Effects of temperature and terrestrial carbon on primary production in lake ecosystems

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Effects of temperature and terrestrial carbon on primary production in lake ecosystems

Mohammed Abdulridha Hamdan

Department of Ecology and Environmental Science

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This work is protected by the Swedish Copyright Legislation (Act 1960:729) Dissertation for PhD

ISBN: 978-91-7855-534-5

ISBN for the digital version: 978-91-7855-535-2 Cover design: Mohammed Hamdan

Electronic version available at: http://umu.diva-portal.org/

Printed by: KBC service center, Umeå university Umeå, Sweden 2021

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I dedicate this work to

My family,

My father, mother, brothers, and sister,

My wife and daughters

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List of chapters

This thesis is a summary of the following four chapters:

I. Hamdan, M., P. Byström, E.R. Hotchkiss, M.J. Al-Haidarey, J. Ask, J. Karlsson. 2018. Carbon dioxide stimulates lake primary production. Scientific reports, 8: 10878, DOI:10.1038/s41598-018- 29166-3

II. Hamdan, M., J. Karlsson, P. Byström, M.J. Al-Haidarey, J.

Ask. Carbon dioxide limitation of benthic primary production in boreal lakes. Submitted manuscript.

III. Hamdan, M., P. Byström, E.R. Hotchkiss, M.J. Al-Haidarey, J.

Karlsson. 2021. An experimental test of climate change effects in Northern lakes: increasing allochthonous organic matter and warming alters autumn primary production. Freshwater biology, 66(5): 815-825. DOI: 10.1111/fwb.13679

IV. Hamdan, M., J. Karlsson., E.R. Hotchkiss, P. Byström. Warming strengthens trophic cascades and top-down control of lake primary production. Manuscript.

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Author abbreviations Mohammed Hamdan (MH) Jan Karlsson (JK)

Pär Byström (PB) Erin R. Hotchkiss (EH)

Mohammed J. Al-Haidarey (MJA) Jenny Ask (JA)

Author contributions Chapter I

MH, JK and PB designed the study with contribution from JA. MH and MJA performed the field and lab work. EH wrote the metabolism codes. MH analysed the data with contribution from EH and PB. MH wrote the manuscript and all co- authors revised the manuscript.

Chapter II

All authors designed the experiment. The field and lab work were performed by MH and MJA. Benthic metabolism was estimated by MH. The data were analysed statistically by MH with help from PB and JA. MH wrote the paper and all authors revised the manuscript.

Chapter III

JK and PB designed the experiment. The field and lab work were performed by MH and MJA. The metabolism codes were written by EH. Primary production was estimated by MH. The data were analysed statistically by MH with help from PB. MH wrote the paper and all authors revised the manuscript.

Chapter IV

JK and PB designed the experiment. The field and lab work were performed by MH and PB. EH wrote the metabolism codes. Primary production was estimated by MH. The data were analysed statistically by MH. MH wrote the paper and all authors revised the manuscript

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Abbreviations

C Carbon

CO2 Carbon dioxide CO3-2 Carbonate

cDOM Coloured dissolved organic matter Chl a Chlorophyll a

DIC Dissolved inorganic carbon DO Dissolved oxygen

DOC Dissolved organic carbon ER Ecosystem respiration

EXEF Umeå University Experimental Ecosystem Facility GPP Gross primary production

HCO3- Bicarbonate

Iz Light intensity at depth z kd Vertical attenuation coefficient Ki Gas exchange velocity for oxygen K600

Ki standardized to a Schmidt number of 600 derived from wind speed

NaHCO3 Sodium bicarbonate NEP Net ecosystem production

NH4+ Ammonium

NO3− Nitrate

PAR Light intensity [photosynthetic active radiation]

pCO2 Partial pressure of CO2

Pmax Maximum photosynthesis at light saturation PO43− Phosphate

TN Total nitrogen TP Total phosphorous zmix Mean mixing depth

 Initial photosynthetic rate

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Abstract

Climate warming is predicted to affect northern lake food webs in two ways: (1) directly via changes in water temperature and ice conditions, and (2) indirectly via changes in catchment characteristics and processes that influence input of allochthonous coloured dissolved organic matter (cDOM) and nutrients. Input of cDOM increases carbon dioxide (CO2) availability, causes brownification and reduced light conditions, and may increase nutrient availability especially for pelagic primary producers. Increased water temperature and light penetration and longer ice-free periods affect metabolic rates. These changes are expected to influence gross primary production (GPP) and growth of higher trophic levels.

However, majority of studies focus on pelagic processes and net effects at whole lake scale is not well understood. Consequently, the lack of knowledge of what factors control benthic GPP makes predictions of net effects of climate change on whole-ecosystem GPP spurious. The aim of this thesis was to experimentally test effects of warming and increased input of allochthonous cDOM on habitat- specific and whole-ecosystem GPP in lakes. First, by manipulating the CO2

concentrations in large scale pond ecosystems, we showed that increased CO2

stimulated whole-ecosystem GPP. In a separate incubation study with natural lake sediments in a boreal lake, we tested the role of CO2 as a limiting factor for benthic GPP under different light levels. The results showed that CO2 supply stimulated benthic GPP at high but not at low light availability, suggesting that benthic GPP can be CO2-limited. In the same experimental pond ecosystems, the combined effect of increased allochthonous cDOM and warming (+3.5°C) on GPP was studied. The results showed that cDOM input decreases whole-ecosystem GPP, mainly as a result of decreased benthic GPP due to light limitation not fully counteracted by an increase in pelagic GPP under ambient conditions. Warming on the other caused a hump shaped increase in whole-ecosystem GPP with increasing cDOM input mainly due to a positive response in pelagic GPP due to relaxed nutrient limitation. Finally, by manipulating the fish consumer biomass in the same experimental pond ecosystems we showed that whole-ecosystem GPP can be controlled by top-down effects under warm (+ 3.0°C) but not ambient temperature conditions. The decline in whole-ecosystem GPP was mainly attributed to a warming-stimulated consumer-driven trophic cascade in the pelagic habitat and top-down control by zooplankton on phytoplankton growth, while no corresponding cascade was evident in the benthic habitat.

Taken together, the results suggest that climate change impacts, as increasing inputs of cDOM, warming and changes in food webs, have different effects on habitat specific GPP and alone or in combination have impacts on whole-lake GPP. This thesis offers important insights to better understand the factors that control lake GPP and to predict future lake ecosystem responses to environmental change.

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Background

Gross primary production (GPP) is a fundamental ecosystem process that forms the resource base for higher trophic levels (Odum, 1956). In lakes, phytoplankton have for long been considered the main driver of whole-lake productivity (Byylinsky & Mann, 1973; Schindler, 1978). Phytoplankton are limited by nutrient and light (Gikuma-Njuru & Hecky, 2005; Bergström & Karlsson, 2019), which both may be influenced by allochthonous cDOM input. Earlier studies have shown that phytoplankton biomass and GPP are positively related to phosphorous concentration (Dillon & Rigler, 1974; Schindler, 1977). Recent studies have also found nitrogen limitation of phytoplankton productivity in oligotrophic lakes (Paerl et al., 2014; Poxleitner et al., 2016; Trommer et al., 2020).

In addition, some experimental studies showed that phytoplankton productivity is dissolved inorganic carbon (DIC) limited (Jansson et al., 2012; Kragh & Sand- Jensen, 2018). These paradigms of nutrient and DIC limitation of lake productivity are based on studies on phytoplankton, despite that benthic algae contribute to whole-lake ecosystem GPP (Vadeboncoeur et al., 2002). Some studies have emphasized that periphyton in benthic habitat are light limited and may contribute to a significant part of whole-ecosystem GPP in lakes (Vadeboncoeur et al., 2003; Karlsson et al., 2009). Furthermore, warming impacts on lake productivity are still uncertain (Kazanjian et al., 2018), especially in combination with increasing inputs of cDOM. The available results regarding warming impacts have been showing various responses of phytoplankton biomass; direct positive (Yvon-Durocher et al., 2015), negative (Butterwick et al., 2005) or non-significant impacts (Huertas et al., 2011). It has also been shown that rising water temperature affects phytoplankton biomass growth indirectly due to its impact on consumer consumption and metabolism (O’Connor et al., 2009; Elert & Fink, 2018; Gibert, 2019). Still, there are several unresolved questions that prevent making firm assessments for the impacts of climate change on lake productivity.

Carbon dioxide limitation

The studies showing nutrient limitation of lake productivity led to a consensus among freshwater ecologists in the 1970s that DIC does not constrain phytoplankton productivity. Instead, it was generally regarded that carbon dioxide (CO2) uptake from the atmosphere could cover the demanded of CO2 for photosynthesis (Schindler et al., 1972). Recent studies do however suggest that availability of CO2 can constrain GPP.

In water, CO2 makes up the total DIC pool together with bicarbonate (HCO3-) and carbonate (CO3-2). The DIC concentration is controlled by a range of biological,

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chemical and physical processes, including in situ primary production, respiration (ER) and photooxidation, inputs from external sources, and exchange with the atmosphere. Allochthonous dissolved organic carbon (DOC) input causes lakes to be CO2-supersaturated (del Giorgio & Peters, 1994) by promoting heterotrophic mineralization and photooxidation (Karlsson et al., 2007; Vachon et al., 2017). At the same time, allochthonous DOC reduces light availability and constrains primary production, especially in benthic habitat (Ask et al., 2009).

The role of CO2 in controlling lake productivity is not as well understood as nutrient and light limitation. Since primary producers take up CO2 by the Rubisco enzyme through photosynthesis (Badger et al., 1998), CO2 concentration can be significantly depleted during phytoplankton blooms (Society, 1976; Maberly, 1996). Recent studies have now actually shown that CO2 availability can constrain photosynthetic carbon fixation and phytoplankton growth rates. Small scale experiments have shown that increased CO2 concentration stimulates phytoplankton biomass and pelagic GPP (Jansson et al., 2012; Vogt et al., 2017).

Moreover, mesocosm results have suggested that high supply of DIC promotes phytoplankton productivity in eutrophic lakes (Verspagen et al., 2014; Kragh &

Sand-Jensen, 2018). CO2 limitation for phytoplankton GPP has also been observed in nutrient-rich waters (Hammer et al., 2019).

In contrast to CO2 effects in pelagic habitats, the effects on benthic GPP is largely unknown, especially with increasing light attenuation via increasing allochthonous DOC inputs. Recent studies emphasize to include both pelagic and benthic habitats to understand whole-ecosystem productivity (Vadeboncoeur et al., 2001; Karlsson et al., 2009). The role of CO2 availability to control whole- ecosystem GPP, especially in shallow lakes where both pelagic and benthic habitats may contribute significantly to whole-ecosystem GPP, has never been tested.

Combined effect of warming and allochthonous dissolved organic matter

Lakes in northern regions are rapidly warming (Niedrist et al., 2018). It is expected that warming influences all trophic levels of aquatic food webs directly and indirectly. Warming affects GPP of aquatic ecosystems due to direct effects on metabolic rates of autotrophs (Yvon-Durocher et al., 2010), but net effects on lake productivity are still not clear (Kazanjian et al., 2018). Different types of primary producers may show contrasting responses to warming. Aquatic macrophytes growth can be promoted by warming (Rooney & Kalff, 2000). In contrast, the response of benthic algae is less clear, with studies showing both positive (Tarkowska-kukuryk & Mieczan, 2012), negative (Cao et al., 2014) or no

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direct effects (Shurin et al., 2012; Hao et al., 2018). Similarly, phytoplankton have shown positive (Petchey et al., 1999; Yvon-Durocher et al., 2015), negative (Butterwick et al., 2005; Shurin et al., 2012) or non-significant (Huertas et al., 2011) responses to warming. Warming could also affect GPP indirectly via impacting heterotrophic consumers and their potential top-down control of autotrophs (Sommer & Lewandowska, 2011). Warming is also likely to affect northern lake ecosystems by changing the duration and thickness of ice cover and snow, resulting in delayed ice on and earlier ice off (Gebre et al., 2014), which in turn influences light availability and thus potentially GPP (Lenard, 2015;

Obertegger et al., 2017).

Increasing air temperatures and precipitation are expected to increase allochthonous cDOM input to northern lakes as a result of elevated runoff, terrestrial GPP and thawing of permafrost (IPCC, 2013; Creed et al., 2018).

Increased input of allochthonous cDOM results in water brownification and increased light attenuation (Nydahl et al., 2019), which generally influence whole- ecosystem GPP and shift the relative contribution of habitat-specific GPP from benthic to pelagic habitats (Karlsson et al., 2009; Seekell et al., 2015).

Allochthonous cDOM input also provides additional nutrients that can promote pelagic GPP (Jansson et al., 1996). Moreover, as mentioned above, allochthonous cDOM input enhances in situ CO2 production which may also promote GPP.

Despite that climate change is expected to cause both warming and browning of lakes, few studies have addressed their combined effects on aquatic GPP.

Previous studies have largely focused on ecological and biogeochemical consequences of climate change impacts in summer or winter season, while less attention has been given to test these impacts on ecological processes during autumn-winter transition. The combined impact of warming and allochthonous cDOM inputs on whole-lake GPP during autumn is largely unknown. While warming can enhance metabolism, reduced light availability may constrain the predicted positive warming response of autotrophs. This mismatch will likely be enhanced when light limitation exceeds nutrient limitation with increasing cDOM inputs.

Top-down controls in a warmer climate

GPP can be affected by top-down controls by grazers. It has been demonstrated that top-down effects of plankton communities could influence pelagic GPP of lake ecosystems (Brooks & Dodson, 1965; Carpenter et al., 1987; Hiroki et al., 2020). Reducing abundance of planktivorous fish populations could decrease phytoplankton growth due to trophic cascade effects via enhancing grazing by zooplankton (Lynch & Shapiro, 1981; Sosnovsky & Quiro, 2009). Hence, herbivory

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can be a major driving factor for depleting phytoplankton biomass which can affect GPP (Sperfeld et al., 2010). Similarly, herbivorous fish and zoobenthic invertebrates exert top-down control of benthic algae biomass (Darcy-Hall, 2006;

McIntyre et al., 2006; Holomuzki et al., 2010), which may affect benthic contribution to whole-lake primary production.

Moreover, consumers are more sensitive to temperature than producers (Ji et al., 2017). A potential decline in fish biomass production with ongoing warming in northern lakes (e.g. Tammi et al., 2003; Dorst et al., 2019) may increase grazer biomass via reduced predation, and in turn causes more pronounced top-down effects on the phytoplankton community (Rall et al., 2012). Hence, warming can indirectly reduce phytoplankton biomass growth by promoting zooplankton grazing rates (Sommer & Lewandowska, 2011). Warming effects on benthic communities are poorly studied, and existing results are mixed, including negative effects on benthic invertebrate abundance (Finlay et al., 2001; Jyväsjärvi

& Hämäläinen, 2015) and positive effects on benthic invertebrate grazing rates (Dumont & Schorreels, 1990), but these studies did not assess top-down effects on benthic primary production..

Consequently, studies regarding the effects of trophic cascades and top-down controls on whole-lake GPP have so far only been focused on pelagic habitats (Carpenter et al., 1987; Auer et al., 2004), implying it is presently not known how these controls will be affected by warming to impact lake primary production.

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Aim of the thesis

The overall objective of this thesis is to study the impacts of warming and increasing inputs of allochthonous carbon sources on lake primary production.

Particularly, I address the following research questions (numbers refer to the individual chapters):

I. Is carbon dioxide availability important to control whole-lake GPP?

II. Is benthic GPP of northern lakes carbon dioxide-limited?

III. How do warming and allochthonous cDOM input affect whole- ecosystem GPP of northern lakes in autumn?

IV. How does warming influence trophic cascades and top-down controls of lake GPP?

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Methods

Study systems and methods

Experimental pond system

Three studies were carried out at the Umeå University Experimental Ecosystem Facility (EXEF) located at (63° 48ʹ 34ʹʹ N, 20° 14ʹ 33ʹʹ E). EXEF is a large-scale experimental pond system (73 m long, 25 m wide and 1.5 m depth). It is divided into 20 enclosures (11.5 × 6.7 m) (Figure 1). EXEF allows for semi-natural ecosystem studies that includes yearly natural ice and snow cover during winter season. Each enclosure has separated inlet and warming with individual heat exchangers is possible for eight of the enclosures to a predetermined level above ambient temperature during the ice-free season. Each enclosure contains an ecosystem with a soft bottom benthic habitat and naturally occurring benthic and pelagic primary producers and invertebrate consumers. In addition, three-spined stickleback (Gasterosteus aceulatus) populations were present in one experiment as a top consumer. This species is from the family of Gasterosteidae and it is a common species in both freshwater and marine systems. Three-spined sticklebacks are omnivorous and feed on both zooplankton and benthic macroinvertebrates communities. Furthermore, in another experiment and to mimic increased input of allochthonous cDOM to freshwater systems as a climate change impact, natural humic water was transported at regular time intervals from a small boreal river, Hörneån (63° 57' N, 19° 25' E) to EXEF and stored in a large tank.

EXEF was used to carry out experiments during ice-free and ice-on seasons (Figure 1 and 2). A test of the role of elevated CO2 in controlling whole-ecosystem GPP (I) was carried out during ice-on period, taking the advantage of ice cover presence. Accumulated CO2 under ice was manipulated by ice-removal treatment for a group of enclosures, while keeping another group of ice-covered enclosures as controls (Figure 2). Two experiments were carried out during ice-free periods:

to investigate responses of whole-ecosystem and habitat-specific GPP in northern lakes to the combined effect of warming and allochthonous cDOM input during autumn (III), as well as the role of warming in driving top-down controls of pelagic and whole-ecosystem GPP (IV).

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Figure 1. A) Air view of the EXEF facility with its 20 enclosures. The four enclosures in the middle served as temperature buffer zone, while the other eight on each side were used for experimental purposes. On the right shore tank, the small construction to house the heat exchangers (top) and the large tank to store DOC water (top ais visible). B) Trawling of fish. C) Removed three-spined stickleback fish. D) MiniDOT logger and pelagic incubation camber. E) Benthic incubation chamber.

F) All equipment installed in an enclosure (a free MiniDOT logger, pelagic and benthic chambers, and a light sensor).

(B) (C)

(D) (F)

(A)

(E)

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Figure 2. A) Ice-covered enclosures of EXEF during winter. B) 10 % ice-cover removal treatment. C) 50% ice-cover removal treatment.

Photos: Mohammed Hamdan (A)

(B) (C)

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Natural lake

One of the experiments (II) in this thesis was carried out in Lake Ljusvattentjärn in the summer 2017. The lake (mean depth: 5.5 m, area 1 ha) is situated (64° 5' 30.97" N, 18° 55' 52.74" E) in northern Sweden (Figure 3). The lake receives high input of organic matter from the surrounding catchment (dominated by coniferous forest and mires), therefore light availability in this lake is rapidly attenuated with increasing depth. The vertical attenuation coefficient (kd, m^-1) in the lake water was 1.4 m^-1. Water chemistry of the lake was: 7.35±0.11 mg L^-1DIC, 7.45±0.11 mg L^-1 DOC, 240.08±27.66 µg L^-1 total nitrogen (TN), 21.32±1.16 µg L^-1 total phosphorous (TP), 3.80±0.07 µg L^-1nitrate (NO3−), 13.22±1.71 µg L^-1 ammonium (NH4+), and 0.75±0.05 µg L^-1phosphate (PO43−).

Figure 3. Shore view of Lake Ljusvattentjärn (left) and a sediment core with microbenthic algae layer (right).

Photos: Mohammed Hamdan

Abiotic variables

Light intensity [PAR, photosynthetic active radiation (μmol m^-2 s^-1)] was continuously measured every 10 min over the whole study periods by light sensors (SQ-110, Apogee USA) which were deployed at 0.8 m depth at each enclosure and recorded with loggers (Delta-T Devices, UK) (I, III, IV) or fixed at 0.5 m depth to record PAR every 20 minutes (II) during the entire experiment. In addition, PAR was measured every second day at every 0.5 m between the surface and the bottom using a LI-193 Spherical Quantum Sensor (LI-COR Biosciences, Lincoln, Nebraska, USA) (II). kd was calculated as the slope of the linear regression between the natural logarithm of PAR and depth (II). From the kd and PAR data at 0.5 m, I calculated PAR for the twenty-minute intervals at each incubation depth (II). Dissolved oxygen (DO) and water temperature were

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measured at ten-minute intervals by logging sensors (MiniDOT, PME, Vista, CA, USA), either deployed at 0.5 m below the water surface in the centre of each enclosure (I, III, IV) or placed inside the incubation chambers during incubations for pelagic (III, IV) and benthic measurements (II, III).

For benthic incubation (II), surface sediment cores (with associated benthic microalgae) (Figure 3) were collected from 1-1.5 m using a sediment gravity corer.

The top 10 cm of the sediment, with approximately 0.5 L overlying water, were gently transferred into 2 L (32 cm height, 8.6 cm inner diameter) transparent acrylic incubation chambers of the same diameter as the collection cores. The chambers were divided into one control and two treatment groups with different sources of CO2. As a direct source, we increased the concentration of DIC in the water by adding 10 mL of a sodium bicarbonate (NaHCO3) solution (12 mM DIC).

As an indirect source (i.e., via mineralization of DOC), we added 20 mL of a glucose solution (7 mM DOC).

Water samples were taken every second day (I), before and after incubation (II), and every second week (III, IV). Water samples were filtered and stored at -20

℃ for later analysis of total phosphorous (TP) and total nitrogen (TN) (I, II, III, IV). TP was measured according to Murphy & Riley, (1962) by using potassium persulfate for digesting the samples. For DOC (II, III), 50 ml of water sample was filtered through burnt (550℃, 4 h) acid washed 0.45 µm Whatman GF/F filters, acidified with 500 µl 1.2 M HCl, and stored at 4℃ until analyses. For DOC and TN, water samples were analysed using a combustion chamber (IL550 TOC/TN analyser, Hach Lange GmbH, Germany). For NO3−, PO43− and NH4+, water were filtered (GF/F as above) and stored in freezer until analysis with photometric flow injection analysis (FIA) method (Gray et al., 2006) (I, II, III, IV). Partial pressure of CO2 (pCO2) in the enclosures was manually measured in situ with a hand-held nondispersive infra-red CO2 sensor (Vaisala GM70 Carbon dioxide meter) (III).

The concentration of CO2 (I), and of DIC (II), was also estimated by using a headspace equilibration technique (Lundin et al., 2013) and analysis by gas chromatograph (Perkin Elmer Clarus 500).

Whole-ecosystem and habitat-specific gross primary production

Whole-ecosystem and habitat-specific GPP were calculated from the changes in oxygen concentration over time. GPP was calculated with inverse modelling and Bayesian parameter estimation using a similar parameter estimation approach as for diel dissolved oxygen in streams (Hotchkiss & Hall, 2014). Dissolved oxygen data from the free oxygen loggers in the centre of each enclosure were used to estimate whole-ecosystem GPP (I, III, IV), while habitat-specific GPP was

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estimated using data from loggers in incubation chambers: a 2 L (32 cm height, 8.6 cm inner diameter) transparent acrylic tubes were positioned vertically 0.5 m below the water surface for pelagic GPP (III, IV) and at four incubation depths for benthic GPP (II), while a 12 L (35 cm inner diameter) semi-spherical transparent polycarbonate chambers grounded to the bottom sediment surface for estimating benthic GPP (III). The benthic chambers have a metal frame underneath assuring tight grounding to the sediments surface (III). Habitat- specific GPP was estimated as whole-ecosystem rates (same model), but the emission flux of oxygen to or from the atmosphere was fixed at zero for closed chambers.

The metabolism model used a “random walk” metropolis algorithm and Markov Chain Monte Carlo (MCMC) sampling from the “metrop” function in the “mcmc”

package of the statistical program R (Geyer & Johnson, 2013) to find the best fit between measured and modelled dissolved oxygen data given model estimates of GPP and respiration. Each parameter estimate was derived from 10000 model iterations after removing an initial 1000 iterations of “burn-in” from parameter starting values. Then, we checked for convergence of parameter estimates and removed days with negative GPP and with poor fits between measured and modeled dissolved oxygen.

Phytoplankton biomass

Every second week (III) and every fourth week (IV), 100 ml water samples were filtered by 0.45 µm Whatman GF/F filters to measure Chl-a biomass. Chl-a was extracted in 95% ethanol for 24 h in the dark. Extraction vials were shaken several times during the extraction. Chl-a was then analyzed in a Perkin Elmer spectrofluorometer (LS-55) with the excitation wavelength set to 433 nm and emission wavelength to 673 nm (Strickland & Parsons., 1972). To provide estimates of carbon by phytoplankton Chl-a biomass, C:Chl-a ratio was calculated for carbon and Chl-a data of pelagic habitat for cDOM gradient treatment in ambient and heated enclosures (III).

Invertebrate biomass

Zooplankton were sampled by a zooplankton net (diameter 20 cm, 100 µm mesh size) drawn vertically trough whole water column of each enclosure and preserved in Lugol’s solution every second week (I) and every fourth week (IV).

Zooplankton biomass was calculated using a semi-automatic ZooScan system (HYDROPTIC) where the samples were scanned in the scanning cell of an area of 15×24 cm and digitized at a resolution of 2400 dpi in the laboratory. Zoobenthos were sampled every second week (I) and every fourth week (IV) with a net (30 cm wide, 1 mm mesh size), dragged about 1 m along the homogenous soft bottom of

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each pond. Each sample was then preserved in ethanol for later analysis. In the laboratory, zooplankton and zoobenthos were classified to order, family, or genus. Biomass then was estimated using the dry weight estimates (Bottrell et al., 1976; Netto & Gallucci, 2003).

Fish

A fish top consumer population, the three-spined stickleback (Gasterosteus aculeatus) has been present in each enclosure since spring 2012 were 40 adults were introduced to each enclosure. Three-spined stickleback is a small omnivorous fish which feeds on both zooplankton and small benthic invertebrates (Wootton, 1984). On the 13-15^th of July 2015 the number of fish in each enclosure was determined by seine-netting three subsequent times each enclosure with a seine net (IV). Captured fish were placed in plastic containers and photographed from above. The number of fish per catch were counted using image analysis on site within an hour of capture. The number of individuals in each enclosure were then estimated by the pass removal method (Zippin, 1956).

After removal of predetermined proportion of fish, the remaining fish were released back to each enclosure. Number of fish and individual length were later estimated again by photo image analysis technique and population biomass and biomass of removed sticklebacks were estimated from a common length-weight regression for the removed fish from each enclosure.

The three spine stickleback populations were present in the enclosures up until spring 2017 when the whole pond was emptied of water, all sticklebacks were removed, and the pond refilled again. In May 2018 new populations of nine-spine sticklebacks (Pungitus pungitus) were established in each enclosure at the start of a new experiment.

Ethical approval

The use of fish in one of the studies (IV) was approved by the local ethics committee of the Swedish National Board for Laboratory Animals in Umeå (CFN, license no. A-20-14 to Pär Byström).

Statistical analyses

The used statistics methods varied dependent on the design of the different studies. Repeated measures ANOVA was used to account for time effects between treatments periods (I), while two-way repeated measures ANOVAs were used to account for the time and the treatments effects over the experiment periods (III).

Two-way ANOVAs were used to test the effects of treatments, incubation depths and their interaction on the variables (II), as well as to test the responses of GPP

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to cDOM inputs and warming treatments during the third and fourth sampling periods of the experiment (III). To identify the significant differences in the responses to the treatments at the different incubation depths (II), Tukey post hoc tests were used when the interaction term was not significant, while separated one-way ANOVAs were used when the interactions were significant to test the effects of treatments at each incubation depth. Regression analyses were used to test the response of variables to the gradient of cDOM inputs (III) as well as to fish harvesting levels (IV). Analysis of covariance (ANCOVA) was used to test responses to warming treatment compared to ambient as well as the effect of fish harvesting level as a continuous variable (IV). T-tests were used to test differences in variables between the control and treatment (I), (II), (III), and (IV). The correlations between selected variables in (I), (II), (III), and (IV) were calculated using Pearson correlation coefficient (r).

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Major results and discussion

Carbon dioxide controls whole-lake primary production

In chapter I, we took the advantage of high accumulated CO2 under ice cover over winter to test its effect on whole-ecosystem primary production. We decreased CO2 concentration in water column by ice-cover removal allowing release of CO2

to the atmosphere, while keeping the control enclosures with high CO2

concentration. The whole-ecosystem GPP was positively related to CO2

concentration in water column (Figure 1 and Table 1, I). Whole-ecosystem GPP and CO2 concentration in control enclosures were higher during ice cover than after ice break-up (Figure 1 and 2, I). In ice cover removal enclosures, whole- ecosystem GPP and CO2 concentration did not change by 10% ice-cover removal treatment compared to control but were negatively affected by 50% ice-cover removal (Figure 2 and Table 1, I). When both control and treatment enclosures became ice-free, the CO2 concentration and whole-ecosystem GPP decreased and were similar between control and treatment enclosures (Figures 1, 2 and Table 1, I). Other abiotic or biotic variables as nutrient concentrations (NO3−, PO43− and NH4+), PAR, water temperature, or zooplankton biomass and zoobenthos biomass did not significantly differ between control and treatment enclosures, therefore they do not explain the differences in whole-ecosystem GPP observed between control and treatment groups. Previous studies have demonstrated that CO2

concentration positively impacts pelagic GPP (Jansson et al., 2012; Vogt et al., 2017). Our results show the importance of CO2 at the whole-ecosystem GPP scale.

Given that northern lakes are generally CO2 supersaturated, our results suggest that CO2 stimulation of whole-ecosystem GPP may be common in northern lakes.

Carbon dioxide limitation of benthic primary production In chapter II, we tested if CO2 limitation may control benthic GPP in a boreal lake. We incubated lake surface sediments (with associated benthic algae) from a small boreal lake in Northern Sweden together with a direct (DIC addition) or an indirect (CO2 production via mineralization of DOC) source of CO2 and examined the effects on benthic GPP at different light levels (generated by incubation at different depths). Nutrient concentrations did not change with the DIC and DOC additions and were independent of the interaction between light availability and treatments, suggesting that nutrient availability did not affect the benthic GPP results. The results showed that benthic GPP was stimulated by CO2 from the different sources when light availability was high, but not when light was at suboptimal levels (Figure 2, II). These results further stressed the importance of light for benthic GPP and show that additional CO2 cannot stimulate benthic GPP when light is limiting. Our results also stress the complex role of allochthonous

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DOC for primary production, via direct negative effects on light availability but indirect positive effects on nutrient and CO2 availability. Allochthonous organic carbon stimulate heterotrophic bacteria in pelagic systems to outcompete algae for limiting nutrients (Jansson et al., 1999). Bacteria may thus supply algae with CO2 by mineralizing DOC (Nydahl et al., 2019), but at the same time decrease the available nutrients (Danovaro, 1998). However, soft-bottom benthic algae generally obtain nutrients from the nutrient-rich sediments (Bonilla et al., 2005) and boundary layer effects are pronounced at the sediment surface (Riber &

Wetzel, 1987). This suggest that CO2 limitation may be more common for benthic than for pelagic algae and that the net role of bacterial metabolism for benthic GPP is positive (via production of CO2) rather than negative (via bacterial nutrient uptake).

Combined effect of warming and allochthonous dissolved organic matter on lake primary production

In chapter III, we experimentally increased water temperature and applied a gradient of inflow rates of stream water with high cDOM in EXEF in autumn to test the combined effect of warming and cDOM on primary production. The results showed that GPP was impacted by both cDOM input and warming.

Increased cDOM negatively affected whole-ecosystem GPP at ambient conditions by reducing benthic GPP more than stimulating pelagic GPP. Warming increased whole-ecosystem GPP across all levels of cDOM due to the stimulation of mainly pelagic GPP (Figure 3, III). Warming shifted the negative effects of light limitation via increasing cDOM on whole-ecosystem GPP to a hump-shaped response.

Pelagic GPP increased at low and medium levels of cDOM, while decreased at the high level. This result suggests that phytoplankton growth was nutrient limited and stimulated by nutrients associated with cDOM when light was readily available. It is also likely that increased CO2 via mineralization of cDOM stimulated pelagic GPP (Jansson et al., 2012) due to its role as substrate for photosynthetic enzymes (Badger et al., 1998). The decreased pelagic GPP at the highest level of cDOM could be mainly attributed to the shift from nutrient to light limitation (Bergström & Karlsson, 2019). The magnitude and hump-shaped response in pelagic GPP to cDOM gradient input was stronger with warming likely due to that warming enhances phytoplankton nutrient uptake rates (Rhee

& Gothan, 1981; Malik & Saros, 2016).

Benthic GPP decreased with increasing cDOM input which suggests that light was the primary controlling factor of benthic primary production. Benthic algae can get nutrients from the sediment and sediment-water interface (Bonilla et al., 2005), therefore they are not expected to directly rely on additional nutrient via

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cDOM inputs. Warming enhanced benthic GPP at low and medium cDOM inputs likely due to increased photosynthetic rates when light availability was relatively higher but not at the highest level of cDOM since light was limited. This result suggests that light limitation can counteract any positive temperature response of GPP in benthic habitats.

Warming extended the duration of ice-free period by two weeks compared to ambient enclosures. The initial formation of a transparent ice cover did not significantly affect the incoming light availability in ambient ice covered compared to heated ice-free enclosures. The differences in GPP between ambient and warm enclosures during this period (Figure 3, III) can be attributed to increased photosynthetic rates by higher temperature (Finkel et al., 2010) in warmed ice free compared to ambient ice covered enclosures. In the last part of the experiment when both ambient and warm enclosures were ice-covered, whole-ecosystem and habitat-specific GPP were only affected by cDOM input (Figure 3; Table 2, III) via similar reduction in light availability.

The results (III) suggest that both cDOM inputs and warming can have strong effects on lake GPP. It is likely that warming stimulates whole-ecosystem GPP in systems with low and intermediate concentrations of cDOM, but the effect is diminished in systems with high cDOM inputs due to increased light limitation.

Hence, we conclude that climate change may alter patterns of whole-ecosystem GPP through asymmetric responses of habitat-specific GPP to warming and increasing cDOM inputs.

Warming strengthens trophic cascades and top-down control of lake primary production

In chapter IV, we experimentally manipulated planktivorous fish biomass (three- spined stickleback) at ambient and warming temperatures (+3.4°C) in EXEF to test the impact top-down control and warming on whole-lake primary production. The results showed that both warming and fish removal affected whole-ecosystem primary production. Fish removal caused a trophic cascade with increased zooplankton and zoobenthos biomass and decreased whole- ecosystem primary production. Interestingly, the cascading top-down effects on whole-ecosystem GPP was only at warming and in the pelagic habitat only, while no impact was present under ambient conditions and in the benthic habitat.

It has been suggested that the fish predation per se, and the cascading effects on phytoplankton biomass under warming conditions, is stronger than the direct stimulating effects on phytoplankton of warming itself (Meerhoff et al., 2012).

Further, in a mesocosm study, Hansson et al., (2013) showed that warming stimulated phytoplankton biomass when planktivorous fish were present, but

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suppressed phytoplankton community abundance when planktivorous fish were absent. Our results suggest that lake GPP can be impacted by warming- enhanced grazing pressure on phytoplankton. Pelagic GPP in warm enclosures declined with increasing zooplankton biomass. In contrast, despite the significant increase in zoobenthos biomass in warm treatments with decreasing fish biomass, presumably due to reduced predation (Nyberg et al., 2010) combined with stimulated benthic invertebrate growth at higher temperatures (Baulch et al., 2005), benthic GPP did not decline. Our results agree with Hansson, (1992) who found that warming and food web composition are of minor importance for periphyton growth. In addition, since benthic GPP is less sensitive to warming compared to pelagic GPP (Rodríguez & Pizarro, 2015), it could be possible that our warming treatment was not enough to get the targeted response in benthic primary production. It is also possible that increased light availability for benthic algae due to the reduced shading from phytoplankton may have caused an increased benthic GPP which compensated for the increased grazing from benthic grazers.

Our results suggest impacts of warming on lake GPP vary with top-down grazing pressure on the algae. Thus, warming plays an important role to strengthen trophic cascades and top-down effects to indirectly control lake primary production. This also suggest that overall response likely varies across lakes since multiple factors affect the fish community in addition to warming (Dantas et al., 2019), for instance invasive piscivore fish (Nõges et al., 2018) and human implications such as fish catch and overfishing (Zwieten et al., 2002; Mölsä et al., 1999).

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Conclusions and outcomes

In this thesis, I have examined the knowledge gaps concerning controls of ecosystem GPP of northern lakes. I found that CO2 availability is important limiting factor for whole-lake (I) and benthic (II) GPP and that the latter also depends on light availability (II). The results imply that allochthonous carbon input (via elevated CO2 concentration) can have a positive impact on GPP in shallow lakes and in lakes with low to intermediate input of allochthonous DOC, while in deep and more DOC-rich lakes light limitation should override any positive effect of CO2. Hence, the results suggest including our findings when developing models describing controls of lake ecosystem productivity and impacts to environmental change. More studies regarding the complex interactions between light, CO2, and nutrients are required to better understand limitations of lake GPP to conceptualize the role of allochthonous carbon in northern lake ecosystems.

Further, I found (III) that GPP was impacted by both cDOM input and warming.

At natural temperature conditions, the cDOM input decreased whole-ecosystem GPP mainly because of lower benthic GPP not fully compensated by an increase in pelagic primary production. Warming increased whole-ecosystem GPP due to a positive response in mainly pelagic GPP at all levels of cDOM input. These results suggest that climate change, via the interactive effects of allochthonous cDOM inputs and warming, has strong impacts on lake GPP and provides an experimental evidence for the predicted hump-shape response of GPP to increasing cDOM inputs (Seekell et al., 2015). Hence, we conclude that climate change can change whole-ecosystem GPP through asymmetric responses of habitat-specific GPP to warming and increasing cDOM inputs. The results stress the importance of accounting for multiple climate drivers and habitats when predicting lake GPP responses to climate change.

In addition to direct impacts of warming on autotrophs, warming reinforces higher trophic levels and that disrupts herbivorous communities in food webs to stimulate primary producers’ growth indirectly. Many studies predicts that climate warming may affect freshwater food webs by reducing biomass of higher trophic levels (Arim et al. 2007; O’gorman et al. 2016; Dantas et al. 2019). We found (IV) that warming and fish removal can affect whole-ecosystem primary production. However, trophic cascades and strong top-down effects were only observed in the pelagic habitat, while no impact was present in the benthic habitat. Taken together our results suggest that whole-ecosystem GPP of lakes in warm conditions may be negatively impacted by changes in fish abundance and the effects are mainly caused by changes in the pelagic habitat via top-down effects of zooplankton on phytoplankton and pelagic GPP. These effects suggest

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that trophic cascades and effects on lake GPP will be more likely to occur and become stronger as climate may become warmer. Our findings increase the understanding of controls of GPP in lake ecosystems with ongoing global warming and suggest that GPP of northern lakes will be negatively affected by warming.

Overall, the results of this thesis provided new knowledge on factors controlling habitat-specific and whole-lake GPP but also left some unexplored knowledge gaps and possible future important research directions regarding the factors that control GPP of northern lakes under ongoing climate change. For instance, it would be interesting to investigate the combined effect of increased CO2

concentration and warming on the GPP of northern lakes. It would also be interesting to investigate the role of these two factors in combination with increasing light extinction, which is due to increased allochthonous DOC inputs, on primary production.

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Acknowledgement

I thank Jan Karlsson, Pär Byström, and Erin Hotchkiss for all valuable comments on this thesis summary. Work described in this kappa was financed by grants from the Ministry of Higher Education and Scientific Research in Iraq to MH (dnr: 18603-2014-12-06) and by the Knut and Alice Wallenberg Foundation to JK (dnr: 2016.0083).

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