Productivity and carbon transfer in pelagic food webs in response to carbon, nutrients and light

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Productivity and carbon transfer in pelagic food webs

in response to carbon, nutrients and light

Carolyn Faithfull

Department of Ecology and Environmental Science Umeå University

Umeå 2011

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List of Papers

This thesis is a summary of the following papers, which will be referred to by their roman numerals.

I. C.L. Faithfull, A.-K. Bergström, T. Vrede. Effects of nutrients and physical lake characteristics on bacterial and phytoplankton production – a meta-analysis. Submitted manuscript.

II. C. L. Faithfull, M. Huss, T. Vrede and A.-K. Bergström (2011).

Bottom–up carbon subsidies and top–down predation pressure interact to affect aquatic food web structure. Oikos, 120: 311–320.

III. C. L. Faithfull, M. Huss, T. Vrede J. Karlsson and A.-K. Bergström Transfer of bacterial production based on labile carbon to higher trophic levels in an oligotrophic pelagic system. Submitted manuscript.

IV. C.L. Faithfull, A. Wenzel, A.-K. Bergström, T. Vrede. Lower bacterial production and phytoplankton edibility reduces crustacean zooplankton biomass at low light. Manuscript.

Paper II is reproduced with permission from the publisher

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Some of the major problems we face today are human induced changes to the nitrogen (N), phosphorus (P) and carbon (C) cycles. Predicted increases in rainfall and temperature due to climate change, may also increase dissolved organic matter (DOM) inflows to freshwater ecosystems in the boreal zone. N, P, C and light, are essential resources that most often limit phytoplankton (PPr) and bacterial production (BP) in the pelagic zone of lakes. PPr and BP not only constitute the total basal C resource for the pelagic aquatic food web, but also influence ecosystem function and biogeochemical cycles.

In this thesis I studied how N, P, C and light affect the relative and absolute rates of PPr and BP, along a wide latitudinal and trophic gradient using published data, and in two in situ mesocosm experiments in a clear water oligotrophic lake. In the experiments I manipulated bottom-up drivers of production and top-down predation to examine how these factors interact to affect pelagic food web structure and function.

The most important predictors of PPr globally (Paper I) were latitude, TN, and lake shape. Latitude alone explained the most variation in areal (50%) and volumetric (40%) PPr. In terms of nutrients PPr was primarily N-limited and BP was P-limited. Therefore bacteria and phytoplankton were not directly competing for nutrients. BP:PPr was mostly driven by PPr, therefore light, N, temperature and other factors affecting PPr controlled this ratio. PPr was positively correlated with temperature, but not BP, consequently, higher temperatures may reduce BP:PPr and hence the amount of energy mobilised through the microbial food web on a global scale.

In papers II and III interaction effects were found between C-additions and top-down predation by young-of-the-year (YOY) perch. Selective predation by fish on copepods influenced the fate of labile C-addition, as rotifer biomass increased with C-addition, but only when fish were absent. Interaction effects between these top-down and bottom-up drivers were evident in middle of the food web, which is seldom examined in this type of study. Although the energy pathway from bacteria to higher consumers is generally longer than from phytoplankton to higher trophic levels, increased BP still stimulated the biomass of rotifers, calanoid copepods and YOY fish. However, this appeared to be mediated by intermediate bacterial grazers such as flagellates and ciliates.

Light was an important driver of crustacean zooplankton biomass (paper IV), but the light:nutrient hypothesis was inadequate to predict the mechanisms behind the decrease in zooplankton biomass at low light. Instead, it appeared that reduced edibility of the phytoplankton community under low light conditions and reduced BP most strongly affected zooplankton biomass. Thus, the LNH may not apply in oligotrophic lakes where PPr is primarily N-limited, Daphnia is rare or absent and mixotrophic phytoplankton are abundant.

N, P, C and light manipulations have very different effects on different parts of the pelagic food web. They influence the relative rates of PPr and BP, affect phytoplankton community composition, alter the biomass of higher trophic levels and change pathways of energy transfer through the pelagic food web.

This thesis adds valuable information as to how major changes in these resources will affect food web structure and function under different environmental conditions and future climate scenarios.

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Productivity and carbon transfer in pelagic food webs in response to carbon, nutrients and light

Introduction

Why is carbon, nutrients and light important for production in lakes?

One of the environmental problems we face today is the anthropogenic alteration of the global biogeochemical cycles of nitrogen (N), phosphorus (P), and carbon (C), which have increased in magnitude by c. 100%, c. 400%, and c.

13%, respectively, from pre-industrial levels (Falkowski et al. 2000).

Additionally, with future climate change and enhanced air temperatures, inputs of terrestrial dissolved organic matter (DOM) to lakes is predicted to increase in the boreal zone (Tranvik and Jansson 2002; Karlsson et al. 2005; Roulet and Moore 2006). Hence, quantifying the combined effects of climate change and alteration of biogeochemical cycles on DOM, nutrient (N, P, C) concentrations and light availability, and how these changes in turn affect the microbial food web and higher trophic levels in the pelagic zone of lakes, has become a major subject of recent research (Carpenter et al. 2005; Cole et al. 2006; Karlsson et al. 2009). In freshwater ecosystems N, P, and C, along with light availability are essential resources that most often limit phytoplankton (PPr) (N, P, light) and bacterial production (BP) (N, P, C) in the pelagic zone of lakes (Tranvik 1988;

Jones 1992; Elser et al. 2007). These elements are also structural components of phospholipids (P and C), amino acids (N and C), carbohydrates (C), and nucleic acids (C, N, and P), which are required by all organisms for survival and growth (Sterner and Elser 2002). The relative and absolute rates of PPr and BP not only constitute the total basal C resource for the pelagic aquatic food web (Fig. 1), but also influence ecosystem function and biogeochemical cycles (del Giorgio and Peters 1994; Jansson et al. 2007). Hence, it is important to describe and understand what determines the production of bacteria and phytoplankton and their relative proportions; especially with regard to how this affects energy and nutrient transfer to higher trophic levels such as zooplankton and fish.

Like all photosynthetic organisms, light is essential for phytoplankton, and planktonic PPr represents the autotrophic proportion of basal production in the pelagic food web. Historically nutrient limitation of PPr has been considered to be mainly driven by P availability in freshwater ecosystems (Schindler 1977).

However, this can differ along a gradient from oligotrophic to eutrophic lakes (Downing and McCauley 1992), across lake size (mean depth and area) (Kalff 2003), and along a gradient of atmospheric N deposition (Elser et al. 2009). In

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fact, N-limitation of PPr has been recorded in many areas (Downing and McCauley 1992; Bergström and Jansson 2006; Abell et al. 2010). Additionally, physical factors which have previously been found to affect PPr include latitude and temperature (Vrede et al. 1999; Flanagan et al. 2003). PPr tends to decrease with increasing latitude in northern hemisphere lakes (Håkanson and Boulion 2001; Flanagan et al. 2003). This pattern may be controlled by mean annual temperature, variation in solar angle or photosynthetically active radiation (PAR), terrestrial productivity or atmospheric N deposition rates (Campbell and Aarup 1989; Håkanson and Boulion 2001; Bergström and Jansson 2006).

BP represents the heterotrophic portion of pelagic basal production (Jones 1992). It is generally acknowledged that when there is little terrestrial input of C, BP can be regulated by the amount of internally produced C by phytoplankton, as a by-product of photosynthesis (Kirchman 1994). Terrestrial DOM, thus, functions as an external energy and C source for bacteria (Tranvik 1988). Additionally, due to the high affinity of bacteria for P they are good competitors for P compared to phytoplankton (Mindl et al. 2005). However, due to the high cell P content of bacteria they are often P-limited in natural systems (Vadstein 2000), and, hence, produce less C per unit P than phytoplankton. The availability of terrestrial DOM releases bacteria from dependence on phytoplankton as a C and energy source, thus allowing them to outcompete phytoplankton under oligotrophic conditions (Jansson 1998; Vadstein 2000).

Large amounts of C can be lost in bacterial respiration depending on the bioavailability of the C resource and bacterial growth efficiency (McCallister and del Giorgio 2008). It follows that enhanced DOM input to lakes may be accompanied by a reduction in basal energy production, caused by decreased PPr due to competition between bacterioplankton and phytoplankton for limited inorganic nutrients or increased respiration by bacteria (Drakare 2002;

Jansson et al. 2003). Alternatively, DOM may serve as a subsidy for the food web by increasing BP, without affecting PPr, thus supplementing basal energy production and the pool of C available as energy for the pelagic food web (Jansson et al. 2007).

Consequences of changes in bacterial and phytoplankton production for higher trophic levels in pelagic food webs

From a bottom-up perspective, the strength by which external terrestrial C fuels the pelagic food web will depend on the transfer of C via bacteria to higher trophic levels (Fig. 1). This depends upon several factors, i.e., the magnitude of BP (Karlsson et al. 2007), the feeding mode of grazers (Grey et al. 2001;

Persaud et al. 2009), and the number and strength of links in the food chain (Hairston 1993; Karlsson et al. 2004). Thus, increased energy production at the

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base of the food web, either driven by increased PPr or BP on external C- sources, is expected to increase the growth rates or biomass of higher trophic levels (Legendre and Rassoulzadegan 1995; Work et al. 2005; De Laender et al.

2010). In turn, the fraction of bacterial or phytoplankton C that is transferred to cladocerans and copepods appears to be proportional to the relative rates of BP and PPr (i.e. the BP:PPr ratio) (Karlsson et al. 2007). Crustacean zooplankton (i.e. copepods and cladocerans), which are the key link between basal production and fish in the pelagic food web (Fig. 1), differ in their feeding mode and size selectivity of prey.

Figure 1. A simplified pelagic food web model based on our experimental system.

Bacterial production is driven principally by terrestrial DOM, phytoplankton carbon (C) exudates and phosphorus (P). Bacteria are consumed by mixotrophs, ciliates and cladocerans, and bacterial-C can also end up in copepod and fish biomass via copepod grazing on mixotrophs and ciliates. Light and nitrogen (N) are the primary drivers of phytoplankton in this model, and phytoplankton are in turn grazed by cladocerans, copepods and potentially some of the larger ciliate and rotifer taxa. Planktivorous fish (young-of-the-year perch) preferentially graze on copepods but can also consume cladocerans. Grey arrows are elemental fluxes, black arrows indicate predation and arrow thickness indicates coupling strength between the different compartments. Parts of the food web which each paper deals with are shown with grey boxes.

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Since copepods are inefficient grazers on small particles such as bacteria (Zöllner et al. 2003), bacterial C must be transferred through the microbial food web via protozoans, with associated energy losses at each additional trophic level, to reach copepod consumers (Fig 1) (Jansson et al. 2007). In contrast, bacterial C may be more efficiently transferred in food webs dominated by cladocerans (and rotifers) that are able to feed directly on small particles. Thus, we would expect the structure of the zooplankton community to affect how efficiently bacterial C is transferred through the food web, as fewer trophic levels would result in fewer opportunities for respiratory C losses (Pace and Cole 2000; Sommer and Sommer 2006). Increased BP may also affect the structure of the zooplankton community, by increasing the biomass of bacterial grazers, and increased BP:PPr tends to increase the average number of trophic levels in the food web, due to small bacterial grazing protists becoming more abundant (Berglund et al. 2007).

PPr is assumed to be more directly available for higher trophic levels than BP, as many phytoplankton taxa fall within an edible size range for both cladocerans and copepods (Cyr and Curtis 1999). Phytoplankton are also considered to be a high quality food source compared to bacteria (with the notable exception of cyanobacteria), as they contain essential fatty-acids and sterols required by zooplankton, that bacterioplankton lack (Brett and Müller-Navarra 1997).

However, the quantity as well as the quality of PPr may change with manipulations of light, nutrients and C. Light availability may not only affect the magnitude of PPr, but also the C:nutrient ratio of phytoplankton cells, and therefore the quality of phytoplankton as food for higher consumers. When light availability is high, but nutrients are limiting, phytoplankton tend to have high C:nutrient ratios, as the excess available C can be stored within phytoplankton cells (Elser et al. 2003). Thus, phytoplankton are said to be stoichiometrically flexible (flexible C:nutrient ratios). However, phytoplankton taxa can differ in their stoichiometric flexibility, and some taxa may release excess C to help maintain a relatively fixed stoichiometry (Obernosterer and Herndl 1995). The stoichiometric flexibility of phytoplankton can lead to a mismatch between producer supply and grazer demand for nutrients, as grazers such as meta- zooplankton have relatively fixed stoichiometric ratios compared to phytoplankton (Hessen 1992). As a consequence of this, although phytoplankton biomass may be high under high light conditions, the quality of this biomass as a food source for higher trophic levels may be low due to high C:nutrient ratios (Sterner et al. 1998). This can result in low consumer growth rates and respiration of excess C (Hessen and Anderson 2008).

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Subsequently, changes in the absolute rates of PPr, BP, BP:PPr, and the stoichiometry of this production may affect higher trophic levels, such as flagellates, ciliates, rotifers, crustacean zooplankton and even planktivorous young-of-the-year (YOY) fish in the pelagic food web. However, these bottom- up effects on higher trophic levels may also be mediated by top-down affects by consumers. For instance, selective predation by YOY perch (Perca fluviatilis) on copepods may change C-transfer efficiency in the food web (Bertolo et al. 2000), due to the ability of copepods to selectively graze on high quality prey. DOM inflows and light intensity may also alter whole lake fish production, with the pelagic food web becoming more important in DOM rich lakes (Karlsson et al.

2009). Little work has been conducted on the effects of BP and the BP:PPr ratio on fish production, although studies from marine systems suggest that BP may be an important C source for planktivorous fish depending on season (De Laender et al. 2010).

Objectives of the thesis

This thesis consists of four papers (I–IV below) which focus on the effects of N, P, C (glucose), DOM, and light intensity on the relative and absolute rates of PPr and BP, and the subsequent consequences for higher trophic levels in pelagic freshwater ecosystems. The aims of the four papers are as follows:

I To investigate how the relative and absolute rates of BP and PPr are influenced by elemental (N, P and C) and physical (lake morphology, latitude and temperature) factors in lakes along a wide latitudinal and trophic gradient.

II To test how the combined effects of a bottom-up C subsidy (glucose) and top-down predation by YOY perch affect PPr and BP and the pelagic community composition in an oligotrophic clear water lake.

III To assess the relative influence of phytoplankton C and external C sources on higher trophic levels.

IV To examine how N, P, C (glucose) and light manipulations affect the quantity and nutritional quality of basal production, and in turn how this influences crustacean zooplankton biomass in an oligotrophic clear water lake.

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Methods

Data was collected from published studies for a meta-analysis (Paper I). Two sets of mesocosm experiments using different food web configurations and elemental manipulations were conducted in an oligotrophic clear water lake in Northern Sweden (Papers II, III, IV).

Meta-analysis

To obtain an overview of how the absolute and relative rates of PPr and BP are affected by light, nutrients and C along a latitudinal and trophic gradient, published data was collected from field studies for 300 lake years and 249 independent experimental studies (Fig. 2).

Figure 2. World map showing locations of experimental studies and field studies obtained from literature sources or by pers. comm. Reproduced from paper I.

In order to deal with the problem of multicollinearity for both our explanatory and response variables, both multiple regression and hierarchical partitioning methods were used. Hierarchical variance partitioning jointly considers all possible models in a multiple regression data set, which allows the identification of variables that are independently correlated with a response variable, even when multicollinearity is present (Murray and Conner 2009). The field data was analysed to determine how the explanatory variables (N, P, DOM, latitude, temperature, lake morphology) influenced areal and volumetric BP, PPr and BP:PPr ratios. Areal measurements take into account lake euphotic depth and morphometry, thus, producing a water column average, whereas volumetric measurements were taken in the epilimnion, but standardised for euphotic depth/lake depth. For the experimental studies Hedge’s g (Lipsey and Wilson

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2001) was used as the effect size metric to compare and combine the treatment effects. Positive effect sizes indicated a positive response to the treatment.

Mesocosm experiments

Mesocosm experiments are a half-way house between a controlled laboratory environment and a natural ecosystem. The advantages of using mesocosms are that they are in situ and should therefore be subject to the same conditions as the lake, but can be manipulated with nutrient or C additions and shaded to reduce incidence light (Petersen and Englund 2005). Treatments applied to mesocosms can also be replicated to increase statistical power, which tends to be costly and difficult with natural ecosystems (Carpenter 1989). Mesocosms have been shown to represent ecological processes with reasonable accuracy enabling these findings to be scaled up to natural systems (Spivak et al. 2011), and in our own study we found the size of the experimental unit did not systematically affect the experimental outcomes (Paper I). However, there are also disadvantages to using mesocosms. Mesocosms have walls, enabling periphyton growth, which can potentially change the structure of basal production in the system (Schindler 1998; Petersen et al. 1999), and in our case they were closed at the bottom, preventing any sediment water interactions. For our purpose, however, we required a system that could be replicated, was large enough to include YOY fish, but to exclude predation on the fish, and contained a natural pelagic planktonic community. In papers II and III we used large 18 m³ mesocosms, and crossed three levels of glucose addition and three levels of YOY perch density in a full factorial design. This gave us 9 treatments, which were applied in triplicate to the mesocosms. For the experiment in paper IV we used smaller mesocosms (2.8 m³), and crossed glucose, inorganic N and inorganic P addition with shading in a full factorial design to give 16 treatments, replicated twice to give 32 mesocosms.

The first experiment in the large mesocosms ran for 45 d in summer 2007 and was sampled before treatment addition and three times over the course of the experiment. A natural pelagic community including all components of the food web up to zooplankton was present at the start of the experiment. YOY perch were added after the first sampling date and glucose was added twice a week for the duration of the experiment. The second experiment using smaller mesocosms ran for 22 d in summer 2009 and was sampled three times: before treatment addition, after 7 d incubation with N, P, glucose and light manipulations, then zooplankton were added at natural lake densities, and the mesocosms were sampled again after a further 14 d incubation.

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In both experiments we had an ambitious sampling regime. In situ we measured temperature, oxygen concentration and light intensity. Chemical parameters such as dissolved inorganic, organic and particulate C, total, dissolved and particulate N and P, and chlorophyll-a concentrations were measured. Sestonic particulate N, P and C were size fractionated (>100 µm, 100-30 µm, 30-10 µm, 10-1.6 µm and <1.6 µm) for paper IV. Biomass and abundance of bacteria, phytoplankton, flagellates, ciliates, rotifers and zooplankton taxa were obtained using the Utermohl settling technique and standard counting methods. BP and PPr were measured using the leucine (protein production in bacteria) and C¹⁴ (rate of C formation due to photosynthesis) isotope methods, respectively.

Stable isotope samples for dissolved inorganic C, particulate organic C, YOY perch biomass, Bosmina sp., Holopedium gibberum and Eudiaptomus gracilis were collected and measured for paper III.

The use of glucose as a labile carbon source

Natural DOM contains not only C, but also N, P and coloured substances that reduce light availability for photosynthesis (Jansson 1998; Klug 2005). In previous studies with natural DOM additions, it has been impossible to separate the effects of nutrients, C and light on BP and PPr (Klug 2005; Berglund et al.

2007). In order to tease apart the mechanisms of terrestrial DOM effects, we chose to focus on the effects of C subsidies alone on the pelagic food web for papers II and III, and to manipulate N, P, C and light in a full-factorial design for paper IV. Consequently, we used glucose as an alternative C source to DOM, as it is readily bioavailable for bacterioplankton but has a negligible effect on light and nutrient conditions. Obviously glucose is not a direct substitute for DOM, as it is highly labile and terrestrial DOM varies greatly in bioavailability, depending on age and source (Tranvik 1988; Berggren et al. 2009). However, labile C is not an ecologically unimportant C source, as it is continually renewed in the water column due to inflows of low molecular weight allochthonous C (originating from terrestrial sources) (Berggren et al. 2010b), or in lake processes, such as photo-chemical degradation of allochthonous C (Jones 1992;

Moran and Zepp 1997), phytoplankton extracellular C release (Sundh and Bell 1992) or enzymatic degradation of complex DOM molecules (Docherty et al.

2006).

Stable isotopes

In paper III we used the distinct stable isotopic signature of glucose compared to natural C sources to determine the fraction of bacterial C transferred to cladocerans, copepods and YOY perch. Measuring stable isotopes of C and N has become a popular method to trace energy flows through food webs, and glucose is δ¹³C enriched (δ¹³C = -11.6‰) compared to natural organic C sources (δ¹³C =-

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27 to -43‰) found in Northern Swedish lakes (Karlsson et al. 2003). By comparing the δ¹³C signals of zooplankton taxa and YOY perch in treatments with and without glucose addition we could calculate the amount of bodily C in these taxa originating from glucose. Because glucose was undetectable in the mesocosms after addition and BP was stimulated by glucose addition, we assumed that all glucose ending up in higher trophic levels was transferred through bacteria. We used δ¹⁵N and a trophic fractionation constant of 3.4‰

(Post 2002) to calculate the trophic levels of cladocerans, copepods and YOY fish.

Major results and Discussion

Factors affecting the absolute rates of phytoplankton and bacterial production

The most important predictors of areal and volumetric PPr globally (Paper I) were latitude, TN, and lake shape. Latitude alone explained the most variation in areal (50%) and volumetric (40%) PPr. Much of this variation was accounted for by temperature, as latitude became important when we excluded temperature from the models. PPr can vary with many factors that are correlated with latitude i.e., mean annual temperature, variation in solar angle or photosynthetically active radiation (PAR), terrestrial productivity or atmospheric N deposition rates (Campbell and Aarup 1989; Håkanson and Boulion 2001; Bergström and Jansson 2006). The combination of these factors into the single variable latitude probably gave latitude such a high predictive power for PPr. TN was also an important predictor of areal (15%) and volumetric PPr (29%). Research has shown that in areas with low atmospheric N deposition (such as at high latitudes) N strongly limits PPr, especially in unproductive lakes (Vitousek and Howarth 1991; Bergström and Jansson 2006;

Elser et al. 2009). In the experimental meta-analysis and in paper IV we also found that PPr was most strongly N-limited. Positive synergistic effects of combined N- and P-addition on PPr were evident in the nutrient enrichment experiments, since single enrichment of either N or P likely induces limitation by the other element (Elser et al. 2007; Bergström et al. 2008).

DOM concentrations can negatively influence PPr (Paper I) (Jansson et al.

2003). However this varied greatly, as the experimental meta-analysis showed a positive effect of DOM on volumetric PPr, and volumetric PPr in the field data set was unaffected by DOM. One explanation for this is that DOM reduced light levels for photosynthesis in lakes (Jones 1992), but not in the experiments.

Generally all the experiments used in the meta-analysis kept light intensities

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constant, but the experiments that had the lowest PPr and highest BP:PPr reduced light levels (Berglund et al. 2007). In paper IV we reduced the average incidence light at 1 m depth in the mesocosms from 91.7 to 58.0 µmol m^-2 s^-1, but this had no effect on the magnitude of PPr. Instead the phytoplankton community shifted towards golden algae (Dinobryon sp.) and dinoflagellates (gymnoids), which have pigmentation better adapted to low light conditions (Johnsen and Sakshaug 1996), the ability to migrate within the water column to reach optimal light intensities (Clegg et al. 2003) and can even ingest bacteria as an alternative energy source, thus, outcompeting obligate phototrophs at low light intensities (Bird and Kalff 1987; Hitchman and Jones 2000; Floder et al.

2006).

The main determinant of volumetric BP and areal BP across the field data set, the meta-analysis of experimental studies and in paper IV was P. This reflects earlier studies that have shown bacteria are most often P-limited (Vrede et al.

1999; Vadstein 2000). DOM was positively correlated with BP in the field and experimental studies, and with both areal and volumetric BP, as has been well documented in the literature for temperate lakes (Tranvik 1988; Jones 1992). In papers I, II and III, glucose addition increased BP, although this increase was not significant in paper IV. N-addition had no effect on BP. Volumetric rates of BP were positively correlated with PPr along a wide trophic gradient (Paper I), and bacteria also appeared to depend on phytoplankton as a C source in paper IV. In paper IV BP was lower at low light levels, which could have been due to a decrease in autochthonous C release by phytoplankton, which is an important C substrate for bacterial growth (Baines and Pace 1991).

Factors affecting the relative rates of phytoplankton and bacterial production

In the meta-analysis (Paper I) glucose addition did not negatively affect PPr as we might expect if bacteria and phytoplankton are competing for nutrients and bacteria are no longer dependant on phytoplankton as a C source. This coupled with the fact that PPr did not change with glucose addition in papers II or IV (Fig. 3), suggests that we cannot generalize that bacteria outcompete phytoplankton for nutrients when there is an external C source. Indeed in papers I and IV BP and PPr were P and N limited respectively and therefore do not appear to be competing for the same limiting nutrient (Fig. 3). Alternatively, it appears that other properties of the system, such as trophic state (Jones 1992), nutrient stoichiometry (Danger et al. 2007), light limitation (Jones 1992) and the proportions of autotrophic and mixotrophic phytoplankton biomass (Bergström et al. 2003) may regulate the interactions between PPr and BP.

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Although positive relationships between BP and temperature have been found in the laboratory and across natural systems (White et al. 1991), this relationship was not evident in the experimental studies or the field data set (Paper I). Other studies have found that BP still occurs at very low temperatures (<10–4ºC), and temperature only tends to limit BP when other factors such as nutrient and C concentrations are not limiting (Laybourn-Parry et al. 2004;

Berggren et al. 2010a).

Figure 3. Changes in elemental additions (± 1SE) of carbon (C), nitrogen (N), phosphorus (P) and shading (S) combined (n=16), for a) phytoplankton production (PPr), b) bacterial production (BP) and c) the BP:PPr ratio. Initial measurements and after 6 and 22 d incubation are shown.

Stars indicate treatment additions that were significantly different (p < 0.05) from mesocosms without that treatment addition according to the ANOVA results. Modified from paper IV.

Increased bacterial respiration relative to BP has been found when manipulating temperature in the laboratory, however, bacterial communities in situ tend to be adapted to in situ conditions, and this adaptation may occur within days (Adams et al. 2010; Berggren et al. 2010a). Consequently, it seems unlikely that BP will increase relative to PPr during climate warming, due to rapid adaptation of the bacterial community. Given the positive relationship with PPr and temperature and the negative correlation with BP:PPr and temperature found in paper I, one can predict that when considering lakes along a wide trophic gradient, temperature increases due to climate change could

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decrease the importance of energy mobilized through the microbial food web.

However, this finding probably only applies as a general pattern over a wide trophic and latitudinal gradient, as for example, studies from the Baltic sea have predicted that BP and therefore BP:PPr will increase with increased temperature (Müren et al. 2005; Hoppe et al. 2008).

BP:PPr appears to be most strongly regulated by changes in PPr rather than changes in BP (Paper I) (c.f. del Giorgio and Peters 1994), therefore at high latitudes and low TN:TP ratios BP makes up a larger part of the available basal production. This has been shown for oligotrophic lakes in low atmospheric N- deposition areas in Northern Sweden (Karlsson et al. 2002; Bergström et al.

2003). Consequently, the microbial food web may be more important for energy transfer to higher trophic levels at low TN:TP ratios and at high latitudes.

Additionally, we found that in experimental studies manipulating the BP:PPr ratio, may be best done by changing factors that effect PPr, such as N concentration, or light intensity (Papers I, IV).

How do phytoplankton affect higher trophic levels?

It is generally acknowledged that phytoplankton are high quality food for zooplankton, and the ‘bread and butter’ of a zooplankton diet. However, many phytoplankton taxa can become poor quality food if they are grown under high light and low nutrient conditions according to the light:nutrient hypothesis (LNH) (Sterner and Elser 2002; Elser et al. 2003). In this case zooplankton growth can become nutrient limited, even though the biomass of phytoplankton may be more than enough to meet their energy needs. In lower light conditions phytoplankton may have lower C:nutrient ratios, but lower growth rates, therefore zooplankton would tend to be energy limited (Sterner et al. 1997;

Sterner and Elser 2002). We tested the LNH in paper IV by manipulating light levels and nutrient concentrations. We found that although seston C:P and C:N (10–30 µm) ratios decreased somewhat in the lower light treatments, this had no affect on zooplankton biomass. Indeed, edible C:P seston (0.7–30 µm) ratios were already low before light manipulation in this experiment, and did not change significantly with light manipulation as predicted by the LNH, possibly due to the abundance of mixotrophs in the phytoplankton community (Katechakis et al. 2005).

In fact zooplankton biomass was much lower in the shaded treatments, which we would expect to be an effect of lowered PPr. However, PPr did not vary with light. Instead, at low light levels the phytoplankton community shifted towards species that are adapted to low light conditions, such as Dinobryon sp.

(Chrysophytes) and gymnoids (Dinoflagellates). Therefore, one of the

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explanations we offer to explain this pattern is that the change in phytoplankton species composition changed the edibility of the phytoplankton community.

Dinobryon sp. forms large branching colonies which may be an induced defense against zooplankton grazing (Hessen and van Donk 1993), and the biomass of gymnoids was negatively correlated with all zooplankton taxa biomasses (except Bosmina). Some mixotrophs and other dinoflagellates have been found to be toxic (Kubanek et al. 2007), or to employ behavioral defenses against zooplankton grazing (Selander et al. 2011), thus, reducing energy transfer to zooplankton when they are abundant (Katechakis et al. 2005). However, this has not been documented so far for gymnoids in oligotrophic lakes. Therefore, although food quality in terms of C:nutrient ratios appeared to be unimportant for zooplankton in this experiment, phytoplankton community composition might be an important food quality variable for zooplankton (Paper IV).

Another possible explanation for lower zooplankton biomass in shaded treatments is reduced BP, which is discussed below.

How does increased bacterial production affect higher trophic levels?

Changes in food web structure and function with glucose-C addition at first seemed few and insignificant (Papers II, III, IV). Flagellate, ciliate, and most crustacean zooplankton taxa biomasses were not affected by glucose addition.

This was hypothesised to be due to a large proportion of the glucose C being respired by bacteria when C:nutrient ratios were high (Paper II) and bacterial growth efficiency was low (Jansson et al. 2006). However, when fish were absent, rotifer and calanoid copepod biomass increased with glucose addition (Papers II, III). There was no direct relationship between rotifer or calanoid biomass and BP or PPr. According to the stable isotope results in paper III, cladocerans (Bosmina sp. and H. gibberum) consumed the most glucose (and therefore BP), however, cladoceran biomass did not increase with increased BP.

Bosmina sp. and H. gibberum can incorporate bacterial C either directly (Hessen 1985; Vaqué and Pace 1992) or indirectly through flagellate or small ciliate grazing (DeMott and Kerfoot 1982; Persson 1985).

Calanoid copepod biomass increased with glucose addition (Paper III), even though copepods cannot graze on small particles such as bacteria (Hansen et al.

1994; Burns and Schallenberg 1996). However, the enriched δ¹³C and δ¹⁵N signals of calanoid copepods and YOY perch suggest that bacterial consumers (i.e. flagellates and ciliates) were contributing to a proportion of their diet, thus, acting as a conduit for nutrients and energy to higher trophic levels (Fig. 4).

Indeed, although calanoid copepod biomass was not correlated with an increased incorporation of glucose C or BP, it was positively correlated with the

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biomass of large ciliates (such as Strombilidium sp.). Thus, in glucose treatments copepods may have been stimulated by increased availability of bacterivorous ciliates, as ciliates may perform trophic upgrading i.e. de novo synthesis of PUFA or preferentially retain rare nutrients (Klein Breteler et al.

1999; Bec and Desvilettes 2009).

Figure 4. δ¹³C and δ¹⁵N concentrations (mean ± 1 SE, n = 3 per treatment) for crustacean zooplankton taxa and young-of-the- year (YOY) perch over three levels of glucose addition, no addition (open symbols), low (420 µg glucose-C L^-1) addition (grey symbols) and high (2100 µg C L^-1) addition (black symbols). Less negative δ¹³C values represent more glucose incorporated (through bacterial production), and higher δ¹⁵N indicates higher trophic position. Reproduced from paper III.

In paper IV we also found evidence that increased BP had a positive effect on crustacean zooplankton biomass. Zooplankton biomass and BP were lower in shaded treatments. All zooplankton taxa (except for calanoid copepods) were also positively correlated with BP. Although bacteria have high concentrations of P and therefore zooplankton may offset P-limitation by bacterial grazing in some taxa, this did not appear to be the case, as edible C:P seston ratios were lower than C:P ratios previously reported that limit zooplankton growth (Sterner and Elser 2002; Katechakis et al. 2005). Consequently, trophic upgrading by intermediate trophic levels may also have been an important mechanism for BP transfer to higher trophic levels in this experiment (Bec and Desvilettes 2009).

The importance of the intermediate step from bacteria to zooplankton

Bacteria do not contain polyunsaturated long chain fatty acids (PUFA) or sterols that are essential to animals (Brett and Müller-Navarra 1997; Martin-Creuzburg et al. 2005). Since a diet poor in PUFA results in slow growth and reproduction of crustacean zooplankton (Brett et al. 2009), the growth of cladocerans in paper III may at least have been partially determined by the availability of PUFA and not only by the total amount of C available. Copepods may have been stimulated by an increased availability of bacterivorous ciliates, as ciliates may

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perform trophic upgrading (Klein Breteler et al. 1999). However, although cladocerans can also consume bacterivorous flagellates and small ciliates, they do not seem to benefit from bacterial based food to the same extent as copepods in our experiments. This could be because the proportion of bacterial grazing protists consumed by Bosmina sp. and H. gibberum were not sufficient to improve the quality of the bacterial resource through trophic upgrading.

Bosmina sp. and H. gibberum are generally considered to be unselective grazers with regard to food quality (Cyr and Curtis 1999; Hambright et al. 2007) and therefore unlikely to selectively graze on high quality protists.

In contrast calanoid copepods are selective grazers and can discriminate between poor and high quality food (Cowles et al. 1988; Burns and Schallenberg 2001). Alternatively, the bacterial grazing protists consumed by Bosmina sp.

and H. gibberum may not be as efficient trophic upgraders as the protists consumed by calanoid copepods, as different species of protists differ in their abilities to synthesise fatty acids (Klein Breteler et al. 1999; Bec et al. 2010).

Although the microbial pathway can possibly off-set biochemical limitation of zooplankton growth, we suggest that this off-set may benefit different zooplankton taxa depending on the abilities of their prey to improve food quality and the ability of the zooplankton taxa to select prey. All zooplankton taxa in paper IV appeared to benefit from increased BP, where nutrients were also added in addition to glucose C to stimulate bottom-up production (Karlsson et al. 2007). But this was not the case in papers II and III, where glucose was added alone. Increased bacterial respiration due to decreased bacterial growth efficiency during acute nutrient limitation (P) may limit the amount of bacterial C that is transferred to higher trophic levels in papers II and III (Jansson et al. 2006).

Interaction effects of YOY perch grazing and carbon (glucose) on the pelagic food web

It has been argued previously that top-down and bottom-up forces (such as fish grazing and labile-C addition, respectively) often have strong direct effects that can become weaker with distance from the origin (McQueen et al. 1986; Brett and Goldman 1997), especially in natural planktonic communities where distinct trophic levels are difficult to define and omnivory is abundant (Persson 1999). Thus, in an experimental system where both top-down and bottom-up factors are manipulated simultaneously, one could expect interaction effects to become evident in the middle of the food web. This is exactly what was found in paper II, as rotifers were the only taxa to exhibit a statistically significant interaction between treatments, i.e., rotifer biomass increased with glucose concentration, but only when fish were absent. Rotifers are located in the

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middle of the food web, with crustacean zooplankton as potential predators and/or competitors, and ciliates, flagellates, phytoplankton and bacterioplankton as potential prey. However, in published studies interaction effects are rare between top-down and bottom-up drivers (Brett and Goldman 1997; Gruner et al. 2008), but this may be an experimental artefact. Most studies measure the response of the basal trophic level (bacteria and phytoplankton) and the upper trophic levels (crustacean zooplankton and fish) to bottom–up and top–down drivers without measuring the responses of the trophic levels between these two extremes (but see Pace et al. 1998).

The effects of carbon (glucose) addition and increased bacterial production on young-of-the-year fish biomass

BP differently affected YOY perch depending on fish stocking density. BP was positively correlated with YOY perch survival and population growth rates at high fish density, but negatively correlated with individual fish growth (Paper III). This effect of bacteria appears to be an indirect bottom-up effect mediated via the microbial food web, resulting in increased prey quality, as calanoid copepods increased with glucose addition and are a favored prey of YOY perch (Huss et al. 2007). Given density-dependent growth, increased fish survival can in turn explain the lower individual growth rates observed with increasing BP at high fish density, i.e., YOY perch were more resource limited when survival rates were high (Persson et al. 2000). The availability of the favored prey (i.e.

calanoid copepods) appears to be the most important determinant of YOY perch growth rate. However, given that BP only influenced fish survival and population growth at high densities, it appears that the ‘quality effect’ of resources only appears once preferred resources are limited.

Conclusions

Paper I shows that the rates of BP and PPr are often determined by different drivers (i.e. BP by C and P and PPr by N and latitude), and this was consistent across field and experimental studies. However, the ratio of BP:PPr is mostly driven by changes in PPr, and is difficult to manipulate in experiments, as volumetric BP is also positively correlated with PPr. PPr, but not BP was positively correlated with temperature. Therefore increased temperatures and N availability due to climate change could lead to higher PPr and lower BP:PPr, potentially decreasing the importance of energy mobilized through the microbial food web on a global scale. Few studies were available from Africa, Asia and the tropics. Tropical systems may be particularly important, as the few

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studies conducted suggest that resource limitation paradigms from northern temperate lakes may not apply (Farjalla et al. 2009).

In paper II increased BP and top-down predation by YOY fish interacted to affect the biomass of rotifers, which are located in the middle of the food web.

This study illustrates that top-down and bottom-up drivers may have interacting effects that become evident in the middle of the food web, which are often missed in studies where only changes in basal production and meta- zooplankton biomasses are considered.

Although increases in BP due to labile-C (glucose) addition (Paper III) did not appear to directly affect crustacean zooplankton production, increased BP may increase the growth rates or abundances of bacterial consuming protists, which have the potential to transform bacterial C into a better quality food resource for zooplankton. Consequently, increases in BP may fuel higher trophic levels when intermediate grazers are present and are consumed by crustacean zooplankton.

Higher BP was associated with increased survival and population growth of YOY perch when stocked at high densities, which suggested that BP had a density dependant effect on fish growth. The role of ‘trophic upgraders’ in transferring bacterial C to higher trophic levels may be important and requires further study to determine the effects of environmental changes on the mechanisms and ecological role of these taxa.

In Paper IV reduced light intensity decreased the biomass of crustacean zooplankton. It was not possible to predict the mechanisms behind this result using theory derived from the LNH. Instead changes in the rate of BP and the edibility of the phytoplankton community composition at low light intensities appeared to affect zooplankton biomass in this experiment. Thus, although the LNH may be useful for hypothesis testing, it may be inadequate in predicting the mechanisms behind changes in crustacean zooplankton biomass with changes in light and nutrient availability in oligotrophic lakes, where PPr is primarily N-limited, Daphnia is rare or absent and mixotrophic phytoplankton are abundant. Instead, the mechanisms behind reduced edibility of the phytoplankton community under low light conditions and the importance of bacteria as an energy source for crustacean zooplankton requires further investigation.

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Acknowledgements

Many thanks to Ann-Kristin Bergström and Tobias Vrede for comments on this thesis summary. The research in this thesis was conducted as part of the strong research environment Lake Ecosystem Response to Environmental Change (LEREC) and was supported by grants from the Wallenberg foundation, the Göran Gustafsson foundation, the Kempe foundation and the Swedish Research Council for Environmental and Spatial Planning (FORMAS).

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Productivity and carbon transfer in pelagic food webs in response to carbon, nutrients and light

Productivity and carbon transfer in pelagic food webs

in response to carbon, nutrients and light

Carolyn Faithfull

Table of Contents

Productivity and carbon transfer in pelagic food webs in response to carbon, nutrients and light