watersof volcanic hot springs, for example, where some may be at toxicconcentrations (Brock, 1978), none of these is usually limiting togrowth and production in freshwaters (though a case can be madefor K in some circumstances (Talling, 2010), and iron perhaps, inregions of non-sedimentary rocks, and there are hints of trace elementdeficiencies in waters derived from soils of ancient landscapes, suchas those of Australia and even more recent formations in the USA(Goldman, 1965). There are many subtleties, however, and smallchanges in major ions (Na, K, Cl) may favour one species over anotherthrough osmoregulatory mechanisms (Sutcliffe, 1978) or precipitationof other scarcer elements, for example calcium and phosphorus (OtsukiandWetzel, 1972).Much less recent emphasis has been placed on theseelements than on C, N, and P by ecologists, though themajor ions, espe-cially, are often routinely measured, either separately, or collectively as

conductivity, in water quality and hydrological investigations, and maygive useful information on collective processes such as rock weathering.Human activities have often upset the natural order of biogeochemistry,especially by doubling the global rate of nitrogen fixation through theHaber Process (Reay et al., 2008; Vitousek et al., 1997), by mobilisingphosphorus from geological deposits through fertiliser and detergentuse, and through atmospheric pollution by acids, ozone, particulatematter, mercury and persistent organic pollutants (Bergin et al., 2005).Especially though there has been the increased release of greenhousegases, such as carbon dioxide, nitrous oxide andmethane, which are par-ticularly prominent in lakes and wetlands (Bastviken et al., 2008, 2011;Cole et al., 2007; Dalal and Allan, 2008; Duarte et al., 2008; Le Quéré etal., 2009; Seitzinger et al., 2006; Tranvik et al., 2009).

Finally, in determining the parameters for this review, it is necessaryto define climate change. Climates have been continually changing foraround the four billion years that water has been able to persist as aliquid on Earth. The glacial and interglacial periods of the Pliocene, Pleis-tocene and Holocene are amply reflected in the remains in lakedeposits, with phases of drying indicated by diatom fossils characteris-tic of slightly more saline waters (e.g. Andreeva et al., 2004; Battarbee,2000; Gasse and van Campo, 2001; Jones et al., 2000), and phases ofwarming of now cooler regions by seeds of subtropical water plantslike the water chestnut, Trapa natans (Godwin, 1985). There are manydefunct lake basins in now arid regions (Burrough and Thomas, 2008;Churcher et al., 1999) and records of low and high water levels inlakes like Naivasha (Richardson and Richardson, 1972; Verschuuren,2001), which once became a dry sand flat for three thousand years,having previously been a very deep lake, and now is a shallow lake ofgreatly fluctuating water level.

However, current concerns, and those of this review, are with thewarming trend that set in with the industrial revolution and iscurrently increasing global temperatures at unprecedented rates(Intergovernmental Panel on Climate Change (IPCC), 2007; Kundzewiczet al., 2007). Its existing and likely medium-term future effects, otherthan warming by up to several degrees, are greater precipitation, redis-tribution of precipitation into winter or existing wet seasons, extremedrying of Mediterranean regions, an increase in the frequency ofextreme events such as droughts, floods and short very hot periods,and a rise in sea level through thermal expansion and glacier melting.

133B. Moss / Science of the Total Environment 434 (2012) 130–142

Effects on lakes have already been felt particularly in the arcticand boreal regions (Mueller et al., 2009; Prowse et al., 2006a, 2006b;Schindler, 1998; Schindler et al., 1996; Wrona et al., 2006), wherethere are innumerable lakes, though evidence of change is universaland generally tangled with other human impacts on lakes such as acid-ification, eutrophication through urbanisation, deforestation, and inten-sive agriculture, pollution by heavy metals and persistent organicpollutants, and introduction of exotic species that become strongly in-volved in nutrient cycling through their large biomass or alteration offood webs (Johnson et al., 2008; Manca and Demott, 2009; Rahel andOlden, 2008;Wiedner et al., 2007). Moreover prediction of likely futureeffects is complicated because of natural stochasticity in atmosphericsystems (Overpeck and Cole, 2006), potential feedbacks in climate cy-cles (Lenton et al., 2007) and in natural systems that currently store car-bon (Walter et al., 2006), and the unpredictability of the degree andtiming with which human societies will attempt to control emissions(Anderson and Bows, 2008, 2011). Though the IPCC (2007) uses fourmain scenarios for prediction, there is, in fact, an infinity of possibilities.

Within these parameters, I will focus on attempting to answer fourquestions: (1) What effects have current climate trends already hadon the nutrient processes in lakes? (2) What likely future changesmight there be? (3) Which effects might seriously affect the biodiversityor ecosystem services of lakes? (4) Could anything be done to mitigateor obviate them?

3. Approaches

There are several approaches to answering these questions (Hering etal., 2010). The effects of climate change so far can be deduced fromlong-term records and from palaeolimnological studies. Especially forphysical characteristics, such as surface temperature and temperatureprofile down the water column, and dates of freezing and thawing ofthe winter ice, there are many records (e.g. Adrian et al., 2009; Austinand Colman, 2007; Coats et al., 2006; Hambright et al., 1994; Hamptonet al., 2008; Livingstone, 2003; Macintyre et al., 2009; Magnuson et al.,2000; Moore et al., 2009; Quayle et al., 2002; Verburg and Hecky,2009). For chemical effects there is amuch leaner picture and the difficul-ty that climate-induced changes are always confounded with other an-thropogenic changes, particularly eutrophication and restoration fromit (Battarbee, 2010; Battarbee et al., 2002; Catalan et al., 2002; Leavittet al., 2009), despite increasingly sophisticated statistical techniquesavailable to separate different effects (Simpson and Andersen, 2009).

Sometimes there are long-term records of biological phenomena,such as annual dates of appearance of adults of dragonflies and dam-selflies (Hassall et al., 2007), which are prominent insects that catchthe imagination of amateur naturalists, who are largely responsiblefor such records. The UK is particularly rich in such data (Thackerayet al., 2010), which overwhelmingly show that life history eventsand seasonal appearances have become progressively earlier in theyear in recent decades. Because of the importance of phytoplanktonto the drinking water industry, there are also some long-term recordsof plankton changes, such as the peak of the spring diatom growth(Elliott and May, 2008; Thackeray, 2008).

The longest records are potentially those from sediments (Smoland Douglas, 2007). Palaeolimnology, however, suffers from theadded complication of inevitably confounded changes that cannotbe as easily separated as in fuller contemporary data, and it hasproved difficult to distinguish subtle climate change from othertrends in a record that is also selective in preservation of fossils, andpreserves only the end products of chemical processes. Vallentyne(1996) wrote that: ‘no anatomist or physiologist in his right mindwould ever base a study of the life history of an organism on the analysisof its accumulated faeces. This is, however, precisely the position of apalaeolimnologist with respect to the developmental history of a lake.Sediments are lacustrine faeces, the residue remaining after lake metab-olism’. But gross long-term features of climate change, drying out for

example, are readily recorded in sediments (Fritz et al., 1999; Korholaet al., 2005; Weckström et al., 2006), if not always the subtleties ofvery recent change. Polar systems are most likely to show unequivo-cal effects of temperature. Distinct climate-induced changes in dia-tom communities have been shown for Arctic lakes (Ruhland et al.,2008; Smol et al., 2005) and shifts in salinity owing to increase inevaporation in some Antarctic lakes (Hodgson et al., 2006).

Forecasting, or rather accurate and precise forecasting, of likely fu-ture effects of change is also difficult. It can be approached throughspace-for-time studies, and through direct experimentation.Space-for-time studies use latitudinal gradients and the presumptionthat future climates will be similar to present climates displaced pole-wards, or upwards in mountainous regions. Climate is much morethan temperature so this is an optimistic view and the conclusionsare triply speculative on account of the uncertainties also of what fu-ture temperatures will be, and the confounding of other influences.The same is true also of direct experimentation, except that con-trolled experiments, in laboratory cultures or heated mesocosms,can eliminate confounding factors, though decisions still have to bemade about the changed climate to be imposed in the experiment.An additional uncertainty is the complexity of system to be studiedexperimentally. It is tempting to use laboratory microorganism com-munities, for they are cheap, can be easily controlled and abundantlyreplicated (e.g. Petchey et al., 1999; de Senerpont Domis et al., 2007),though they lack the complex structure and diversity of natural sys-tems and there is a temptation to push temperatures beyond likelyreality to amplify results. Open-airmesocosms, either placed in a seriesof similar lakes on a latitude gradient (Meerhoff et al., 2007a, 2007b;Moss et al., 2004; Stephen et al., 2004) or with controlled heatingsystems in the same location, (Liboriussen et al., 2005; McKee et al.,2000) offer much greater reality but heated systems are expensive tomaintain, and thus replication has to be more limited.

Experimental studies, however, offer the most unambiguous in-formation for future prediction. The likely least reliable approachesare those of predictive modelling and ‘horizon scanning’ in which ex-pert groups speculate on potential effects, though this is inexpensiveand therefore very popular (Heinol et al., 2009; Hobbie et al., 1999;Jeppesen et al., 2009, 2011; Mooij et al., 2005; Moss et al., 2009;Moss, 2010b; Schindler, 1997, 1998, 2001, 2009; Veillette et al.,2008). Modelling is most effective for relatively simple systems suchas physical structure or the phytoplankton community (Elliott et al.,2005, 2006; Fang and Stefan, 2009; Markensten et al., 2010) butlakes are much more than their plankton. There can also be no check-ing of expert judgement through horizon scanning until after the event,but many more variables can be taken into account qualitatively thancan be quantified in predictivemodels. The two approaches are comple-mentary andmostmodels and predictions are based on a long and solidunderstanding of overall lake function, and almost certainly reveal reli-able trends, though non-linear behaviour, which is usually not takeninto account, could bring surprises. So could ignorance of the individualresponses of different bodies of water, with their own individual catch-ments, histories, and current impacts (Blenckner, 2005).

Answers to my third and fourth questions depend on the limita-tions of the answers to the first two questions. These answers alsoare subject to judgement, for example on what the relative values ofecosystem services are, whether the concept has value outside con-ventional economics and what priorities future societies will have.

4. Questions 1 and 2: Current Effects of Changing Climate onNutrients in Lakes and Implications for Future Warming

4.1. Ocean and atmosphere

Ocean and atmosphere processes (Fig. 1) impact nutrient processingin lakes in several ways: through weather systems affecting seasonalprecipitation and annual temperature and the timing of biogeochemical

134 B. Moss / Science of the Total Environment 434 (2012) 130–142

events; through the delivery of major ions in sea spray; through distil-lation of volatile pollutants; and through salinisation of coastal lakesas sea levels rise. In lakes of the English Lake District, the timing of zoo-plankton growth peaks (George, 2001), particularly the incidence ofDaphnia in spring has been linked to the position of the North Atlanticoscillation (George, 2010) and the position of the Gulf Stream (Georgeand Taylor, 1995), though it is yet not clear if these systems have yetbeen affected by climate change. Similar linkages have been demon-strated in other European lakes (Jentsch et al., 2007; Straile and Adrian,2000). Because zooplankters are important in consuming algae inspring and these in turn deplete to greater or lesser extents the pulseof nutrients that has built up over the winter and thus determine thenutrient regime for the succeeding summer (see below), there arealso ultimate effects on nutrients (George et al., 2004).

The effects of El Nino Southern Oscillation (ENSO) in the southernhemisphere are likely to have impacts through alternating floods anddroughts and effects are also felt in more distant weather systems.Links between El Nino and reservoir water quality have been foundin Spain (Marce et al., 2010), and in East Africa, in the water levelsof Lake Victoria and other African great lakes, though the incidenceof sunspots seems to be a stronger driver (Stager et al., 2007). It isyet unclear whether the frequencies and intensities of the ENSO arebeing changed by global warming (Latif and Keenlyside, 2009).

Lakes within about 100 km of coasts, with onshore prevailingwinds, as in northwest Europe, receive substantial amounts of saltin storm-transported sea spray blown inland. This affects the ionicbalance of water in lakes and wetlands and may determine communi-ty composition or occurrence of particular species (Sutcliffe, 1978)and again, though there has been an increase in storminess in thenorthern hemisphere at least (Min et al., 2011), close linkage of anychange has yet to be unequivocally demonstrated.

There is more evidence for increased atmospheric transport of vol-atile pollutants, though not nutrients, as a result of warming (Grimaltet al., 2010). Pollutants, however by interfering with community func-tion and composition will have effects on nutrient cycling. Organicpollutants and mercury tend to be volatilised as temperatures increaseand then condense from the atmosphere in cooler locations. There isevidence of transfer tomountain and polar lakes. Salinity rises in coastallakes may also occur as sea levels rise and tides penetrate further upriver, or ground water levels very close to the coasts are increased.There is some indication of this (Moss et al., 1984; Raymond et al.,2008) but it is difficult to separate the effects of climate change fromthose of land use change, river engineering, whichmay constrain chan-nels in the interests of floodplain drainage close to the sea, and of irriga-tion abstraction of down flowing freshwater from upstream. Potentiallyat least, however, salinity effects are likely.

4.2. Catchment

Demonstration of climate-induced catchment (watershed) effectson lakes is commoner but still relatively unspecific. Rock weatheringrates are dependent on temperature (Baron et al., 2009; Catalan et al.,2009; Rustad et al., 2001) and higher rainfall should contribute togreater transfer of ions derived from chemical weathering to riversand then lakes (Jeppesen et al., 2009; Neal et al., 1986, 2001). Min-erals from physical erosion, moving as sediments in river systemsshould also weather more rapidly. In two mesocosm experiments(McKee et al., 2003; Feuchtmayr et al., 2009), there was a steadyincrease in conductivity in the warming treatments that could notbe attributed to evaporative concentration but only to release ofmajor ions from the sediments in the tanks, and this may give aclue to what is happening in catchments. However because majorions are unlikely to be limiting and, in freshwaters, far from toxic,the effect is unlikely to have major consequences. Changes in use ofroad salt consequent on changed winter weather are likely to have

local and episodic effects (Winter and Likens, 2009) but again, long-termchange is unknown.

Despite a long history of research on phosphorus leaching and onthe importance of phosphorus in lakes, specific influences of climatechange remain speculative, not least because of other masking,anthropogenic effects (Hessen et al., 2009). Silicate, a required ionfor diatom growth, is likely to weather more readily as mineralsdecompose at increased temperatures. Silica may limit the growthof diatoms in spring in lakes (Lund, 1950, 1964) and diatoms areprime food sources for zooplankton. In turn zooplanktivorous fishmay benefit but there are too many confounding factors to be certain.Nonetheless there are strong hints of important processes, not least inmountainous areas. Increased temperature has been associated withgreater weathering and increases in pH and major ions inalpine lakes (Koinig et al., 1998; Sommaruga-Wögrath et al., 1997).Drought has reduced inputs of coloured dissolved organic matter(Sommaruga-Wögrath et al., 1997; Yan et al., 1996), with conse-quences for reduced absorption of potentially damaging UV-B radiation(Sommaruga et al., 1999). Melting of rock glaciers (boulder moundsheld together with ice) has released high concentrations of trace ele-ments such as nickel into some alpine lakes (Nickus et al., 2010).

There may also be many secondary catchment effects of climatechange on nutrient loading. These include increases in frequencyand intensity of forest fires (Bayley et al., 1992; Kelly et al., 2006)and of deforestation by increased outbreaks of insect pests (Kurz etal., 2008). Some migratory bird flocks, for example snow geese,are increasing in size, as growth seasons lengthen, and potential forguanotrophication increases (Cote et al., 2010). Conversely clima-te-related changes in ocean currents are believed to be contributingto reduction in numbers of anadromous fish that were previouslyimportant in completing the nutrient cycles of headwater lakes,where they spawn (Reist et al., 2006a, 2006b).

More is perhaps known about catchment and airshed effects ofatmospherically derived elements like N, and of C because of theirroles as greenhouse gases. Evidence has accumulated that the plankton-ic systems, at least, of lakes are likely to be heterotrophic in their pristinestates (Alin and Johnson, 2007; Cole and Caraco, 2001; Reynolds, 2008).There has been an increase in dissolved organic matter (DOC) deliveredto lakes from their catchments in recent decades (Evans et al., 2006;Worrall et al., 2004) and the rather refractory brown and yellow DOCcompounds, which remain after decomposition of terrestrial litter, maybe rendered less refractory by the effects of ultra violet light duringtheir passage down rivers (Cole, 1999). This may amount to a scenarioof increased bacterial and animal production in lakes owing to climateinduced mobilisation of terrestrial organic matter, but there are otherpotential explanations for the recent increase in transported DOC. Oneis that soils, becoming less acid, as sulphur emissions have been reduced,release more organic matter (Monteith et al., 2007; Tranvik and Jansson,2002) and another is that land use changes, including deforestation,peat drainage, and cultivation,may be responsible There appears to be lit-tle experimental evidence for any of the explanations. Yet again we aretalking of possible effects of climate change rather than convincinglydemonstrated ones because of the confounding effects of other processesand the lack of direct experimentation.

Lakes and rivers are frequently supersaturated with carbon diox-ide resulting from respiration of organic matter that must have beenproduced outside the lake (Cole et al., 1994) (if it had been producedwithin the lake, carbon dioxide concentrations would fluctuatearound equilibrium). Whether this excess carbon dioxide is importedas carbon dioxide respired in the terrestrial soils, or in the headwaterstream systems, which are assuredly heterotrophic in forested ter-rain, or as particulate organic matter respired within the lake is notknown. However, it is clear that a great deal of carbon dioxide(Sobek et al., 2005), and also of methane is released from lake andriver systems and that the freshwater system is not a passive trans-port system for carbon from the land to the sea, as has generally

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been assumed in models of the global carbon cycle (Cole et al., 2007).Indeed much of the carbon transported from the land or wetland sys-tems may either be stored in lake or wetland sediments, or metabo-lised. The storages (Dean and Gorham, 1998) appear to be substantialand greater than those of the oceans (Downing et al., 2008) and muchof the excess net production of land ecosystems, believed to be held inland storage, and calculated by difference rather than directlymeasured(IPCC, 2007), may in fact be processed within the freshwater system.This has major implications in that management and use of rivers andlakes could have effects on carbon transfers to the atmosphere. Drain-age of floodplain systems could have increased carbon emissions by ox-idation of storedmaterial on the onehand,whilst eutrophication,whichtends to reduce dependence of lake metabolism on imported organicmatter, could have increased the amounts stored in lake sediments.

Because of the strong greenhouse effect of nitrous oxide there hasbeen interest in denitrification. Nitrogen enters the freshwater sys-tem through direct in-situ fixation, through indirect fixation in theterrestrial soils and subsequent leaching, through ammonia andnitrate dissolved in rain and originating from volatilisation frommanure and fossil fuel burning, respectively, and or through leachingof fertiliser applied to agricultural land andplantation forests. In pristinesystems nitrogen was probably scarcer than phosphorus (Bergstromand Jansson, 2006) or both were co-limiting (Moss, 1990; Moss et al.(in press)). Terrestrial systems have access to weathered soil phos-phorus through roots andmycorrhizae, whereas many of the aquaticproducers depend on direct uptake from water that is low in both Nand P, because of efficient retention, at least in pristine land systems.N was probably fixed less readily in land systems because fixationrequires microaerophilic conditions that can be found in root nod-ules and soil clusters, but more readily in waterlogged habitats.Tropical habitats tend to be more depleted in nitrogen than coolerones (Talling and Lemoalle, 1999) partly because denitrification istemperature-dependent, but perhaps also because of loss of nitro-gen as ammonia when the landscape is naturally or deliberatelyburned. Increased warming may thus increase denitrification; itmay also increase fixation, which is similarly dependent, so we donot know the net effect. The current production of about as muchfixed nitrogen by the Haber Process as natural fixation confoundsthe issue, and the build up of both ammonium and nitrate in the at-mosphere through intensive livestock rearing and vehicle enginecombustion also make it very difficult to estimate potential climateeffects There are suggestions that increased nitrogen availabilitythrough fertilisation may be resulting in greater land productionand carbon fixation, but the net effects on lakes are unknown and in-deed the net effects on the global carbon cycle are difficult to esti-mate as greater production in some areas may be offset by landdegradation elsewhere (Reay et al., 2008).

4.3. Internal Lake Processes

There ismore substantial ground for determining effects of changingclimate on in-lake processes. There have been widespread increases intemperature, increases in the length of the ice-free season and longerperiods of lake stratification (Adrian et al., 2009; Magnuson et al.,2000). There has also been an increase in the dry periods of arid-landlakes, increases in salinity and extinction of many of them in areas likethe Middle East (Beklioglu and Tan, 2008; Kucuk et al., 2009), centralAfrica (Onyekakeyah, 2010) and the prairie provinces of Canada(Laird et al., 2003; Van der Kamp et al., 2008).

Much work has concentrated on internal changes in the openwater of temperate lakes. The typical pattern of nutrient change incool temperate lakes tends to be the yardstick against which changesin other lakes is measured for there has been much more emphasis onsuch lakes than on others, simply because of the concentration of lim-nologists in Europe and North America and Japan. Non-conservativenutrients, such as N, P, and Si, whose concentrations are greatly

changed by biological activity, tend to build up during winter andearly spring when inflow is greatest. Frozen winter landscapes delaythis process until spring thawing. Biological activity is not absentduring winter, but it is low largely for lack of light to drive photosyn-thesis, especially under frozen lakes with an opaque cover of snow.There is a major uptake of nutrients in spring and a timing of algalgrowth that is prolonged until one or other nutrient, or several simul-taneously, become limiting, and taken up at rates greater than there-supply from the inflows and internal recycling. One effect of risingtemperatures is thus to increase the period of re-supply by earlierthawing of the catchment and to bring the start of spring activity ear-lier through melting of the lake ice and snow (Winder and Schindler,2004), with subsequent effects on zooplankton populations (Winderet al., 2009). Greater winter rainfall will also have similar effects.

Following the spring pulse, available nutrients usually becomescarce, and meanwhile the thermal stratification of the lake, if it isdeep enough, has begun. In general the warmer the lake the moreprolonged and stable is the stratification because the rate of changeof decrease in density of water increases as temperature increases.Phytoplankton and detritus are generally denser than water andsink, being otherwise maintained in suspension by eddy currents,and as stratification strengthens, nutrient-containing material fallsthrough the thermocline. As nutrients are depleted in the epilimnionthey accumulate in the hypolimnion through bacterial decompositionso long as oxygen stocks last, after which a set of well-known redoxprocesses, also driven by bacteria, leads to denitrification of nitrate,accumulation of ammonium, mobilisation of reduced ions of manga-nese and iron, conversion of sulphate to sulphide and its subsequentprecipitation as the black iron II sulphide that colours anaerobic sedi-ments, release of phosphate, and finally a switch from aerobic respira-tion, with carbon dioxide as the end product, to anaerobic respirationand methane production (Mortimer, 1941, 1942). Intensification andprolongation of thermal stratification with warming intensifies theseprocesses and their biological consequences (Jensen and Andersen,1995; Dröscher et al., 2009; Durant et al., 2007).

Methane escapes to the atmosphere once the hypolimnion wateris saturated and there may be some return of available phosphateand ammonium to the epilimnion in summer, owing to some windgenerated mixing around the thermocline, but generally the summeris a period when nutrients are scarce in the epilimnion, for there islittle replenishment from the catchment, where evaporation nowmatches or exceeds precipitation. This does not mean a cessation ofbiological activity in the lake, however, because there is recycling(Laird et al., 2003) within the epilimnion, driven by Protozoa and zoo-plankton feeding on detritus and algae, on fish predation of the zoo-plankton, and animal excretion. There may also be movements ofcyanobacteria and dinoflagellates between the surface waters andthe thermocline, where nutrients regenerated in the hypolimnionmay be picked up (Ganf and Oliver, 1982) and a distinct algal commu-nity around the thermocline, a region called the metalimnion. If suffi-cient light penetrates, there may be layers of photosynthetic bacteriausing hydrogen sulphide and other reduced substances as hydrogendonors in the metalimnion and hypolimnion (Moss, 1969). Intensi-fied stratification, however, may override these adjustments.

In autumn, nutrient supply increases again as more water entersfrom the catchment, and when the stratification is weakened by cool-ing and overturned by the rising winds. The comparative biologicalquiescence of winter then takes over and nutrients again begin tobuild up in the water until the catchment freezes again. This basicpattern is altered in polar lakes by a prolonged winter freeze and avery short spring and summer. Under prolonged ice cover, inversestratification develops because (pure) water is densest at 3.94 °Cand the resulting isolation from the atmosphere may lead to anaero-biosis and a parallel set of chemical changes to those occurring in ahypolimnion in summer. Methane may accumulate very abundantlyto be released when the ice melts (Walter et al., 2006). In polar

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summers, the waters may not stratify and nutrients are kept in circu-lation until refreezing perhaps only two or three months later. Forone well-studied arctic lake, Toolik, in Alaska, a comprehensivescenario has been worked out for a continued warming trend (Hobbieet al., 1999). It involves thawing of permafrost, mobilisation of morephosphorus, and increase in benthicmoss andfish production, followedby stronger summer stratification, loss of nutrients to the sediments,deoxygenation of the hypolimnion and eventual loss of top predatorfish, increase in forage fish, reduced zooplankton grazing and increasedalgal crops. The importantmessage is that climate changewill not resultin a single change, but a set of continuing consequences, whose ultimatedestination is highly debatable.

In tropical lakes there is ‘endless summer’, with prolonged or per-manent stratification and, in the dry tropics, very limited pulses ofnutrients derived from the catchment, where rainfall is low and highlyseasonal. In the wet tropics, prolonged stratification may be accompa-nied by continuous inflow, but its nutrient content is low because ofefficient retention by the continuously growing catchment vegetation.Loss of nutrients in the dry season through more intense stratificationhas been associated with reduction in plankton and fish productivity inthe tropical Lake Tanganyika (O'Reilly et al., 2003), which has warmedby about 0.6 °C since 1970, and there have been similar changes in LakeMalawi (Castaneda et al., 2009). There may be confounding of nutrienteffects, however, with reduced fish production through over-fishing(Sarvala et al., 2006).

Additional dimensions to an infinite continuum of latitudinal lakestates are given by altitude, where the latitudinal changes are mirrored,and warming has had consequences for benthic chironomid communi-ties (Eggermont et al., 2010), and by area and depth, where in shallowlakes there may be no stratification and dominance by littoral commu-nities that are present, but proportionately small, in deeper, larger lakes.The continuum is also extended by small ponds, where fish and theirinfluences may be absent, and reservoirs, often already disabled lakes(Moss, 2008), lacking a littoral zone, and managed at the whim ofhuman need that alters inflow and outflow rates. The many ways thathuman activities change nutrient loading, in the global problem ofeutrophication complicate the pattern even more.

All this provides a vast set of particular circumstances for the pro-duction of PhD theses, but makes generalisation of the effects of climatechange on lake nutrient cycling particularly difficult. Reductions in theperiod of ice cover, increases in the strength of stratification and earlieronset of the spring growth of algae and zooplankton are all well illus-trated (Dröscher et al., 2009; Winder and Schindler, 2004). Additionaleffects come from changes in disease incidence. Chytrid fungi infectalgae, and infection rates may increase with warming, resulting in dis-placement of previously dominant species by others (Ibelings et al.,2010). The ramifications of changes in spring in terms of summer pro-cesses, such as summer production, survival of young-of-the-year fish,and their impacts on zooplankton, and thence the composition andactivity of the summer communities, are less clear. The existing exper-imental work is very limited and confined to a very few studies onexperimental mesocosms that inevitably mimic small, shallow lakes,dominated by littoral zone conditions. For deeper lakes, experimentswith artificial mixing and isolation of water in large tubes (M. Forsiusin Nickus et al., 2010; Reynolds and Butterwick, 1979) give only a fewclues as to how more intense stratification and changes in rainfall andnutrient loading may affect lake functioning.

4.3.1. Experimental StudiesTwo main sets of well-controlled, shallow-lake mesocosms have

been studied, one in the north-west UK (Feuchtmayr et al., 2007,2009; Feuchtmayer et al., 2010; McKee et al., 2000, 2002a, 2002b,2003; Moss et al., 2003; Moran et al., 2009) the other in Denmark(Christoffersen et al., 2006; Jeppesen et al., 2010a, 2010b; Liboriussenet al., 2005; Ventura et al., 2008). Two, twenty-four month longexperiments on the effects of temperature (ambient, +3 °C and

+4 °C), nutrient loading and presence and absence of fish havebeen carried out in the UK mesocosms; the Danish experiment is along-running one and uses three temperature regimes (ambient,IPCC scenario A2 and A2+50%) on treatments that resemble systemsof turbid, plankton-dominated, high-fish-density, shallow lakes andclear, macrophyte-dominated, low-fish-density lakes. A third, smallerset of less-well-controlled mesocosms has been established in thesouth of England (Yvon-Durocher et al., 2010, 2011), from whichresults have been published on carbon exchange and phytoplanktoncommunity structure. There has also been a partly controlled experi-ment in mesocosms within a lake in Canada (Graham and Vinebrooke,2009) and an experiment done by establishing similar mesocosms inbroadly similar shallow lakes across a latitudinal gradient with six loca-tions from Finland to Southern Spain (Moss et al., 2004; Stephen et al.,2004). The Canadian experiment investigated the effects of reducingand increasing inputs of catchment water, including differential amountsof nutrients and dissolved organic carbon, in suspended polyethylenebags thatwerewarmedby placing transparent covers over them to createa local greenhouse effect and by immersing canisters of warmwater, andcooled using ice; the European experiment looked at the effects of nutri-ent additions in the presence or absence of fish. There has also been aSwiss experiment with heated mesocosms set in a shallow lake, whichconcerned itself with the effects of temperature on decomposition pro-cesses (M.O. Gessner in Jeppesen et al., 2010b).

The NW UK experiment in 1998–2000 heated the mesocosms by3 °C above ambient in a randomised block design that included amild eutrophication treatment and the presence or absence of fish.Warming had no effects on nitrate and ammonium concentrations,but significantly increased soluble reactive and total phosphorus con-centrations, conductivity and alkalinity, and decreased pH (McKee etal., 2003). In a second experiment in 2006–2007 using a 4 °C increaseand nutrient additions in line with current loads in agriculturalareas, warming again significantly increased SRP, and significantlydecreased TN, increased pH and increased conductivity (Feuchtmayret al., 2009). The common nutrient trends in the two experimentswere rises in SRP and conductivity, the former attributed to greaterrelease from the sediments, the latter to mineralization of soil parti-cles. In both experiments warming significantly reduced oxygen con-centrations and saturations and the conclusion was that warmingwould exacerbate the symptoms of eutrophication. There weresome fish kills attributable to warming in the first experiment, andin the second, warming significantly reduced fish biomass, and incombination with nutrient addition killed all the fish by the end ofthe experiment (Moran et al., 2009). Concomitant controlled aquariumexperiments showed thatwarming through up to 6 °C resulted in a pro-gressive decline in breeding activity and subsequent care of the youngin the fish (three-spined stickleback, Gasterosteus aculeatus), used inthe experiments (Hopkins et al., 2011). In the second experimentwarming also promoted the growth of floating plants (Feuchtmayr etal., 2009), in a parallel with a tendency for floating plants to dominatein tropical lakes and with the results of simpler experiments underglasshouse conditions (Netten et al., 2010). Floating mats create dark,still, deoxygenated conditions under them. Such changes have conse-quential effects on nutrients through release of phosphorus and ammo-nium from sediments.

4.3.2. Exacerbation of Eutrophication SymptomsSpace-for-time studies also suggest an exacerbation of eutrophica-

tion symptoms in warmed lakes through changes in the food webs.Common symptoms of eutrophication are increases in phytoplanktonalgae and particularly in cyanobacterial blooms. These can comeabout by various combinations of increased nutrient loading anddecreased zooplankton grazing, itself exacerbated by increased fishpredation (Moss et al., 2004). Warm lakes tend to have large popula-tions of small, zooplanktivorous or omnivorous fish (Texeira de Melloet al., 2009) that reproduce several times each year and reduce

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zooplankton populations to low numbers of small species that areleast efficient at grazing (Gyllstrom et al., 2005; Iglesias et al., 2011;Jeppesen et al., 2010a, 2010b; Moss, 2010b; Vakkilainen et al.,2004). The chlorophyll to phosphorus ratios tend to be higher in suchlakes, as do the proportions of Cyanobacteria. In recent years limnolo-gists have promoted long-known concepts of nutrient limitation andsufficiency to the purported nomenclatural novelty of stoichiometry,though this term should perhaps be allowed to retain its precisemeaningthat relates to the proportions of elements in compounds and reactions,rather than in mixtures. They argue that increased carbon dioxide levelscoupled with reduced phosphorus owing to stabler stratification willlead to high C to N ratios and production of algae such as Cyanobacteriathat may be less palatable to zooplankters, thus reducing the efficiencyof nutrient recycling within the lake (van de Waal et al., 2010).

In the NW UK mesocosms there was an increase in chlorophyll,attributable to warming in the second experiment, but no increasein the biomass or proportion of Cyanobacteria. This was also thecase in the southern UK experiment (Yvon-Durocher et al., 2011)where the organism sizes of the algae decreased. This may havebeen because the mesocosms were littoral systems, dominated byplants, whereas bloom-forming Cyanobacteria are characteristic ofopen waters not dominated by plants. Meta-analysis of data on bacte-ria, invertebrates and fish suggests that with warming organismsbecome smaller, as a phenotypic effect, and more fish are clusteredin smaller size classes (Daufresne et al., 2009), but whether this find-ing has relevance when species selection and natural selection arechanging the community is uncertain. Cyanobacteria are often abun-dant in shallow lakes where plants have disappeared. In temporarymesocosms set in lakes in Europe there was some evidence of greatercrops of Cyanobacteria and of reduced grazing at the warm end of thegradient (Vakkilainen et al., 2004; Van de Bund et al., 2004) and therole of nutrient limitation, as opposed to fish predation in determin-ing the phytoplankton community became more important withdecreasing latitude (Moss et al., 2004). In the Canadian experiment,(Graham and Vinebrooke, 2009), warming over 50 days gave someincrease in moderate sized algae when DOC concentrations wereincreased and there were complex interactions between warmingand DOC on different groups of zooplankters. The results differedfrom observations in nearby lakes that had been monitored whilstwarming through the global trend. Disparity between small meso-cosms and large lakes is likely to be general where effects on planktoncommunities are concerned; effects on littoral communities deducedfrom mesocosms are likely to be more realistic.

Predictions that Cyanobacteria will increase in proportion withwarming are based on space-for time studies, knowledge of traits, andmodels (de SenerpontDomis et al., 2007; Jöhnk et al., 2008;Markenstenet al., 2010; Paerl and Huisman, 2008; Wagner and Adrian, 2009a,2009b; Kosten et al., 2012) but as yet only a little direct experimentalevidence (Van de Bund et al., 2004). Several studies have pointed outthat eutrophication effects per se have been much more importantthan climate effects so far in determining plankton structure and func-tion (Kosten et al., 2009; McKee et al., 2003; Moss et al., 2003,) butindications are that symptoms of eutrophication will be exacerbatedby warming (Blenckner et al., 2006; Jeppesen et al., 2010a, 2010b)and that consequently measures for restoration of eutrophicated lakesby control of nutrients will have to become more stringent.

4.3.3. Carbon ExchangeThe decline in oxygen concentrations in warmed mesocosms

offers a second insight intomajor effects of warming on nutrient cycles.In theNWUK2007 experiment, diel cycles of oxygenweremeasured inmid summer, in heated and unheated mesocosms, and estimates madeof gross production and community respiration (Moss, 2010b). Themesocosms contained organic sediment with about 8% organic matter,well within the range found for shallow lakes, and, despite abundantplants, were heterotrophic systems even at ambient temperatures.

Warming by 4 °Cmade them evenmore heterotrophic with very signif-icantly increased depletion of oxygen and thus release of carbondioxide. Net ecosystem production, the difference between gross pro-duction and community respiration, decreased from −4.08 to−6.73 mg O2 L−1 h−1 and the ratio of community respiration togross production increased from 1.41 to 1.85. To some extent this effectmay have been exacerbated by release of more oxygen than carbondioxide direct to the atmosphere by the floating plant cover, butsimilar results have also been obtained in the southern UK experiment(Yvon-Durocher et al., 2010). These mesocosms were autotrophic atambient temperature, had submerged plants but fewer floating ones,and were heated by 3–5 °C. Warming significantly increased the ratioof community respiration to gross photosynthesis from an annualmean of 0.83 to 0.98, an 18% difference. The experiments were carriedout every two months for a year and showed a consistent pattern ofraised gross production and respiration with warming, but always agreater effect on respiration, such that the warmed systems becameheterotrophic from May to October. Warming generally increases therate of respiration of lake sediments (Gudasz et al., 2010).

The significance of the findings of both sets of experiments is thatwarming may mobilise a great deal of carbon from stores in the sys-tems. A large carbon store exists in the wetlands and shallow lakesof the subarctic and boreal regions (Millennial Ecosystem AssessmentBoard, 2005), where temperatures are likely to rise more than theglobal mean (IPCC, 2007). Standing waters also release a great dealof methane (Huttunen et al., 2003; Xing et al., 2005), potentiallymore than stored as carbon in terrestrial systems (Bastviken et al.,2011).

4.3.4. Internal AdjustmentsWarming has often advanced seasonal events in lakes (Adrian et

al., 2009; Thackeray et al., 2010) and these inevitably have effectson subsequent internal processing of major nutrients. However,rapid evolutionary adaptation to warming, at least in organisms upto the size of zooplankters, (Hairston et al., 1999; Van Doorslaer etal., 2007, 2009, 2010), and even in large fish (Hendry et al., 2000)might counteract to some degree any disruption in existing seasonalpatterns. There is also a high capacity for physiological adjustmentin many organisms and evidence of changes in range, particularly ofinsects with aerial adult though aquatic juvenile stages (Hassall etal., 2007; Parmesan and Yohe, 2003). There is also a likelihood thatinvasive species, many of which come from warmer climates,simply because biodiversity is greater there, are favoured by warming(Stachowicz et al., 2002; Winfield et al., 2008). Changed precipitationpatterns will also mean greater water storage in more reservoirs,which appear to act as stepping-stones for invasion (Johnson et al.,2008). Inevitably it will be as impossible to predict the detailed effectsof warming on communities as it is to disentangle existing effects.Also many changes are not linear with temperature but show abruptresponses (Wagner and Adrian, 2009b; Weyhenmeyer and Karlsson,2009). We may have to confine our predictions to those of overallgross processes such as changes in overall diversity, in gross levelsof nutrients and in ecosystem processes such as gross photosynthesisand respiration (Moss et al., 2009). The key problems come with therange and complexity of other impacts on lake systems on the onehand and the difficulty of realistically replicating a catchment/lakesystem under controlled experimental conditions.

5. Questions 3 and 4: Importance of Likely Future Effects and theirMitigation

Many of the detailed effects that warming will cause in lakes maybe of little ultimate importance, though there is a tendency for theirseriousness to be over-emphasised in a world where the acquisitionof research funds has become highly competitive. There is normallya degree of variation in seasonality, driven by weather and the

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bringing forward of spring events by days, or even a month, is likelyto be met by adjustments within the system. Matches and mis-matches in events are normal parts of an ecosystem that, beingparts of a fluctuating hydrological system, are annually accommodat-ed. The basic processes of primary production, decomposition andmineralization will no doubt adjust, available nitrogen or phosphorusmay become limiting earlier in summer, hypolimnia that presentlyhave a little oxygen left may become anaerobic. But then, manyalready naturally do. There is much talk of mitigation in policy circles,but given an inevitable temperature rise, there is nothing that willsignificantly alter these changes. They are the adjustments that thesystem internally makes to accommodate change.

Real problems come with the consequences for ecosystem ser-vices to human societies, particularly the provision of drinkingwater and the availability of irrigation water from storage reservoirs.The impacts of introduced species, particularly floating plants, thatmay be promoted by increased release of phosphorus from sedi-ments, and fish that might increase pressures on zooplankton andperiphyton grazers and result in increase in algal crops, and in thesymptoms and therefore problems of eutrophication, are also likelyto be notable. The problem of eutrophication is already extensiveand although in the developed world there has been much effort atreducing it, particularly through phosphorus removal at wastewatertreatment plants, there remains a major issue of diffuse sourcesfrom agriculture, which are likely to increase with greater winterrainfall (Jennings et al., 2009; Jeppesen et al., 2009, 2011). In develop-ing countries, with high population densities, it seems likely thateutrophication problems will inevitably become very serious irre-spective of climate change. A final chapter, (Moss, 2010c) in a recentbook on climate change and its effects on freshwaters (Kernan et al.,2010) gives accounts of likely changes in human terms, based on dis-cussion workshops with scientists working at different latitudeswithin Europe. There will be many detailed impacts, though mostconcern a future lack or excess of water rather than changes in itschemical composition. Likewise, salinification owing to rises in sealevel is likely to be a secondary effect in a scenario of serious floodingof coastal cities.

Perhaps the key problem, however, will be the impact of increasein temperature on mobilisation of carbon from sediments and peats(Kosten et al., 2010) within lakes, particularly of the boreal and northpolar zone. The freshwater system is a major focus, possibly the majorfocus of transfer of carbon back to the atmosphere following its fixationin photosynthesis. The indications are that a rise in temperature, wellwithin the predicted range for later this century, could lead to massiverelease of carbon dioxide and of methane. It is no longer a matter of sci-ence fiction that positive feedback effects from this could lead to a run-away greenhouse effect.

Mitigation against such a possibility then becomes a seriousmatter. The lay public widely believes that all that needs to be doneto halt climate change is to reduce carbon emissions from the burningof fossil fuel. Reducing carbon emissions gives the possibility of halt-ing then reversing temperature rise but does not guarantee it. Therate of emission has to become lower than the rate of carbon storagebefore temperature rise will reverse and carbon storages are indecline.

The Millennium Ecosystem Assessment (Mantua et al., 2005)found that 50% of most natural ecosystems had been seriouslyimpaired by 1950 and projected that more than 70% will have beenlost or seriously damaged by 2050. The two ecosystems that haveremained extensive are the tundras and boreal forests, but it is inthese that most of the world's lakes and wetlands, created by theFlandrian glaciations, are found and in these where remobilisationof carbon dioxide and methane is likely to be most intensive. Theoceans provide a considerable carbon sink (IPCC, 2007), but progres-sive acidification owing to carbon dioxide dissolving from the atmo-sphere may be undermining this (Guinotte and Fabry, 2008). There

is much talk of geoengineering (Lampitt et al., 2008; Lovelock,2008), including many symptom treatments and some, such as carboncapture and storage (Lal, 2009), that seek to retain carbon dioxidereleased from continued burning of coal, or devices to artificially absorbcarbon dioxide chemically from the atmosphere.

But almost no attention has been given to reinstating natural eco-systems that, through the efficient tempering of natural selection, areprobably the most efficient systems of all for manipulating the carboncycle. Reafforestation has been mooted, but on a limited scale, whilstpreservation of existing forest, although essential, does nothing buthold the line. Extensive reafforestation is an attractive idea, butforests that retain carbon and the associated freshwaters that storesome and metabolise other of it, are not the simple plantations envis-aged. They are integrated systems, with freshwaters bearing to theforest a relationship not unlike the bloodstream and the tissues, in-separable and mutually dependent. Restoration of forest must be res-toration of complete systems if there are to be tangible benefits, andthat means a strategy that includes the release of large areas of landfor ecosystem restoration. Such a strategy would have to include cre-ation of liveable cities and a highly efficient agriculture on a muchsmaller area of land than presently used, to feed a population thatwill continue to increase until the middle of this century. There willalways be lakes in the landscape. The cogs in the endless machinewill continue to turn, but whether in a smoothly functioning engineor a Heath-Robinson contraption (Heath Robinson, 2007) is quiteunknown.

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