Aquatic Food Web Structure and the Flow of Carbon

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1 Article

Aquatic food web structure and the flow of carbon

Vladimir Matveev and Barbara J. Robson* CSIRO Land and Water, GPO Box 1666, Canberra, ACT 2601, Australia * Corresponding author: [email protected]

Received 23 December 2013; accepted 29 August 2014; published 3 November 2014

Abstract

Carbon cycling is a cornerstone concept of ecosystem ecology, which has implications for climate change, ecosystem health, and human activities. This review investigates pathways of carbon within freshwater ecosystems, the role of terrestrial carbon in food webs, and the effects of food web structure on C emissions. Carbon may co-limit primary production even in waters

super-saturated with CO2. Allochthonous carbon-subsidies make most lakes and rivers net heterotrophic; however, the use of carbon-subsidies by the food web (FW) may be limited by low nutritional quality of terrestrial C-compounds and the inability of bacteria to synthesise polyunsaturated fatty acids (PUFA), which are essential for metazoan growth. Bacterivorous nanoflagellates which can synthesise PUFA are likely to create a channel connecting allochthonous C with metazoan production in some water bodies. Published studies suggest that FW structure may affect: carbon fluxes in and out of lake ecosystems; carbon accumulation and distribution within food webs; burial of carbon and carbon sequestration. Food web structure and nutrients can affect the carbon-emission/sequestration ratio and shift the state of the aquatic ecosystem between being a source or a sink for atmospheric carbon. Small lakes, such as farm ponds, are the dominant type of world fresh waters with highest carbon burial rates. Their productivity and FW structure are often modified by humans through nutrient fertilisation and fisheries management. We hypothesise that the planned management of these activities targeting a desirable emission/ sequestration ratio, can be used as a tool for the reduction of carbon emissions to the atmosphere.

Keywords: Carbon cycling; organic carbon; terrestrial subsidies; HNF; food webs; microbial loop; trophic transfer efficiency; carbon emission and sequestration.

Introduction carbon cycle and may affect regional carbon balances (Cole et al., 2007) and global climate (Tranvik et al., 2009). Total

Understanding carbon (C) cycling is central to global emissions of CO2 from inland waters are similar

understanding global climate change and regional trends in magnitude to CO2 uptake by the oceans and to global in ecosystem transformations induced by human activities. terrestrial net ecosystem production (Tranvik et al., 2009). Inland waters are a significant component of the global

DOI: 10.1608/FRJ-7.1.720 Freshwater Reviews (2014) 7, pp. 1-24 © Freshwater Biological Association 2014 2 Matveev, V. & Robson, B.J.

Food webs are the key to understanding regulation other units do not have (Müller, 1992). Ecosystems have of the C-cycle by ecosystems; their structure affects autotrophic and heterotrophic components, which capture primary productivity, fish production and water quality energy, carbon and nutrients and transfer them through (Gophen, 1990; Kitchell & Carpenter, 1993). In this paper, food webs. Ecosystems are characterised by simultaneous we analyse how C enters freshwater ecosystems and is processes of primary production (carbon acquisition), processed metabolically, review how internal and external secondary production (carbon transfer) and decomposition C sources influence the structure of freshwater food webs, (carbon re-mineralisation). All three processes are and evaluate current conceptual models and hypotheses accompanied by respiration (carbon loss as CO2). regarding pathways of carbon in freshwater food webs. Carbon enters freshwater ecosystem metabolism through the following pathways: (a) autochtonous Carbon inputs and ecosystem primary production; (b) microbial decomposition; (c) metabolism consumers of live terrestrial organisms; (d) consumers of dissolved organic carbon (DOC) (Roditi et al. 2000); Where once lakes tended to be considered as isolated (e) consumers of imported detritus; (f) consumers of microcosms, it is now understood that lakes, like other colloidal microparticles formed from dissolved organic freshwater ecosystems, can be viewed as input–output matter by physical processes (Kerner et al., 2003) or from systems of energy (Hannon, 1973). Because most of an light-mediated flocculation of DOC (von Wachenfeldt organism’s energy is stored in carbon bonds (Morowitz, et al., 2008). These pathways can be called ecosystem 1968) and carbon accounts for a large proportion of an metabolic gates, because they control the mobilisation organism’s mass (e.g. 45–55% of the dry mass of plants and (sensu Jansson et al., 2007) and incorporation of carbon freshwater invertebrates (Salonen et al., 1976; Schlesinger, into ecosystem metabolism. Sources, sinks, and metabolic 1991), carbon is considered the currency of energy transfer gates in freshwater ecosystems are summarised in Table 1. in aquatic ecosystems (Dodds, 2002) and ecosystem Carbon may also enter ecosystems through paths productivities are often expressed in carbon units. that bypass these metabolic gates. For instance, charcoal Ecosystems may be defined as units of biological from bushfires deposited in river sediments has little organisation with specific emergent properties which or no nutritional value to consumers or decomposers

Table 1. Sources, metabolic gates and sinks of carbon in freshwater ecosystems.

Sources Metabolic gates Sinks microbial respiration atmospheric CO2 autochthonous primary production microbial decomposition terrestrial POC animal and plant respiration consumers of detritus

microbial decomposition burial in sediments terrestrial DOC consumers of DOC, such as some molluscs consumers of colloidal C or flocculated DOC removal by migratory or terrestrial animals, including humans live terrestrial organisms consumers of live terrestrial animals

export to downstream aquatic live aquatic organisms migratory fish and other animals environments refractory terrestrial carbon N/A (physical processing only) burial export downstream

and will not have a significant direct effect on ecosystem of CO2. Negative values of NEP imply a heterotrophic metabolism. Accumulation of charcoal indirectly affects ecosystem (Odum, 1971), supported by imported C. ecosystem metabolism by altering the properties of Table 2 summarises where P/R ratios of various benthic sediments and thereby modifying the composition values are likely to be found in freshwater ecosystems. and productivity of benthic communities. Benthic The majority of ecosystems of lakes and rivers are community structure and abundance may depend on heterotrophic (del Giorgio et al., 1999; Marcarelli et al., the sizes of substratum particles (Harrison et al., 2007). 2011) with a median ratio of P/R equal to 0.5 in streams Recalcitrant carbon, in general, has a modulating rather and 0.6 in lakes (Marcarelli et al., 2011). This means than a direct effect on ecosystem functioning, through that the release of CO2 from the ecosystem exceeds its modification of processes and interactions (Prairie, 2008). capture by photosynthesis and implies that the dominant The primary focus of this review is the fate of carbon role of C-subsidies in fresh waters is commonplace. compounds that enter ecosystem through metabolic gates. In a subtropical black-water river, the P/R-ratio could drop as low as 0.09–0.25 and stay low for years (Edwards Carbon balance and P/R-ratios in & Meyer, 1987). Similarly, a P/R ratio as low as 0.2 has been lakes and rivers measured in the epilimnia of humic lakes (Salonen et al., 1983). This suggests that these systems are heterotrophic Carbon enters aquatic ecosystems either through the and depend on external subsidies of organic carbon. conversion of CO2 into organic compounds in the By contrast, in the Murray River, Australia, the P/R process of photosynthesis (gateway a, above), or through ratio may stay at 1.0 along most of the river length during the import of and subsequent processing of terrestrial the flood-free period, so the input of allochthonous organic matter (gateways b to f), which entails respiratory organic C may be less significant in fuelling ecosystem processes. Primary production and respiration together metabolism (Oliver & Merrick, 2006) and the food web characterise the metabolism of an ecosystem. Gross could depend on phytoplankton. However, the P/R primary production (P) is the fixation of CO2 -carbon ratio may be expected to drop if flooding would bring by photosynthesis. Ecosystem respiration (R) is total large quantities of DOC, stored in the floodplain black remineralisation of organic carbon by all organisms to water (Howitt et al., 2007). In a smaller Australian river

CO2 or CH4. The ratio between primary production and with forested headwaters, the P/R-ratio varies from 0.05 respiration (P/R) partly characterises the input/output to 0.5, suggesting strong heterotrophy (Chessman, 1985). ecosystem carbon balance. The P/R-ratio can vary significantly within the same Net ecosystem production (NEP) is the difference river along the longitudinal gradient. The river continuum between P and R. When P > R, NEP is positive and the concept (Vannote et al., 1980) suggested that P/R can take ecosystem can accumulate or export organic C. Lakes values from under 1.0 in forested headwaters with low light with P > R are net CO2 sinks. When NEP is negative, and large import of organic C, to over 1.0 in downstream R > P and the system respires more C than is produced reaches with good light and smaller external loads of organic by primary producers. Lakes with R > P are sources C. Over the years, several variations on and alternatives to

Table 2. P/R values in freshwater ecosystems. P/R Freshwater environment ≥1 shallow eutrophic lakes and rivers (Oliver & Merrick, 2006); surface photic layer of productive (mesotrophic and eutrophic) lakes (del Giorgio & Peters, 1993) <1 oligotrophic lakes (del Giorgio & Peters, 1993); humic lakes, rich in DOC (Salonen et al., 1983); subtropical blackwater rivers (Edwards & Meyer, 1987); river headwaters (Chessman, 1985) 0 deeper layers, below the surface photic zone (Hessen, 1998); regions of elevated microbial decomposition

DOI: 10.1608/FRJ-7.1.720 Freshwater Reviews (2014) 7, pp. 1-24 4 Matveev, V. & Robson, B.J. the river continuum concept have been proposed. Some deposited at the surface of a water body by wind or rain, of the most prominent of these are summarised in Table 3. or brought into a system by waterbirds or other animals. It has been suggested (Odum, 1985; Xu et al., 2001) Both t-DOC and t-POC provide additional substrates for that in stressed or unhealthy ecosystems, the P/R-ratio microbial decomposition, while t-prey reduce the P/R ratio should become unbalanced (< or >1). However, as in by supporting additional respiration, required for their most lakes and rivers P/R is naturally much lower than 1 digestion and assimilation. In some instances, marine (Marcarelli et al., 2011), this criterion for ecosystem health carbon subsidies to freshwater systems, such as carbon may not hold. In experimental lakes, P/R may increase in brought upstream in the form of migrating fish, have also response to fertilisation, but may decrease with changes in been found to be important (Wipfli et al., 2003). stoichiometry, that is, from high to low N:P-ratios (Schindler, The contributions of the three types of subsidies 1990). It can also increase in response to lake acidification if (t-DOC, t-POC and t-prey) to ecosystem metabolism pH drops below a threshold, which switches off nitrification are not equal. DOC may exceed POC by an order and by this inhibits bacterial activity (Schindler, 1990). of magnitude or more (Allan, 1995; Wetzel, 2001; Ostapenya et al., 2009). In temperate lakes, the pool of Three types of terrestrial subsidies dissolved C, which is often mostly of terrestrial origin, may exceed the combined pools of phytoplankton, Reduced P/R ratios in fresh waters often result from zooplankton and fish by a factor of 53 (Prairie, 2008). the import of catchment organic matter, which leads to The bioavailability of terrestrial organic material varies increased bacterial respiration. There are three types as a function of its origin and chemical form (Baldwin, 2013). of ecosystem subsidies contributing to the observed While the recalcitrant part of t-DOC can be flocculated heterotrophy: terrestrial dissolved organic carbon (t-DOC), (von Wachenfeldt et al., 2008) and stored in sediments terrestrial particulate organic carbon (t-POC), and live prey or exported from freshwater ecosystems, labile DOC is delivered by wind or advection to consumers (t-prey), for readily available for bacterial utilisation. Labile DOC has instance, terrestrial insects eaten by fish. Terrestrial-POC been found to average 14% of total DOC in boreal lakes and t-DOC may be delivered with catchment runoff, and 19% in rivers of varying productivities (Søndergaard & Table 3. Prominent conceptual models of carbon cycling in river systems.

Concept Key features Relevant to Source River Continuum Food webs are driven by terrestrial carbon subsidies River systems with Vannote et al. (1980) Concept in headwaters, grazing of carbon from upstream in forested headwaters middle reaches, and autochthonous production in lower reaches Serial Dams and weirs modify river function, creating a Rivers interrupted Ward & Stanford Discontinuity series of alternating river runs (benthic production by weirs and dams (1983, 1995) Concept and grazing) and weir pools (pelagic production and deposition)

Flood Pulse Carbon may be dominated by floodplain production Tropical rivers and Junk et al. (1989) Concept during flood events other intermittently flooding rivers Functional The metabolism of each part of a river depends on the Large river systems Thorp et al. (2006) Process Zones local physical environment and connectivity with other zones

Middelboe, 1995). This indicated widespread dominance Carbon limitation of primary of recalcitrant DOC, but also the fact that a significant production part of total DOC goes directly to microbial utilisation. In whole-lake experiments, it has been shown that both It has long been known that phosphorus and nitrogen autochthonous and allochthonous sources of carbon are can limit primary production in fresh waters. Elser et al. important for bacterial production (Kritzberg et al., 2004). (2007) provided a comprehensive synthesis of published Consumption of DOC by heterotrophic bacteria is experimental data in support of this concept. On the other one of the largest fluxes of C in most aquatic ecosystems hand, the limiting role of carbon was debated. Import of (Cole, 1999). Transfer of C from the recalcitrant pool to t-DOC to aquatic ecosystems may result in an increased one of the metabolic gates is possible through the process production of CO2. DOC concentration in lakes is strongly of photo-oxidation (Granéli et al., 1996), which can be correlated with pCO2 (Sobek et al., 2003), suggesting further used in algal photosynthesis. Photolysis breaks multiple effects of photo-oxidation and bacterial down complex compounds to the molecules of low decomposition. Most world lakes are supersaturated with molecular weight making them more prone to bacterial CO2 (Cole et al., 1994; Sobek et al., 2003). Supersaturation utilisation (Stewart & Wetzel, 1982; Geller, 1986; Kieber is probably also commonplace in other lentic systems, such et al., 1989; Wetzel et al., 1995; Bertilsson & Tranvik, as reservoirs, ponds and wetlands. 1998; Cole, 1999), and leading to the formation of DOC, It was believed previously that migration of atmospheric which is more efficiently incorporated into bacterial CO2 to lakes was always sufficient to preclude carbon biomass (Lindell et al., 1995; Amon & Benner, 1996). limitation of phytoplankton production in unproductive It has been suggested (Wetzel, 1995; Hessen, 1998) lakes (Schindler et al., 1972; Schindler, 1977). Experimental that large pools of recalcitrant terrestrial DOC in aquatic organic carbon enrichment of a lake had no effect on ecosystems have a stabilising effect on ecosystem primary production (Schindler, 1974). However, it has dynamics by reducing fluctuations of consumer biomass been found that carbon as CO2 can promote phytoplankton through stable supply of low-quality food from the growth under CO2 supersaturation (Jansson et al., 2012). bacterial-based food chain, which may not allow rapid As carbon subsidies drive CO2 supersaturation, Jansson population growth, but can assist consumers’ survival. et al. (2012) proposed that lake primary productivity Although additional input of DOC to lake or river should respond to variations in carbon input from may be thought to increase productivities of trophic levels catchments due to human activities or natural processes. as a result of utilisation of the labile C fraction, modelling The term “cultural eutrophication” has long been suggests that the outcome may be more complex, as optical applied to increases in algal productivity of lakes and inhibition of photosynthesis due to chromatic dissolved rivers accelerated by human activities (Wetzel, 2001). It organic material (CDOM) may exceed the enrichment is generally taken as a “given” that nutrient (nitrogen effects of DOC (Jones et al., 2012). This has been observed and phosphorus) loading drives these algal productivity in the field, where increasing coloured DOC in boreal increases. The finding of the carbon co-limitation of lakes apparently reduced photosynthesis of benthic algae phytoplankton growth (Jansson et al., 2012) gives a new leading to a decline in total primary production (Ask perspective on understanding eutrophication: increased et al., 2009). Secondary production was also decreased phytoplankton productivity can potentially be stimulated as a result. Jones (1992) reviews photo-inhibition by by t-DOC as well as nitrogen and phosphorus. As humic substances of primary production in lakes. microbial activity is temperature-dependent (Castillo et al., Coloured DOC and nutrients can be equally important 2004; Berggren et al., 2009), global warming may accelerate in regulating primary production (Carpenter et al., 1998). both the release of CO2 from organic C imported to fresh waters (Boyero et al., 2011) and primary production.

DOI: 10.1608/FRJ-7.1.720 Freshwater Reviews (2014) 7, pp. 1-24 6 Matveev, V. & Robson, B.J.

Carbon flux through food chains Food chain length

The often-used term “trophic level” implies the existence Food chain length (FCL) is an important ecological of linear food chains, where a plant species is consumed variable, which shows how many times C compounds by an animal, the animal is eaten by a predator, and so on. are transformed and energy used as carbon flows through The notion of the food chain helps us to simplify and better the ecosystem. Each step of transformation includes understand complex trophic interactions (e.g. Sprules & respiratory losses of CO2 and de novo formation of new Bowerman, 1988). A food chain is a path of carbon flux carbon structures in the bodies of consumers of the next within the ecosystem, starting from primary producers trophic level. or detritus. The “trophic level” of an animal is a notional The pioneering idea of the “green world” (Hairston et number of steps in this chain between it and the primary al., 1960) emphasised the potential role of top-down forces producer (trophic level 1). Non-whole number trophic in terrestrial food chains, suggesting that predators reduce levels may be assigned when an animal grazes at multiple the biomass of herbivores, allowing plants to flourish, levels in the food chain (e.g. consuming both predatory which makes the world “green”. In aquatic environments, and herbivorous fish). a similar notion came out of early experiments with fish in Carbon flowing from phytoplankton to zooplankton artificial ponds (Hrbáček et al., 1961), where the addition of grazers and further to fish goes along the herbivore food fish, which suppressed the biomass of zooplankton, caused chain (HFC). Alternatively, it may flow from DOC or an increase in algal biomass and accumulation of carbon in POC along the microbial food chain (MFC). The concept phytoplankton. A related concept of the trophic cascade of a microbial loop was first introduced in marine in lakes, elaborated later (Carpenter et al., 1985), focussed ecology (Azam et al., 1983), but has also been adopted on the effects of stocking piscivorous fish, which cascade in limnology (e.g. Horne & Goldman, 1994). DOC from down the food chain through a series of trophic interactions phytoplankton exudates, lysed cells and other sources and eventually reduce the phytoplankton C pool. provides a highly labile food source for bacteria, which are Food chain length influences community structure, grazed upon by heterotrophic nanoflagellates and ciliates. ecosystem functions (Carpenter & Kitchell, 1993) and Micro-consumers of bacteria may feed larger zooplankton, contaminant concentrations in top predators (Cabana & such as freshwater crustaceans (Burns & Gilbert, 1993; Rasmussen, 1994). It has been hypothesised that the impacts Balseiro et al., 2001) and small fish (Zingel et al., 2012). Thus, of human alterations of productivity will depend on the carbon released as DOC from cells is eventually returned FCL of the affected food chains (Kaunzinger & Morin, 1998). to the herbivore food chain, closing the loop. The import Mathematical models predict that FCL should be of C from catchment to lakes and rivers adds to the DOC limited by production at the base of the food chain (Smith, pool in the microbial loop; however, bacteria experience 1971; Oksanen et al., 1981). Laboratory tests with artificial greater growth efficiency on autochthonous compared to bacteria-based food chains supported the hypothesis allochthonous carbon, so bacterial growth and biomass (Kaunzinger & Morin, 1998), but the analysis of 113 natural correlate well with autochthonous production (Kritzberg terrestrial and aquatic ecosystems did not (e.g. Briand et al., 2005; McCallister & del Giorgio, 2008). Even in & Cohen, 1987). Accurate estimation of FCL based on the case of positive net primary production, however, stable isotope technique was applied in the analysis of 25 allochthonous DOC may account for a substantial lakes of varying trophy by Post et al. (2000), who tested proportion of bacterial biomass (Kritzberg et al., 2006a, b), for the combined or isolated effects of productivity and though it appears that much of this bacterial production ecosystem size and concluded that ecosystem size (lake contributes to bacterial respiration rather than making its volume) was the only predictor of food chain length. way into the food web (McCallister & del Giorgio, 2008).

Omnivory and food webs Effects of food web structure on ecosystem functioning While the notion of the food chain is a useful abstraction, natural communities are based on food webs, because Food web structure (FWS) can determine many properties many consumers are omnivorous (Thompson et al., of aquatic ecosystems. It can affect the community size 2007). Omnivory is believed to be common in freshwater structure of prey when predators are size-selective, such plankton (Sprules & Bowerman, 1988; Adrian & Frost, as planktivorous fish (Brooks & Dodson, 1965; Carpenter 1993). Herbivore and microbial food chains should be parts & Kitchell, 1993), internal and external C fluxes (Schindler of all aquatic ecosystems – the definition of the ecosystem et al., 1997), nutrient recycling (Attayde & Hansson, implies that the processes of production, transformation 2001), primary productivity (Carpenter et al., 1987) and and decomposition of organic matter must all be present. ecosystem P/R-balance (Cole et al., 2000). An ecosystem Plant and animal foods are often combined in the diets of is considered top-down controlled if the FWS and total consumers, at least, during different stages of ontogeny. production are determined by animals at the top of For instance, Nematalosa erebi (Australian gizzard shad or the food chain, and bottom-up controlled if the FWS is bony bream) is carnivorous when young, but feeds on determined by productivity at the bottom of the food web algae and detritus as an adult (Pusey et al., 2004). Even (McQueen et al., 1989). the species traditionally known as “herbivores”, under As the dominance of planktivorous fish in lakes scrutiny turn out to be partial carnivores. For instance, the and reservoirs suppresses herbivorous zooplankton common zooplankton filter-feeder Daphnia, long-believed grazers, carbon accumulation by phytoplankton, to feed only on algae, large bacteria and detritus, has also relieved from grazing, increases (Carpenter et al., 1987), been found to consume ciliates and rotifers (Porter et al., which implies increased capture of CO2 and increased 1979; Jack & Gilbert, 1994; Sanders et al., 1996). sedimentation (Flanagan et al., 2006). The FWS of lakes Key terms introduced in this and the immediately and reservoirs altered by manipulations of piscivorous preceding sections are summarised in Table 4. and planktivorous fish affects phytoplankton biomass, zooplankton size structure and biomass, as well as water quality (Gophen, 1990; Carpenter & Kitchell, 1993). The addition of top predators to lakes can increase

Table 4. Key terms relating to carbon cycling through trophic transfer.

Term Description

The chain of plants and animals through which carbon moves by production, grazing and Food chain predation.

The carbon pathway involving production of carbon by primary producers (plants and Herbivorous food chain Cyanobacteria). Microbial food chain The carbon pathway involving microbial uptake of carbon from non-living DOC and POC. The notional number of steps in a food chain between an animal and a primary producer (in Trophic level the herbivorous food chain) or non-living organic carbon source (in the microbial food chain).

Food chain length The number of trophic transfers as carbon flows through the ecosystem.

Food web A “food chain” involving multiple pathways and omnivory.

DOI: 10.1608/FRJ-7.1.720 Freshwater Reviews (2014) 7, pp. 1-24 8 Matveev, V. & Robson, B.J. zooplankton grazing (Carpenter & Kitchell, 1993), which item size, morphology and palatability often determine if decrease atmospheric carbon invasion to a lake (Schindler it would be ingested or not and eventually determines CE et al. 1997). In this way, top predators have a capacity to (Porter, 1973; Lampert, 1987; DeMott, 1988; deBernardi & alter ecosystem C- fixation. Although temperate lakes Giussani, 1990). are often net heterotrophic with negative ecosystem Consumer AE is a measure of digestibility and a ratio NP, experimental manipulation of the FWS to establish of assimilation to ingestion (Lampert & Sommer, 1997). It dominance of planktivores can shift NP to positive values, has been suggested that in benthic organisms, AE and PE making the ecosystem net autotrophic (Cole et al., 2000). depend on C:P and C:N ratios of food (Frost et al., 2002). As phosphorus often limits phytoplankton growth in Increasing C:P ratios of food reduces zooplankton growth aquatic ecosystems (Peters, 1986; Wetzel, 2001) and fish may (DeMott & Tessier, 2002; Sterner & Elser, 2002), and may play an important role in an ecosystem’s P-budget (Kitchell explain the absence of important herbivores in fresh waters et al., 1975), restructuring of fish communities, which with high sestonic C:P ratios, which are otherwise suitable leads to a new FWS, may imply changes in P-supply rates habitats (Sterner & Elser, 2002). Carbon TTE influences within the ecosystem (Kitchell & Carpenter, 1993; Vanni, fisheries production (Pauly & Christensen, 1995), 2002). Experimental separation of fish nutrient recycling biogeochemical cycling (Sterner & Hessen, 1994) and water effects from predatory effects suggests that fish indeed quality (Müller-Navarra et al., 2000). Meta-analysis by affect the ecosystem recycling pattern and, as a result, Pauly & Christensen (1995) suggests that mean TTE in both primary production (Attayde & Hansson, 2001). Most marine and freshwater aquatic ecosystems is close to 10%. recent research suggests that predator effects on nutrient cycling are likely to be ubiquitous (Schmitz et al., 2010). Bacterial carbon in the food web: Nutrient enrichment increases primary production, link or sink controversy causing lakes to become net sinks for atmospheric carbon; so nutrients and FWS together can determine whether Experiments with 14C-labelling of marine bacteria have lakes and reservoirs are sinks or sources of CO2 (Schindler suggested that bacterioplankton can be a sink for carbon in et al., 1997). The FWS of both lentic and lotic waters has planktonic food webs and may serve principally as agents been shown to affect CO2 emissions (Schindler et al., 1997; of nutrient regeneration rather than as food (Ducklow et al., Flanagan et al., 2006; Estes et al., 2011; Atwood et al., 2013). 1986). On the other hand, the concept of the microbial loop implies the utilisation of bacterial carbon in the food web, Ecological efficiencies and carbon for example by feeding of crustaceans on bacterivorous loss in the food chain ciliates (Azam et al., 1983; Horne & Goldman, 1994; Burns & Gilbert 1993; Balseiro et al., 2001). The debate over the As carbon flows in the ecosystem from primary role of planktonic bacteria is reflected in the “link or sink” producers to top predators along the herbivore controversy (Ducklow et al., 1986; Sherr et al., 1987). food chain, its transformations are accompanied by Bacterivorous nanoflagellates and ciliates are considerable respiratory losses of CO2. The production widespread in freshwater ecosystems, so feeding of and accumulation of biomass at the next trophic level is these protozoa on bacteria must be common (Scavia & affected by the trophic transfer efficiency (TTE), which is Laird, 1987; Chrzanowski & Simek, 1990; Cole, 1999). a product of three variables – consumption efficiency (CE), However, feeding alone is not enough to allow for a assimilation efficiency (AE) and production efficiency (PE) significant flow of energy and carbon between trophic (Townsend et al., 2003). Consumption efficiency is the levels. CE, AE and PE should also be sufficiently high percentage of total productivity available at one trophic to account for significant C-flow. Negative correlations level that is consumed by a trophic level above. Food between abundances of protozoa and bacteria have been

© Freshwater Biological Association 2014 DOI: 10.1608/FRJ-7.1.720 Carbon flow through food webs 9 documented and interpreted as evidence of ciliates’ Because bacteria can use imported and photolysis- regulation of bacterial biomass (Kalinowska, 2004). derived sources of labile DOC, the scale of DOC-based Experimental tests and calculations suggested that the bacterial production is massive (Cole, 1999). However, transfer of carbon along the bacteria–protozoan link this production may not translate into production of may be significant in large lakes (Scavia & Laird, 1987). metazoans (e.g. Prairie, 2008) and may therefore not support production higher in the food web. Many Fate of allochthonous carbon in the freshwater metazoans are not capable of ingesting bacterial ecosystem cells. For instance, copepods, the dominant component of the plankton of many lentic waters, do not usually take up The pathways and rates of carbon flows in ecosystems vary, radioactively-labelled bacterioplankton due to inadequate depending on the types of metabolic gates, intensity of mouthpart morphology (Monakov, 1976), which puts a input and ability of organisms to process and use different limit on their CE. Freshwater Cladocera, such as Daphnia, compounds of C. The relative significance of C received although capable of collecting large bacterioplankton through photosynthesis compared to catchment subsidies (Gophen & Geller, 1984) and assimilating them (Monakov for supporting the food web is an important question, & Sorokin, 1961), do not survive long on pure bacterial which may have management implications. For instance, food supplies (Taipale et al., 2012), indicating a limited if the productivity of fish relies on C from phytoplankton PE. On the other hand, DOC-derived bacterial production as a basal source, the management of fisheries should is known to be used by bacterivorous ciliates and focus on primary production within a water body. If fish heterotrophic nanoflagellates (HNF) (Nakano et al., 1988). are supported by terrestrial subsidies, then management of Both copepods and cladocerans can feed on bacterivorous catchment carbon sources becomes important. ciliates and have high CE and AE (Monakov, 1976; Porter et This question, “how significant is terrestrial C in al., 1979; Sanders et al., 1996; Muylaert et al., 2006). However, freshwater food webs?”, has recently been considered by their PE may still remain low due to the lack in food of Cole (2013a), but we will consider it here in the context polyunsaturated fatty acids (PUFA), which are essential for of various stages in consumption and assimilation metazoan growth, reproduction and productivity (Phillips, of terrestrial C that have the potential to limit its 1984; Müller-Navarra, 1995; Brett & Müller-Navarra, 1997; contribution to the food web (summarised in Table 5). Gulati & DeMott, 1997; Sargent et al., 1999; Sushchik et Total organic C and total DOC in lakes and rivers is al., 2003; Taipale et al., 2014). PUFA are not synthesised often dominated by t-DOC (Wetzel, 2001; Kritzberg, et by bacteria (Phillips, 1984; Napotalino, 1999). As a result, al. 2006a; Prairie, 2008) which is probably what makes the transfer of carbon from the microbial chain (t-DOC – them net heterotrophic (Marcarelli et al., 2011). 13C-tests bacteria – protozoa) to the upper food web (e.g. protozoa suggest that t-DOC can be assimilated by some freshwater – crustaceans – fish) may be limited. It has been shown molluscs (Roditi et al., 2000). This is consistent with the that omega-3 PUFA can regulate carbon transfer and TTE finding that larvae of marine molluscs are able touse from phytoplankton to zooplankton (Müller-Navarra et DOC (Olson & Olson, 1989). If bivalves, such as the zebra al., 2000), and TTE for PUFA significantly exceeds that for mussel Dreissena polymorpha that invaded many European other carbon compounds (Gladyshev et al., 2011). If the and US lakes (Strayer, 1991; Mackie & Schloesser, 1996), lack of PUFA in bacteria limits carbon transfer from t-DOC assimilate t-DOC, then benthivorous fish, which feed to the upper food web, huge transformation of t-DOC on Dreissena (Prejs et al., 1990), may be supported by by bacteria in fresh waters (Cole, 1999) will not translate t-DOC as the basal C-source, creating a significant C-flux into a corresponding increase in the productivity of fish. through the food web. In this case, benthivorous fish The trophic-dynamic approach (Lindeman, 1942) can production may be supported by catchment subsidies. help assess how much of the observed fish productivity

DOI: 10.1608/FRJ-7.1.720 Freshwater Reviews (2014) 7, pp. 1-24 10 Matveev, V. & Robson, B.J.

Table 5. Possible factors limiting the contribution of microbial production to higher foodweb (zooplankton) production, and possible ameliorating factors.

Potential limiting Implication Support Potential counter Support factor t-DOC and t-POC Low microbial Brett at al. (2012) Bacteria can use labile Cole (1999, 2013a) may be refractory on production t-DOC and photolised relevant timescales t-DOC

Many freshwater Low Monakov (1976) Cladocera can ingest bacteria Gophen & Geller metazoans cannot consumption (1984) ingest bacteria efficiency (CE)

Ingested bacteria Low assimilation Brett et al. (2009) Some Cladocera do assimilate Monakov & may not be efficiency (AE) Taipale et al. (2012, 2014) bacterioplankton well. Sorokin (1961) assimilated Assimilation efficiency of Taipale et al. Daphnia grazing on t-POC (2014) is improved if the diet is supplemented by algal sources containing sufficient fatty acids.

Food quality of Low production Ederington et al. (1995) Heterotrophic Zhukova & bacterial C may be efficiency (PE) Sanders et al. (1996) nanoflagellates (HNF) may Kharlamenko inadequate due to synthesise PUFA, thus (1999) lack of PUFA improving the food quality of microbial C

Table 6. Estimated carbon fluxes in north temperate lakes. *Data of Prairie (2008). **Published P/B-estimates: phytoplankton – mean of P/ B=100 yr-1 (Walline et al., 1993) and of P/B=130 yr-1 (Sorokin & Paveljeva, 1972); zooplankton – mean for 7 species (copepods+cladocerans), SE=3.5 (Zaika, 1983); fish – mean of 6 fish species, SE=0.14 (Zaika, 1983). Daily P/B were converted to annual estimates based on the assumption of 8-month vegetation period in the plankton.

Carbon pools C content Mean P/B C flux % phytoplankton (mg C m-2)* (yr-1)** (mg C m-2yr-1) C flux Dissolved organic C 40,000 Phytoplankton 400 115 46000 Zooplankton 150 32 4800 10.4 Fish 200 1.02 204 0.44 Bacteria 1000 212 212000

© Freshwater Biological Association 2014 DOI: 10.1608/FRJ-7.1.720 Carbon flow through food webs 11 can be supported by phytoplankton compared to rivers of both the northern and the southern hemispheres, DOC-derived sources (Brett et al., 2009). Using data on where carbon stable isotope analyses were performed, C-pools for Canadian lakes (Prairie, 2008) and published aquatic algae, and to a lesser extent, phytoplankton and estimates of specific productivities (P/B-coefficients) for macrophytes were identified as the dominant sources phytoplankton, zooplankton and fish, we calculated of carbon for metazoan food webs (Pingram et al., 2012). C-fluxes and their ratios. We assumed a mean TTEof Thus, in many cases allochthonous carbon was found of 10%, based on the analysis of 48 trophic models of aquatic little significance in supporting riverine communities. ecosystems (Pauly & Christinsen, 1995). If the bulk of On the other hand, there are examples (e.g. highly total fish biomass is mostly secondary consumers such as humic lakes, Salonen et al., 1992) where algal production is zooplanktivorous fish (e.g. Lucke et al., 1992; Johnson et low and C-demand of zooplankton could exceed its supply al., 1992), then fish productivity is expected to be 1% of the from phytoplankton. A similar imbalance, implying basal C- flux. If phytoplankton is that only source, then the greater reliance of fish on allochthony was also observed observed ratio of fish to phytoplankton production, fC /Cph, in some US reservoirs (Adams et al., 1983). Overall, should be equal to or less than 1%. If the ratio is significantly the trophic dynamics approach suggests that in lentic higher than 1%, then phytoplankton C is not sufficient ecosystems, food webs may be supported primarily by to explain fish productivity, so a significant contribution autochthonous C-sources, but in humic lakes, where t-DOC from the microbial loop should be inferred. It is assumed import is high, allochthony may also play a significant role. that PUFA-rich nutritious phytoplankton should be A series of studies based on 13C stable isotope analyses, the first preference for consumers over low-quality including experimental whole-lake additions of 13C, DOC-derived food (Brett et al., 2009; Marcarelli et al., 2011). suggested that about a half of zooplankton production The results of the calculations are summarised in in humic lakes could be supported by allochthonous Table 6. They suggest that the observed fish productivity in carbon (Jones et al., 1998; Grey et al., 2001; Pace et al., Canadian lakes can be derived from phytoplankton alone 2004; Carpenter et al., 2005; Cole et al., 2006). Two studies, and no microbial C-flux is needed to account for it. The Cf/Cph making the case even stronger by using three isotopes (C, ratio is 0.44%, which is less than 1%. Our calculations ignored H and N) showed that 20–47% of zooplankton body mass phytobenthos and periphyton, which also contributed could be of terrestrial origin (Cole et al., 2011; Karlsson et to basal C-supply, so the TTE of 0.44% is a conservative al., 2012). However, such results usually come from humic estimate, while the real ratio should be even smaller. lakes (Jones et al., 1998; Grey et al., 2001; Pace et al., 2004; In rivers of ≥ 4th order, metazoan production is Carpenter et al., 2005; Cole et al., 2006, 2011; Karlsson et believed to derive mostly from autochthonous rather than al. 2012), which represent only one special class of lentic allochthonous sources (Thorp & DeLong, 2002). In some waters, known to be very rich in DOC. Furthermore, temperate reservoirs, fish production can be accounted for their conclusions were inconsistent with the fact that most entirely by autochthonous sources (Adams et al., 1983). imported allochthonous material in both lakes (Brett et al., Mass-balance analyses of Canadian lakes suggested that 2009) and rivers (Thorp & Delong, 2002) is recalcitrant. In the bulk of allochthonous DOC utilised by microbial dietary tests with Daphnia, t-POC has been found a very community was very often converted to CO2, rather than poor-quality food. In cultures, Daphnia fed only terrestrial upper food web (Prairie, 2008). In a whole-ecosystem carbon did not grow or reproduce, while Daphnia fed a mix experiment of a US lake, where 13C content of dissolved of t-POC and algal carbon grew and reproduced at a rate inorganic carbon was manipulated, bacteria were shown lower than that of Daphnia fed 100% algal carbon, though to pass little of t-DOC carbon to higher trophic levels, higher than might be expected if they were not using while zooplankton production was mostly derived from t-POC at all but relying only on the algal source. They phytoplankton (Cole et al., 2002). In a review of large concluded that, “even when consuming a diet strongly

DOI: 10.1608/FRJ-7.1.720 Freshwater Reviews (2014) 7, pp. 1-24 12 Matveev, V. & Robson, B.J. dominated by t-POC, Daphnia acquired and selectively There is some indication that significant transfer of retained the majority of their physiologically important carbon from t-DOC to crustacean zooplankton can be fatty acids from the phytoplankton component of their performed by HNF (Salonen & Hammar, 1986; Salonen et diets” (Brett et al., 2009). Positive Daphnia production al., 1992). However, it remains unclear how can animals (growth plus reproduction) could be possible when like Daphnia, which do not grow well without PUFA bacteria constitute <50% of the dietary mixture with (Müller-Navarra, 1995), can reach high productivity while PUFA-containing algae; daphnids did not survive on a consuming HNF, which feed on PUFA-free bacteria. pure bacterial diet (Wenzel et al., 2012; Taipale et al., 2014). The possible answer could lie in the hypothesised Secondly, the 13C studies were based on the assumption ability of HNF to synthesise PUFA. Freshwater HNF that zooplankton grazed exclusively in the upper mixed Paraphysomonas was found to synthesise PUFA de novo layers of lakes (Pace et al., 2004; Carpenter et al., 2005; Cole when feeding on PUFA-free live or decaying Cyanobacteria et al., 2006). However, in a study of 25 temperate lakes, (Park et al., 2003; Bec et al., 2006, 2010). Marine HNF which considered grazing below the epilimnion, terrestrial Bodo sp., which also occurs in lakes and is grazeable for support of zooplankton was found to be trivial (Francis freshwater zooplankton (Jürgens et al., 1996), synthesised et al., 2011). Thirdly, because terrestrial carbon has low PUFA when cultured on PUFA-free media (Zhukova & nutritional quality, zooplankton production derived from Kharlamenko, 1999). However, more evidence is needed it is only conceivable when pools of t-DOC and t-POC are to demonstrate that PUFA synthesis by bacterivorous much larger than algal primary production. This may HNF is widespread. If freshwater HNF are found to often not be the case. Brett et al. (2012) reviewed published convert low-quality bacterial food to PUFA-rich food data and found that 98% of DOC imported to lakes is lost suitable for zooplankton, then the contradiction between to advection and unavailable to zooplankton production. the 13C-studies and the studies emphasising nutritional Advective losses were suggested to be the primary limitations of t-DOC would be partially resolved. fate of t-DOC in lakes with hydraulic retention times Another resolution may lie in the recently (HRT) <3 years (Brett et al., 2012). As rivers have much demonstrated ability of zooplankton to utilise bacterial shorter HRT, it can be expected that t-DOC is even less C from mixtures of phytoplankton rich in PUFA and available for supporting riverine metazoan communities. bacterioplankton. Daphnia have been shown to assimilate In filtered humic lake water, crustacean zooplankton bacterial C with similar efficiency as phytoplankton if were maintained in complete darkness for a long time sufficient essential fatty acids can be obtained froma (Salonen & Hammar, 1986), which implied exclusive high-quality algal source in a mixed diet, though the reliance of zooplankton on non-algal food source. growth rate of Daphnia in these experiments declined On the other hand, the zooplankton did not grow in linearly as a function of C:PUFA in the available food darkness in water from clear-water lakes with low DOC (Taipale et al., 2014). Cole (2013a) reviews and tabulates concentration (Salonen & Hammar, 1986). Under similar estimates of the percent contribution of terrestrial carbon dark conditions without detectable photosynthesis and to the diets of benthic invertebrates and zooplankton high DOC from eutrophic or humic lakes, metazoan from a range of lake studies, finding reported values zooplankton maintained substantial biomass for longer ranging from 0 to 92%. Typically, however, field studies than a year (Daniel et al., 2005). Altogether, this suggests suggest that, even in shallow lakes heavily dominated that t-DOC can support zooplankton production in by terrestrial organic material, t-POC usually accounts humic lakes in agreement with the predictions of the 13C for no more than 50 to 60% of food-web production (e.g. studies (Jones et al. 1998; Grey et al. 2001; Pace et al., 2004, Cole & Solomon, 2012; Wilkinson et al., 2013). Although Carpenter et al., 2005, Cole et al., 2006; Cole et al., 2011). a few higher estimates have been reported, it should

© Freshwater Biological Association 2014 DOI: 10.1608/FRJ-7.1.720 Carbon flow through food webs 13 be remembered that all estimates derived from isotope colonial algae in lakes and reservoirs, phytoplankton that ratios and mixing models are subject to high uncertainty. are not ingested by consumers due to large colony size or Arguments for and against the importance poor nutritional quality (Lampert, 1987) die and sink to the of the microbial loop to zooplankton sediments. Diatoms also sink rapidly. Under eutrophic production is summarised in Table 5. conditions, which often cause these blooms, bottom layers

of water become depleted in dissolved O2 (Wetzel, 2001). Flow rates of carbon in the food The oxygen deficit slows down organic decomposition web rates (Mitsch & Gosselink, 2007), resulting in burial and long-term storage of C. The rate of carbon flow through the ecosystem is Benthic macrophytes in the littoral zone of lakes linked to community structure (Cebrian, 1999). Specific and rivers also contribute to long-term C storage, productivities or productivities per unit biomass through production of refractory plant biomass both (P/B-coefficient) determine the rate of carbon flow. In above and below the sediment surface (Cole et al., 2007). the metabolic theory of ecology, temperature and the Sediment accumulation rates can average about 2 mm size of organisms are the two most important predictors year-1 in temperate lakes (Trolle et al., 2008) and 20 mm yr-1 of P/B-values (Brown et al., 2004). In a steady-state in reservoirs (Mulholland & Elwood, 1982). In lakes the population, specific production reflects the replacement rates are affected by autochthonous primary production of individuals lost to mortality (Brown et al., 2004). In (Dean & Gorham, 1998), lake area (Rowan et al., 1992; Cole, ecological modelling, annual P/B is equated to total 2013a) and exposure of sediments to anoxic conditions mortality observed throughout the year in the population (Sobek et al., 2009, 2011; Cole 2013a). Larger lakes are likely and is often used to estimate the production of a given to have a lower input of terrestrial carbon per unit sediment ecosystem compartment (Christensen et al., 2005). The area (Cole, 2013a) and a higher autochthonous production fraction of PP removed by consumers is correlated with the relative to the total allochthonous input. They thus tend to P/B ratio of the aquatic plant community, probably because have a higher PUFA:C ratio, resulting in greater food-web faster growing communities have greater palatability for assimilation and reduced burial efficiency. Anoxic herbivores (Duarte & Cebrian, 1996). conditions appear to be associated with greater bacterial respiration for a given rate of bacterial production in the Losses of carbon from the presence of allochthonous carbon (Bastviken et al., 2004). ecosystem Globally, lakes accumulate 42 Tg yr-1 of organic C, and reservoirs 160 tTg yr-1. In the long term, sedimentation While C can enter ecosystem metabolism through five turns a natural lake into a wetland, eventually making it metabolic gates, it can leave it through three exits: (1) loss a large storage of trapped C (Mitsch & Gosselink, 2007). of CO2 and methane to the atmosphere; (2) export of DOC The dominant pathways of carbon in any aquatic and POC; and (3) deposition and subsequent burial of POC system depend on the complex interactions between in sediments. Flocculated DOC can also be deposited in carbon availability, macro- and micro-nutrient availability sediments (von Wachenfeldt et al., 2008). Lake sediments and the relative energetic costs associated with taking up are among the largest stores of organic carbon on the carbon and nutrients in various forms. Table 7 summarises continents and endure for longer than millennia (Cole, the implications of interactions between allochthonous and 2013b). While much of the POC in lake and river sediments autochthonous carbon and nutrient inputs for food web comes from terrestrial sources, another cause of POC production and carbon budgets. This may be helpful in deposition in fresh waters is low consumption efficiency, identifying the likely key carbon budget components for CE, in the food web. After blooms of Cyanobacteria or a system in which these have not been directly measured.

DOI: 10.1608/FRJ-7.1.720 Freshwater Reviews (2014) 7, pp. 1-24 14 Matveev, V. & Robson, B.J.

Table 7. Notional fate of carbon in different types of lakes.

Terrestrial inputs Example Implications Primary C sink (relative to lake area) Low C, N and P Clear highland lake (e.g. Low production - inputs Riera et al., 1999) Benthic primary producers dominate Low burial

Low CO2 emissions Low C inputs, Mesotrophic lowland High PE, autochthonous C dominates food Food-web moderate N and P lake (e.g. Goedkoop & web production and Johnson, 1996) Low burial efficiency subsequent export

Low t-DOC and Large lake impacted by High autochthonous production Burial and Food t-POC, high N and P agricultural fertilisers (e.g. Pelagic production dominates web production Yang et al., 2008) Autochthonous C dominates food web except perhaps during blooms of unpalatable or toxic Cyanobacteria Low burial efficiency, but high total burial Moderate t-DOC and Large lake Moderate autochthonous production Food-web t-POC, moderate N Relatively high PE: terrestrial C contributes production and and P to food web production export Low burial efficiency

High t-DOC Small humic lake (Sobek P

High CO2 and CH4 emissions High t-POC, frequent Small, shallow lake or High microbial production, low microbial Burial oxygenation of wetland (e.g. Van der Peijl Respiration: production ratio sediments & Verhoeven, 2000) or Low PE: terrestrial C mostly does not larger lake with a large contribute to food web production catchment area (e.g. Grey High burial efficiency et al., 2001; Karube et al., Potential for high benthic mollusc 2010) production

Moderate CO2 and CH4 emissions High t-POC, Small, deep lake or High microbial production, high microbial Greenhouse gas infrequent reservoir (e.g. Huttenen et respiration emissions oxygenation of al., 2003) Low PE: terrestrial C mostly does not sediments contribute to food web production Low burial efficiency

High CO2 and CH4 emissions

Lakes with different sources and concentrations 1999; Flanagan, et al., 2006) and by primary production of carbon and nutrients can also be expected to have (Trolle et al., 2008). Sedimentation has been suggested differently structured food webs (Reynolds, 2008). to be the factor that, together with nutrients, directly For example, lakes rich in nutrients and supporting controls CO2 flux from fresh waters (Flanagan et al., 2006). substantial pelagic algal production can be expected Freshwater algae and Cyanobacteria are believed to also support abundant pelagic filter-feeders. to be among the major contributors to the formation of fossil fuels, such as oil shales and petroleum source Food webs and carbon rocks (Desborough, 1978; Glikson et al., 1989; Gillaiseau sequestration et al., 1996). For instance, the green planktonic alga Botryococcus seems to be the dominant contributor to Inland waters play important role in regional carbon organic matter in oil shales of US, Europe and Australia budgets and even in the global carbon balance (Cole, 2013a, (Glikson et al., 1989). This suggests that global burial b). Globally, the amount of organic C buried annually in of carbon in lakes through phytoplankton production the sediments of lakes and reservoirs exceeds that in ocean and sedimentation was a massive geological process. sediments by a factor of two (Dean & Gorham, 1998). As the relative contribution of small water bodies to Burial rates of C are highest in small productive lakes and carbon sequestration is potentially high (Downing et al., reservoirs, and the world’s farm ponds alone may bury 2006), we hypothesise that careful management of these more organic C than the oceans (Downing et al., 2008). water bodies through nutrient and fish manipulations Small water bodies dominate the global area covered by may be used to reduce regional carbon emissions. continental waters (Downing et al., 2006). The extent of Odd-numbered food chains seem to suppress this coverage may be sufficient for making the processes freshwater CO2 emissions, while even-numbered food that take place in them globally significant (Downing et chains enhance emissions in both lentic and lotic systems al., 2006). At a regional scale, the role of small lakes may (Schindler et al., 1997; Flanagan et al., 2006; Atwood et be disproportionally greater compared to large lakes. For al., 2013). The number of trophic levels in small water instance, in Finland, small lakes cover only one-third of the bodies can be easily changed by food web management, total national lake area, but bury two-thirds of the total C for instance, through stocking fish with different dietary stored in all lakes of the nation (Kortelainen et al., 2004). requirements. If the ecosystems can be managed towards The P/R ratio increases from <1 in oligotrophic the establishment of an odd number of trophic levels, and conditions to >1 in eutrophic (Table 2). As P/R > 1 implies that if net C-sequestration can be achieved, than CO2 emissions the ecosystem works as a net carbon sink, eutrophication can be reduced. In countries such as Australia, where small, in general and lake fertilisation in particular apparently managed water bodies like farm dams are numerous and lead to carbon sequestration. On the other hand, the fish stocking in them is practiced and coordinated by state effects of food-web manipulation on primary production governments (e.g. Boyd, 2006), considerable progress can be (Carpenter et al., 1985; Carpenter et al., 1987; Carpenter & achieved through simple modification of existing practices Kitchell, 1993), which may imply changes in sedimentation and selection of appropriate fish species for stocking. and storage of C (Håkanson, 1995; Trolle et al., 2008), are In the geological past, atmospheric C was trapped much stronger in small and shallow water bodies than in and buried in lakes through photosynthesis leading large and deep waters (Lammens et al., 1990; McQueen, to the formation of fossil fuels. Present-day industrial 1990; Benndorf, 1995). Alterations of FWS in shallow activities release C from fossil fuels back to the atmosphere, lakes may cause significant shifts in primary production which is believed to cause changes in climate. Through (Scheffer et al., 1993). On the other hand, sedimentation of food-web and nutrient management, the process of carbon C may be affected by lake FWS (Elser et al., 1995; Sarnelle, sequestration and burial by algae and Cyanobacteria can

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Barbara Robson is a Principal Research Scientist in CSIRO Land and Water’s Catchment Biogeochemistry and Aquatic Ecology Research Program where she leads the Aquatic Systems Modelling Team. She has 15 years experience in modelling interactions between hydrodynamics, biogeochemistry and ecology of aquatic ecosystems.