Food web structures and carbon transfer efficiencies in a brackish water ecosystem. Kristin Dahlgren

Transkript

1 Food web structures and carbon transfer efficiencies in a brackish water ecosystem Kristin Dahlgren Department of Ecology and Environmental Science Umeå University Umeå Umeå 2010

2 Copyright Kristin Dahlgren ISBN: Frontcover: Limnocalanus macrurus, photo by UMF and phytoplankton community, photo by Chatarina Karlsson, UMF Elektronic version available at Printed by: Print & Media Umeå, Sweden 2010

3 Till Anders och Axel

4 List of papers This thesis is based on the following papers, which will be referred to in the text by their Roman numerals. І. Dahlgren K, Andersson A, Larsson U, Hajdu S, Båmstedt U (2010) Planktonic production and carbon transfer efficiency along a northsouth gradient in the Baltic Sea. Marine Ecology Progress Series, 409: ІІ. ІІІ. ІV. Dahlgren K, Eriksson Wiklund A-K, Andersson A. Influence of plankton structure and temperature on pelagic food web efficiency in a brackish water system. Submitted manuscript Eriksson Wiklund A-K, Dahlgren K, Sundelin B, Andersson A (2009) Effects of warming and shifts of pelagic food web structure on benthic productivity in a coastal marine system. Marine Ecology Progress Series, 396: Dahlgren K, Olsen BR, Troedsson C, Båmstedt U. Seasonal variation in wax ester concentration and gut content in a Baltic Sea copepod (Limnocalanus macrurus (Sars 1863)). Manuscript Paper І and ІІІ have been reproduced with the kind permission from the publisher: Inter-Research.

5 TABLE OF CONTENTS ABSTRACT 6 INTRODUCTION 7 Pelagic food webs 7 Food web efficiency 8 Seasonal dynamics and pelagic-benthic coupling 8 Energy reserves and fatty acids 9 Climate altered food webs 9 Study area: The Baltic Sea 10 Organism groups and definitions 11 OBJECTIVES OF THIS THESIS 12 RESULTS AND DISCUSSION 12 Factors governing pelagic food web function 12 Climate alterations and potential effects on food web efficiency 13 Life strategy in a dominant Baltic Sea calanoid copepod, Limnocalanus macrurus 15 CONCLUDING REMARKS 16 ACKNOWLEDGEMENTS 16 REFERENCES 17 POPULÄRVETENSKAPLIG SAMMANFATTNING 22 TACK 24

6 Abstract Two differently structured food webs can be distinguished in the pelagic habitat of aquatic systems; the classical one (autotrophic) with phytoplankton as a base and the microbial food web (heterotrophic) with bacteria as a base. Energy (produced at the basal trophic level) reaches higher trophic levels, i.e. zooplankton, directly in the classical food web in contrast to the microbial food web where it passes through additional trophic levels before reaching zooplankton. Energy is lost between each trophic level and therefore less energy should reach higher trophic levels in the microbial food web than in the classical food web. However, factors such as edibility of prey, temperature and properties of the predator, might also influence the food web structures and functions. In this thesis I studied which factors are important for an efficient carbon transfer and how a potential climate change might alter the food web efficiency in pelagic and pelagic-benthic food webs in the Baltic Sea. Furthermore, one of the most dominant zooplankton in the northern Baltic Sea, Limnocalanus macrurus, was studied in order to establish the seasonal pattern of lipid reserves in relation to food consumption. My studies showed that the carbon transfer efficiency during summer was not directly connected to the basal production, but factors such as the ratio between heterotrophs and autotrophs, the relationship between cladocerans and calanoid copepods and the size and community structure of both phytoplankton and zooplankton were important for the carbon transfer efficiency. In a climate change perspective, the temperature as well as the relative importance of the microbial food web is likely to increase. A temperature increase may have a positive effect on the pelagic food web efficiency, whereas increasing heterotrophy will have a negative effect on the pelagic and pelagic-benthic food web efficiency, reduce the fatty acid content of zooplankton and reduce the individual weight of both zooplankton and the benthic amphipod Monoporeia affinis. During the seasonal study on the calanoid copepod L. macrurus, I found that this species is mainly a carnivore, feeding on mesozooplankton during most of the year but switches to feeding on phytoplankton when these are abundant. Furthermore, when food is scarce, it utilizes lipids that are built up during the course of the year. From these studies I can draw some major conclusions; there are many factors that influence how efficient carbon is transferred in the food web and different factors are probably of various importance in different areas. In order to determine the carbon transfer efficiency, the various strategies exerted by different organism groups have to be considered, as for example that some zooplankton utilize lipid reserves instead of feeding all year around. Also, in a climate change perspective, the pelagic-benthic food web efficiency will decrease, as will the quality of zooplankton and M. affinis, possibly having implications for higher trophic levels such as fish. Keywords: Carbon transfer efficiency, Food web efficiency, zooplankton, production, pelagic, benthic, fatty acids, wax esters 6

7 Introduction Pelagic food webs In the pelagic habitat of aquatic systems, phytoplankton and bacteria are the most important basal producers, where the carbon produced is transferred to higher trophic levels either through the classical (herbivorous) food web or the microbial food web (Legendre and Rassoulzadegan 1995), Fig. 1. In the classical food web, nano-and microphytoplankton are grazed upon directly by zooplankton (Uitto and Hällfors 1997, Liu and Dagg 2003) and the zooplankton are in turn eaten by zooplanktivorous fish. In the microbial food web, heterotrophic bacteria use dissolved organic carbon as an energy source that is derived either autochtonously from phytoplankton or other planktonic organism groups (Azam et al. 1983) or from allochtonous sources (Hessen 1985a, Moran and Hodson 1990). Heterotrophic flagellates and ciliates are both important grazers on bacteria (Riemann and Christoffersen 1993, Pace and Cole 1996) and are in turn eaten by zooplankton, thus creating a link between bacteria and zooplankton (Sherr and Sherr 1984), Fig. 1. The relative importance of the two different food webs is to a large extent influenced by nutrient availability; the classical food web is mainly found in nutrient-rich coastal areas and during spring and autumn mixing of the water column (Kiørboe 1993, Kiørboe and Nielsen 1994), whereas the microbial food web is mainly found in stratified, nutrient-poor areas (Legendre and Rassoulzadegan 1995). Figure 1. Simplified view of the two main food webs, i.e. the classical food web and the microbial food web, and the carbon transfer between trophic levels. 7

8 Food web efficiency Zooplankton, e.g. calanoid copepods, cladocerans and rotifers, vary greatly in size and consequently feed on different sized particles. Large zooplankton, such as calanoid copepods, are not able to feed directly on particles as small as bacteria (Sherr et al. 1986, Nejstgaard et al. 1995) and therefore additional trophic levels are needed between bacteria and copepods in the microbial food web, as opposed to the direct link between the basal producer and copepods in the classical food web (Uitto and Hällfors 1997, Liu and Dagg 2003). Between each trophic level, energy (carbon) is lost due to respiration, excretion, sloppy feeding etc (Sanders and Wikham 1993, Hessen 1998), resulting in less energy reaching higher trophic levels through the microbial food web compared to the classical food web (Sanders and Wickham 1993). Food web efficiency, defined as the production at the highest trophic level divided by the production at the basal trophic level (c.f. Berglund et al. 2007), is thus lower in the microbial food web compared to the classical food web. However, the energy can take alternative routes through the trophic levels; Cladocerans are able to feed directly on bacteria (Sommer and Stibor 2002), reducing the number of trophic links and thereby also the energy loss through the microbial food web. Furthermore, filamentous and toxic phytoplankton can potentially reduce the food intake by zooplankton (DeMott et al. 1991, Wolfe and Steinke 1996). This would thus lower the energy transfer in the classical food web. Sommer et al. (2002) concluded that toxic algae are not properly ingested by zooplankton, but the energy is instead reaching higher trophic levels by entering the microbial food web through lysis and excretion. The food web efficiency is thus reduced due to additional trophic levels. Seasonal dynamics and pelagic-benthic coupling At temperate latitudes, the primary production shows a strong seasonality, with a distinct phytoplankton bloom in spring, a somewhat smaller autumn bloom and during the rest of the year primary production is low (Kiørboe and Nielsen 1994, Valiela 1995). The spring bloom is usually dominated by microplankton ( µm), such as diatoms and dinoflagellates, while nano (2-20 µm) and picoplankton (0.2-2 µm), such as autotrophic flagellates and unicellular cyanobacteria, dominate during summer and autumn (Andersson et al. 1996, Samuelsson et al. 2006). Zooplankton production and biomass are also strongly seasonal, with biomass values being > 10 times higher during summer than in winter (Kiørboe and Nielsen 1994). Their production is usually correlated to the phytoplankton blooms (Kiørboe and Nielsen 1994) but due to the relatively long developmental time of zooplankton, i.e. calanoid copepods, maximum zooplankton biomass tend to lag a considerable time after the phytoplankton bloom (Kiørboe and Nielsen 1994). Even though much of the phytoplankton bloom is utilized by the zooplankton, the time lag results in a large part of the spring bloom settling to the benthos. Also, sedimentation rates of plankton depend strongly on the size of the particles (Smayda 1970). Consequently, a higher amount of organic carbon reaches the benthos during the spring bloom, when large diatoms dominate, than during summer and autumn, when nano- and picoplankton dominate (Andersson et al. 1996, Samuelsson et al. 2006). The 8

9 magnitude of the spring bloom and the size structure of the phytoplankton community therefore affect the biomass and community structure of the benthos (Pearson and Rosenberg 1978, Johnson and Wiederholm 1992, Buchanan 1993, Josefson et al. 1993). Energy reserves and fatty acids The strong seasonal dynamics in food supply occurring in polar and temperate regions creates a harsh environment for the zooplankton, i.e. herbivorous calanoid copepods (Hagen and Auel 2001). To cope with the low food supply during a large part of the year the copepods has developed different strategies, as for example to store energy in the form of lipids and/or entering diapause, i.e. descending to deeper, colder water where metabolism is reduced (Kattner and Hagen 1995, Pasternak et al. 2001). The energy storage is mainly in the form of wax esters, which are considered a long-term energy supply, or triacylglycerols, which are a short-term energy supply (Hakanson 1984). These lipids are biosynthesized from dietary fatty acids and fatty alcohols (Sargent and Henderson 1986) and during food shortage they fuel molting, respiration and reproduction. Dietary fatty acids are also important for zooplankton that do not store energy in the form of lipids, since food sources containing high concentrations of fatty acids, especially polyunsaturated fatty acids enhance growth and egg production (Stanley-Samuelson 1994b, Persson and Vrede 2006). Various phytoplankton groups contain different amount of these fatty acids, e.g. diatoms are considered a high quality food whereas cyanophytes are not (Ahlgren et al. 1992). Most bacteria lack these fatty acids (Ahlgren et al. 1990, Brett 1993). Climate altered food webs Since 1861, the earth has experienced a temperature increase of 0.05 C per decade (HELCOM 2007). For the next 2 decades the warming for the entire globe is predicted to be 0.2 C per decade, where the highest temperature increase is expected to occur in the northern latitudes (IPCC 2007). In the Baltic Sea the annual average temperature is predicted to have increased by 3-5 C by the end of this century (HELCOM 2007). This temperature increase will probably affect the whole ecosystem, both directly and indirectly (HELCOM 2007). Direct effects of an increased temperature are for example that metazooplankton development time decrease and biomass increase (Heinle and Flemer 1975, Dippner et al. 2000, 2001, Gillooly et al. 2002) and that the ratio between heterotrophy and autotrophy increase (Müren et al. 2005, Hoppe et al. 2008). Indirect effects of an increased temperature could be a shift in the phytoplankton community from cold-water species to warm-water species (HELCOM 2007) and to one dominated by smaller species (Andersson et al. 1994, Sommer et al. 2007). The climate alterations have also been predicted to cause increased precipitation at higher latitudes, resulting in increased river inflow to the Baltic Sea (Meier 2006, HELCOM 2007). This result in an increased load of humic substances and allochtonous dissolved organic carbon entering the Baltic Sea, as well as a reduction in phosphorous (Bergström et al. 2001) and increased absorbance of light in the water column. Bacteria are able to utilize part of the allochtonous 9

10 dissolved organic carbon (Hessen 1985a, Moran and Hodson 1990) and are therefore less dependent on carbon derived from phytoplankton, resulting in an uncoupling of bacterial and phytoplankton production (Sandberg et al. 2004). The increased freshwater input will also reduce the salinity, which will have effects on the metazooplankton community; cladocerans and small freshwater copepods will be favoured over large neritic copepod species (Vuorinen et al. 1998). Study area: The Baltic Sea The Baltic Sea is a large semi-enclosed brackish sea area, where the three main basins are the Bothnian Bay (1500 km 3 ) in the north, Bothnian Sea (4900 km 3 ) and Baltic Proper (13000 km 3 ) in the south (Niilonen 2002, HELCOM 1990, Elken et al. 1996), Fig. 2. Figure 2. The study area showing the sampling stations in the Bothnian Bay, Bothnian Sea and Baltic Proper for paper І (all stations) and ІV (station A13 in the Bothnian Bay). The experiment in paper ІІ and ІІІ was performed at Umeå Marine Sciences Center (UMSC), with water collected close to the marine station. 10

11 There is a gradual change in several environmental factors from north to south in the Baltic Sea, influencing the production and species composition. Freshwater input in the north and saline water entering from the Atlantic in the south creates a salinity gradient between 1-3 in the Bothnian Bay, 3-7 in the Bothnian Sea and 6-8 in the Baltic Proper (Voipio 1981). Due to the freshwater runoff in the Bothnian Bay, 40 % of the carbon input is derived from allochtonous sources (Sandberg et al. 2004). Availability of dissolved inorganic phosphorus increases from the Bothnian Bay to the Baltic Proper, whereas availability of dissolved inorganic nitrogen decreases in the same gradient, creating a switch from phosphorous to nitrogen limitation along the gradient (Graneli et al. 1990, Wulff et al. 1990, Andersson et al. 1996). Furthermore, the length of the growing season increases from north to south, with spring-warming starting in March-April in the Baltic Proper while being delayed by one or two months in the Bothnian Bay and Bothnian Sea (Kautsky and Kautsky 2000). These factors together contribute to the increase in primary production by a factor of ten from north to south. Bacterial production, however, only increase by a factor of two in the same gradient (Samuelsson et al. 2006), creating a switch from a mainly heterotrophic system in the north to a mainly autotrophic system in the south. Due to the environmental gradient observed from north to south and the low species diversity (compared to fully marine systems), which means fewer trophic linkages to analyse (Elmgren and Hill 1997), the Baltic Sea is especially suitable for studies of structure, function and efficiency of food webs. Organism groups and definitions The organism groups included in this thesis are bacteria, heterotrophic flagellates, ciliates, phytoplankton, zooplankton and a benthic amphipod, Monoporeia affinis. Heterotrophic flagellates and ciliates are both grouped into protozoa. Phytoplankton were divided into picoplankton (0.2-2 µm), nanoplankton (2-20 µm) and microplankton ( µm), based on the largest dimensions of phytoplankton single cells, filaments or colonies. The zooplankton were either termed mesozooplankton ( µm) or metazooplankton (larger than 90 µm). Carbon transfer efficiency was stated in two different ways, i.e. carbon transfer efficiency and food web efficiency. The first was defined as mesozooplankton carbon consumption rate divided by basal production, i.e. the sum of bacterial and phytoplankton primary production (І), and the latter was defined as metazooplankton production divided by basal production (ІІ) and amphipod biomass increment divided by basal production (ІІІ). Thus, both definitions include the measurement of carbon transfer from the lowest trophic level to a higher trophic level. 11

12 Objectives of this thesis The main objective of this thesis was to study food web functions in a brackish water ecosystem, especially carbon transfer efficiency and how it is related to food web structure and climate related factors. The aim of paper І was to assess the efficiency of carbon transfer in the planktonic food web in a natural production gradient and to discuss the main ecological factors governing carbon transfer efficiency. The aim of paper ІІ was to study how climate change, with an increase in temperature and an increase in the ratio between heterotrophy and autotrophy, can influence metazooplankton production and nutritional status as well as food web efficiency in a planktonic food web. The aim of paper ІІІ was to study how climate change, with an increase in temperature and an increase in the ratio between heterotrophy and autotrophy, would affect the productivity of a key benthic amphipod, Monoporeia affinis, as well as the pelagic-benthic food web efficiency. The aim of paper ІV was to define seasonal population cycle, energy status, feeding and food composition in the dominating calanoid copepod in the northern Baltic Sea, i.e. Limnocalanus macrurus. Results and Discussion Factors governing pelagic food web function (Paper І) The classical food web is suggested to be more efficient than the microbial food web since the latter includes more trophic levels where energy is lost between each level (Berglund et al. 2007). However, other factors, such as edibility of prey and zooplankton - and phytoplankton community composition, should also influence the carbon transfer efficiency in pelagic food webs. To study the carbon transfer efficiency and to evaluate which factors govern an efficient transfer, a field study was performed in a northsouth production gradient in the Baltic Sea. Mesozooplankton carbon consumption rate was estimated by measuring oxygen consumption, which was recalculated to carbon consumption rate using a factor to convert oxygen to carbon units, a respiratory quotient of 0.97 (Ikeda et al. 2000) and a mean assimilation efficiency of 0.8 (Lima et al. 2002). Primary and bacterial production was measured using the conventional isotope techniques described by Gargas (1975) and Fuhrman and Azam (1982). The results obtained showed that during summer, carbon transfer efficiency was highest in the intermediate productive area, i.e. in the Bothnian Sea, and lowest in the high productive area, i.e. in the Baltic Proper (І). Thus, carbon transfer efficiency was not directly connected to basal production, but must also have been influenced by other factors. In food webs where cladocerans are the dominant mesozooplankton, the energy 12

13 losses through the microbial food web should be reduced since they, unlike copepods, are able to feed directly on bacteria (Sommer and Stibor 2002). During our investigated period, cladocerans were dominant in the Bothnian Sea as well as at one station in the Baltic Proper in August. Concomitantly, the ratio between heterotrophy and autotrophy was ~1:1 in the Bothnian Sea and ~1:9 in the Baltic Proper (І). Thus, the role cladocerans played for an efficient carbon transfer was likely higher in the Bothnian Sea than in any of the other basins studied. Furthermore, the zooplankton community composition in relation to the food composition and size spectrum seems to be important for high carbon transfer efficiency (І). Of the calanoid copepods, Limnocalanus macrurus dominated in the Bothnian Bay, L. macrurus and Eurytemora affinis dominated in the Bothnian Sea and E. affinis dominated in the Baltic Proper (І). L. macrurus feeds on net phytoplankton, rotifers, as well as nauplii and copepodite stages of cyclopoids and calanoids (Warren 1985), while E. affinis, which is about half the size of L. macrurus, feeds on smaller particles such as detritus and small phytoplankton (Heinle and Flemer 1975, Gulati and Doornekamp 1991). Thus, most of the food size spectrum should be readily available for either of the dominant copepods in the Bothnian Sea. In the Bothnian Bay and the Baltic Proper it is however likely that some of the food size spectrum is left un-utilized (І). Work et al. (2005) concluded that high carbon transfer efficiency is facilitated by a high ratio between grazer size and prey size. This support our results since in the low-productive area where carbon transfer efficiency was intermediate, L. macrurus dominated together with small phytoplankton, whereas in the high-productive area where carbon transfer efficiency was lowest, E. affinis dominated together with large phytoplankton (І). Occurrence of inedible phytoplankton, such as some species of cyanobacteria, reduces the carbon transfer efficiency, as was observed in the Baltic Proper (І). Toxic algae have been shown to reduce the survival and fecundity of mesozooplankton (DeMott et al. 1991, Schmidt et al. 2002), but not all calanoid copepods are negatively affected when feeding on them (Koski et al 2002, Kozlowsky-Suzuki et al. 2003). However, cyanobacteria are seen as a poor quality food source, containing low amounts of essential fatty acids (Brett and Muller-Navarra 1997). Climate alterations and potential effects on food web efficiency (Paper І, ІІ, ІІІ) In a climate change perspective, several factors will likely affect the ecosystems, where increased temperature should have a strong impact and increased river inflow, especially at higher latitudes, will increase the ratio between heterotrophy and autotrophy. A mesocosm experiment was set up in order to study how these two factors, i.e. increased temperature and increased ratio between heterotrophy and autotrophy, would affect food web efficiency in planktonic and benthic systems. We used metazooplankton as the highest pelagic trophic level and the amphipod Monoporeia affinis as the macrobenthic species. Two different temperatures; 5 and 10 C, and two different production systems; a phytoplankton-based and a bacteria-based one, were tested in a fully factorial design. 13

14 A temperature increase was found to enhance metazooplankton production and food web efficiency in the pelagic food webs (ІІ), whereas no difference was found in growth of the benthic amphipod, M. affinis, or in the pelagic-benthic food web efficiency (ІІІ). The direct effect of a temperature increase in the pelagic food webs is a higher metazooplankton production in relation to a stable basal production, resulting in higher food web efficiency (ІІ). However, indirect temperature effects such as a shift in the phytoplankton community (Andersson et al. 1994, HELCOM 2007, Sommer et al. 2007) will likely affect the food web efficiency both in the pelagic and pelagic-benthic food webs (ІІ, ІІІ). To what degree the pelagic food web efficiency will be affected depends on the metazooplankton species composition as well as the population structure of the calanoid copepods (ІІ), since calanoid copepods prefer food particles 2-5% of their prosome length (Berggren et al. 1988). A shift in the phytoplankton community to one dominated by smaller phytoplankton species should reduce the amount of food settling to the benthos (Smayda 1970, Andersson et al. 1994). This was however not observed, possibly due to the short water column in the mesocosms, resulting in most of the pelagic production sedimenting to the benthos (ІІІ). A shift to a higher ratio between heterotrophy and autotrophy resulted in lower food web efficiency both in the pelagic food webs (ІІ) and in the pelagic-benthic food webs (ІІІ). Energy (carbon) loss, in the form of faeces, exudates, respiration and sloppy feeding, occur between each trophic level, leading to more energy reaching higher trophic levels in the phytoplanktonbased food web compared to the bacteria-based food web since the latter includes more trophic levels (Sanders and Wickham 1993, Hessen 1998, Berglund et al. 2007). This probably explains the lower pelagic food web efficiency observed in the bacteria-based food web (ІІ). However, the expected increased freshwater input will reduce the salinity, favouring cladocerans over large neritic copepod species (Vuorinen et al. 1998) and as concluded in (І), cladocerans are important for efficient carbon transfer in areas with a high ratio between heterotrophy and autotrophy. Thus, the reduction in food web efficiency due to an increase in heterotrophy might be partly counteracted by such a change in food web structure. The lower pelagic-benthic food web efficiency in the bacteria-based food web reported in (ІІІ) can be attributed to lower sedimentation rate of bacteria compared to phytoplankton (Smayda 1970) and / or to lower food quality of bacteria compared to phytoplankton. Various phytoplankton groups contain storage lipids such as triacylglycerides and other hydrocarbons, while bacteria do not store lipids at all (Larsson et al. 2000). In addition, most phytoplankton groups contain different amounts of essential fatty acids, whereas bacteria generally lack these fatty acids (Nichols and McMeekin 2002). These fatty acids are also important for zooplankton; polyunsaturated fatty acids are for example known to enhance growth and egg production in cladocerans and copepods (Persson and Vrede 2006). The reduced individual weight of both calanoid copepods (ІІ) and M.affinis (ІІІ) in the bacteria-based food web is most likely due to a low amount of lipids and important fatty acids in the food source. Thus, the food quality for both the benthos and the zooplankton will be reduced in a climate altered food web. 14

15 Life strategy in a dominant Baltic Sea calanoid copepod, Limnocalanus macrurus (Paper І, ІV) The calanoid copepod Limnocalanus macrurus is a brackish water species with a large spatial distribution (Hutchinson 1967, Carter et al. 1980, Roff et al. 1981, Vanderploeg et al. 1998) and is the dominant zooplankton species in the Bothnian Bay and Bothnian Sea during most part of the year (І). L. macrurus is an omnivore (Warren 1985) and is known to store and utilize lipids, mainly in the form of wax esters (Vanderploeg et al. 1998). When estimating the carbon transfer efficiency in study (І), it was assumed that the zooplankton were utilizing the available food sources. However, since L. macrurus utilizes lipids during parts of the year it is likely that this species is more independent of the available food sources during certain seasons. A one year field study was performed in order to estimate how seasonal lipid utilization would impact my previous results. Energy status, feeding and food composition in relation to population structure was determined by combining traditional techniques with state-of-the-art molecular techniques. L. macrurus in the Bothnian Bay was carnivorous, feeding on other copepods and possibly also on its own species, during most of the year and switched to herbivory in July when phytoplankton reached peak abundance (ІV). Furthermore, a flagellate belonging to the group Kinetoplastida was found in our DNA-samples in spring and late summer, but it is not clear whether this was prey or a parasite. The seasonal variation in wax ester concentration was relatively large, with the lowest concentrations found in spring and the highest in fall. Since much of the wax esters were utilized during winter it appeared as if they had been used for reproduction since nauplii abundance peaked in April. Furthermore, the size of the largest oocyte, representative of reproductive state, never reached the size of a mature egg (Mauchline 1998) and we thus concluded that the reproduction took place somewhere between December and April, when the ice situation stopped sampling (ІV). Since the main utilization of lipid reserves was occurring during winter (ІV), the estimated summer carbon transfer efficiency in (І) is not affected by the lipid utilization exerted by the dominant copepod L. macrurus. However, lipid utilization is an important aspect that needs to be acknowledged when estimating the carbon transfer efficiency. Figure 3. Limnocalanus macrurus with a large oil sac. 15

16 Concluding remarks In this thesis I present results showing that the energy flow between trophic levels is dependent on factors such as the ratio between heterotrophy and autotrophy, the relationship between cladocerans and copepods and the size distribution and community structure of phytoplankton and zooplankton (І). However, when estimating the carbon transfer between trophic levels one has to keep in mind that some zooplankton, e.g. Limnocalanus macrurus, utilizes lipid reserves during parts of the year and probably do not feed on lower trophic levels during that time (ІV). In a climate change perspective, many factors will influence the dynamics of the ecosystem. In my thesis I show that increased temperature may have a positive effect on the pelagic food web efficiency (ІІ) and an increased ratio between heterotrophy and autotrophy will have a negative effect on both the pelagic food web efficiency (ІІ) and the pelagic-benthic food web efficiency (ІІІ). Furthermore, the food quality of zooplankton and the benthic amphipod Monoporeia affinis will decrease with an increase in heterotrophy (ІІ, ІІІ), possibly having implications for higher trophic levels, such as fish. Acknowledgements The research presented in this thesis was supported by grants from Umeå Marine Sciences Center, the Swedish Research Council for Environment, Agricultural and Spatial Planning and the Kempe Foundation. Thanks to Ulf, Agneta, Jenny and Nina for valuable comments on earlier versions of this thesis. 16

17 References Ahlgren G, Lundstedt L, Brett M, Forsberg C (1990) Lipid-composition and food quality of some fresh-water phytoplankton for cladoceran zooplankters. J. Plankton Res., 12, Ahlgren G, Gustafson IB, Boberg M (1992) Fatty-acid content and chemicalcomposition of fresh-water microalgae. J. Phycol., 28, Andersson A, Haecky P, Hagström A (1994) Effect of temperature and light on the growth of micro-plankton, nano-plankton and pico-plankton impact on algal succession. Mar. Biol., 120, Andersson A, Hajdu S, Haecky P (1996) Succession and growth limitation of phytoplankton in the Gulf of Bothnia (Baltic Sea). Mar. Biol., 126, Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser., 10, Berglund J, Müren U, Båmstedt U, Andersson A (2007) Efficiency of a phytoplankton-based and a bacteria-based food web in a pelagic marine system. Limnol. Oceanogr., 52, Berggren U, Hansen B, Kiørboe T (1988) Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: Implications for determination of copepod production. Mar. Biol., 99, Bergström S, Carlsson B, Gardelin M, Lindström G, Pettersson A, Rummukainen M (2001) Climate change impacts on run-off in Sweden assessment by global climate models, dynamical downscaling and hydrological modelling. Clim. Res., 16, Brett MT (1993b) Resource quality effects on Daphnia longispina maternal and neonate fitness. J. Plankton Res., 15, Brett MT and Muller-Navarra DC (1997) The role of highly unsaturated fatty acids in aquatic food processes. Freshw. Biol., 38, Buchanan JB (1993) Evidence of benthic pelagic coupling at a station off the Northumberland coast. J. Exp. Mar. Biol. Ecol., 172, 1-10 Carter JCH, Dadswell MJ, Roff JC, Sprules WG (1980) Distribution and zoogeography of planktonic crustaceans and dipterans in glaciated eastern North America. Can. J. Zool., 58, DeMott WR, Zhang QX, Carmichael WW (1991) Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and 3 species of Daphnia. Limnol. Oceanogr., 36, Dippner JW, Kornilovs G, Sidrevics L (2000) Long-term variability of mesozooplankton in the central Baltic Sea. J. Mar. Syst., 25, Dippner JW, Hanninen J, Kuosa H, Vuorinen I (2001) The influence of climate variability on zooplankton abundance in the Northern Baltic Archipelago Sea (SW Finland). ICES J. Mar. Sci., 58, Elken J, Trozinska A, Lysiak-Pastuszak E, Omstedt A, Lass HU (1996) Third Periodic Assessment of the State of the Marine Environment of the Baltic Sea, ; Background Document 64B. Baltic Marine Environment Protection Commission Helsinki Commission. 17

18 Elmgren R and Hill C (1997) Ecosystem function at low biodiversity the Baltic example. In: Ormond RFG, Gage JD, Angel MV (ed), Marine biodiversity. Patterns and processes. Cambridge University Press, Cambridge, pp Fuhrman JA and Azam F (1982) Thymidine incorporation as a measure of heterotrophic bacterioplankton productivity in marine surface waters: Evaluation and field results. Mar. Biol., 66, Gargas E (1975) A manual for phytoplankton primary production studies in the Baltic. The Baltic Marine Biologists, Publication No. 2, The Danish Agency of Environmental Protection, Hørsholm Gillooly J, Charnov E, West G, Savage V, Brown J (2002) Effects of size and temperature on developmental time. Nature, 417, Graneli E, Wallstrom K, Larsson U (1990) Nutrient limitation of primary production in the Baltic Sea area. Ambio, 19, Gulati RD and Doornekamp A (1991) The spring-time abundance and feeding of Eurytemora affinis (Poppe) in Volkerak-Zoommeer, a newly-created freshwater lake system in the Rhine delta (the Netherlands). Hydrobiol. Bull., 25, Hakanson JL (1984) The long and short-term feeding condition in fieldcaught Calanus pacificus, as determined from the lipid content. Limnol. Oceanogr., 29, Hagen W and Auel H (2001) Seasonal adaptations and the role of lipids in oceanic zooplankton, review article. Zool., 104, Heinle DR and Flemer DA (1975) Carbon requirements of a population of the estuarine copepod Eurytemora affinis. Mar. Biol., 31, HELCOM (1990) Second Periodic Assessment of the State of the Marine Environment of the Baltic Sea, ; Background Document. Balt. Sea Environ. Proc. No. 35b, pp HELCOM (2007) Climate Change in the Baltic Sea Area HELCOM Thematic Assessment in Balt. Sea. Environ. Proc. No. 111, pp.1-54 Hessen DO (1985a) The relation between bacterial carbon and dissolved humic compounds in oligotrophic lakes. FEMS (Fed.Eur.Microbiol.Soc.) Microb. Ecol., 31, Hessen DO (1998) Food webs and carbon cycling in humic lakes. In: Hessen DO, Tranvik L (ed), Aquatic humic substances; ecology and biogeochemistry. Springer-Verlag, Heidelberg, pp Hoppe HG, Breithaupt P, Walther K, Koppe R, Bleck S, Sommer U, Jürgens K (2008) Climate warming in winter affects the coupling between phytoplankton and bacteria during the spring bloom: a mesocosm study. Aquat. Microb. Ecol., 51, Hutchinson GE (1967) A Treatise on Limnology, Volume 2, Introduction to lake biology and the limnoplankton. John Wiley and Sons, New York, USA. pp IPCC (2007) Climate change 2007: Synthesis report. Intergovernmental panel on climate change, fourth assessment report. Cambridge University Press, Cambridge, UK, and New York, NY, USA. pp Ikeda T, Torres JJ, Hernández-León S, Geiger SP (2000) Metabolism. In: Harris RP, Wiebe PH, Lenz J, Skjoldal HR, Huntley M (ed) ICES 18

19 Zooplankton Methodology Manual. Academic Press, San Diego, pp Johnson RK and Wiederholm T (1992) Pelagic-benthic coupling the importance of diatom interannual variability for population oscillations of Monoporeia affinis. Limnol. Oceanogr., 37, Josefson AB, Jensen JN, Ærtebjerg G (1993) The benthos community structure anomaly in the late 1970s and early 1980s a result of a major food pulse? J. Exp. Mar. Biol. Ecol., 172, Kattner G and Hagen W (1995) Polar herbivorous copepods different pathways in lipid biosynthesis. ICES J. Mar. Sci., 52, Kautsky L and Kautsky N (2000) The Bothnian Sea, including Bothnian Sea and Bothnian Bay. In: Sheppard CRC (ed) Seas at the millennium: An environmental evaluation. Elsevier Science, pp Kiørboe T (1993) Turbulence, phytoplankton cell size, and the structure of pelagic food webs. Adv. Mar. Biol., 29, 1-67 Kiørboe T and Nielsen TG (1994) Regulation of zooplankton biomass and production in a temperate, coastal ecosystem. 1. Copepods. Limnol. Oceanogr., 39, Koski M, Schmidt K, Engstrom-Ost J, Viitasalo M, Jonasdottir S, Repka S, Sivonen K (2002) Calanoid copepods feed and produce eggs in the presence of toxic cyanobacteria Nodularia spumigena. Limnol. Oceanogr., 47, Kozlowsky-Suzuki B, Karjalainen M, Lehtiniemi M, Engstrom-Ost J, Koski M, Carlsson P (2003) Feeding, reproduction and toxin accumulation by the copepods Acartia bifilosa and Eurytemora affinis in the presence of the toxic cyanobacterium Nodularia spumigena. Mar. Ecol. Prog. Ser., 249, Larsson P, Andersson A, Broman D, Nordbäck J, Lundberg E (2000) Persistent organic pollutants (POPs) in pelagic systems. Ambio, 29, Legendre L and Rassoulzadegan F (1995) Plankton and nutrient dynamics in marine waters. Ophelia, 41, Lima ID, Olson DB, Doney SC (2002) Intrinsic dynamics and stability properties of size-structured pelagic ecosystem models. J. Plankton Res., 24, Liu H and Dagg M (2003) Interactions between nutrients, phytoplankton growth, and micro- and mesozooplankton grazing in the plume of the Mississippi River. Mar. Ecol. Prog. Ser., 258, Mauchline J (1998) The biology of calanoid copepods. Adv. Mar. Biol., 33, Meier HEM (2006) Baltic Sea climate in the late twenty-first century: a dynamical downscaling approach using two global models and two emission scenarios. Clim. dynam., 27, Moran MA and Hodson RE (1990) Bacterial productivity on humic and nonhumic components of dissolved organic-carbon. Limnol. Oceanogr., 35, Müren U, Berglund J, Samuelsson K, Andersson A (2005) Potential effects of elevated sea-water temperature on pelagic food webs. Hydrobiologia, 545,

20 Nejstgaard JC, Båmstedt U, Bagoien E (1995) Algal constraints on copepod grazing growth-state, toxicity, cell-size, and season as regulating factors. ICES J. Mar. Sci., 52, Nichols DS and McMeekin TA (2002) Biomarker techniques to screen for bacteria that produce polyunsaturated fatty acids. J. Microbiol. Methods, 48, Niilonen T (2002) Environment of the Baltic Sea area Balt. Sea Environ. Proc., No. 82B, Helsinki Commission, Helsinki, Finland, p. 215 Pace ML and Cole JJ (1996) Regulation of bacteria by resources and predation tested in whole-lake experiments. Limnol. Oceanogr., 41, Pasternak A, Arashkevich E, Tande K, Fakenhaug T (2001) Seasonal changes in feeding, gonad development and lipid stores in Calanus finmarchicus and C. hyperboreus from Malangen, northern Norway. Mar. Biol., 138, Pearson TH and Rosenberg R (1978) Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr. Mar. Biol. Ann. Rev., 16, Persson J and Vrede T (2006) Polyunsaturated fatty acids in zooplankton: variation due to taxonomy and trophic position. Freshw. Biol., 51, Riemann B and Christoffersen K (1993) Microbial trophodynamics in temperate lakes. Mar. Microb. Food Webs, 7, Roff JC, Sprules WG, Carter JCH, Dadswell MJ (1981) The structure of crustacean zooplankton communities in glaciated eastern northamerica. Can. J. Fish Aquat. Sci., 38, Samuelsson K, Berglund J, Andersson A (2006) Factors structuring the heterotrophic flagellate and ciliate community along a brackish water primary production gradient. J. Plankton Res., 28, Sandberg J, Andersson A, Johansson S (2004) Pelagic food web structure and carbon budget in the northern Baltic Sea: potential importance of terrigenous carbon. Mar. Ecol. Prog. Ser., 268, Sanders RW and Wickham SA (1993) Planktonic protozoa and metazoan: Predation, food quality and population control. Aquat. Microb. Ecol. [Mar. Microb. Food Webs], 7, Sargent JR and Henderson RJ (1986) Lipids. In: Corner EDS and O`Hara SCM (ed), The Biological Chemistry of Marine Copepods, Clarendon Press, Oxford, pp Schmidt K, Koski M, Engstrom-Ost J, Atkinson A (2002) Development of Baltic Sea zooplankton in the presence of a toxic cyanobacterium: a mesocosm approach. J. Plankton Res., 24, Sherr BF and Sherr EB (1984) Role of heterotrophic protozoa in carbon and energy flow in aquatic ecosystems. In: Klug MJ and Reddy CA (ed), Current Perspectives in Microbial Ecology. American Society for Microbiology, Washington DC, pp Sherr EB, Sherr BF, Paffenhofer G (1986) Phagotrophic protozoa as food for metazoans: A missing link in marine pelagic food webs? Mar. Microb. Food Webs, 1,

21 Smayda T (1970) The suspension and sinking of phytoplankton in the sea. Oceanogr. Mar. Biol. Ann. Rev., 8, Sommer U and Stibor H (2002) Copepoda-Cladocera-Tunicata: the role of three major mesozooplankton groups in pelagic food webs. Ecol. Res., 17, Sommer U, Stibor H, Katechakis A, Sommer F, Hansen T (2002) Pelagic food web configurations at different levels of nutrient richness and their implications for the ratio fish production:primary production. Hydrobiologia, 484, Sommer U, Aberle N, Engel A, Hansen T, Lengfellner K, Sandow M, Wohlers J, Zöllner E, Riebesell U (2007) An indoor mesocosm system to study the effect of climate change on the late winter and spring succession of Baltic Sea phyto- and zooplankton. Oecologia, 150, Stanley-Samuelson DW (1994b) The biological significance of prostaglandins and related eicosanoids in invertebrates. Am. Zool., 34, Uitto A and Hällfors S (1997) Grazing by mesozooplankton and metazoan microplankton on nanophytoplankton in a mesocosm experiment in the northern Baltic. J. Plankton Res., 19, Valiela I (1995) Marine ecological processes (second edition). Springer Verlag, New York, USA Vanderploeg HA, Cavaletto JF, Liebig JR, Gardner WS (1998) Limnocalanus macrurus (Copepoda: Calanoida) retains a marine arctic lipid and life cycle strategy in Lake Michigan. J. Plankton Res., 20, Voipio A (ed) (1981) The Baltic Sea. Elsevier Oceanography series 30, Elsevier, Amsterdam Vuorinen I, Hänninen J, Viitasalo M, Helminen U, Kuosa H (1998) Proportion of copepod biomass declines with decreasing salinity in the Baltic Sea. ICES J. Mar. Sci., 55, Warren GJ (1985) Predaceous feeding habits of Limnocalanus macrurus. J. Plankton Res., 7, Wolfe GV and Steinke M (1996) Grazing-activated production of dimethyl sulphide (DMS) by two clones of Emiliania huxleyi. Limnol. Oceanogr., 41, Work K, Havens K, Sharfstein B, East T (2005) How important is bacterial carbon to planktonic grazers in a turbid, subtropical lake? J. Plankton Res., 27, Wulff F, Stigenbrandt A, Rahm L (1990) Nutrient dynamics of the Baltic Sea. Ambio, 19,

22 Populärvetenskaplig sammanfattning Hela 71 procent av jordens yta består av vatten, varav 97 procent i sin tur utgörs av rena marina system och resterande av antingen sötvatten eller brackvatten. Det som främst skiljer dessa system åt är salthalten, där den i marina system är cirka 35 promille och i sötvatten mindre än 0.3 promille. Brackvattensystem har en salthalt som ligger någonstans mellan sötvatten och marina vatten. Östersjön är ett typiskt brackvattensystem, där salthalten är cirka 8 promille i söder och cirka 2 promille i norr. Denna nord-sydliga gradient beror på att vatten med en hög salthalt periodvis flödar in i södra Östersjön medan en stor mängd sötvatten tillförs från mynnande vattendrag särskilt i de norra delarna. Östersjön är ett väldigt ungt hav vilket gör att det finns få rena brackvattenarter. Istället har marina arter och sötvattensarter fått anpassa sig till den rådande salthalten. Detta har bidragit till att Östersjön anses som en tuff miljö för organismer att överleva och föröka sig i, vilket återspeglar sig i det låga antalet arter som finns här. Det låga antalet arter gör dock detta system till en bra plats att studera flödet av energi (kol) mellan olika organismer. Energi transporteras mellan olika nivåer i näringsväven, genom att kol tas upp av celler eller genom att en organism äts av en annan. Dock så försvinner en del av kolet mellan dessa nivåer, bland annat genom att organismerna andas, utsöndrar sina exkrementer eller äter slafsigt så att en del av maten hamnar utanför munnen. Ju fler organismer som kolet ska transporteras via, desto mindre kol når de högsta nivåerna i näringsväven. Jag har i min avhandling studerat hur effektivt kolflödet är i Östersjön och vad som påverkar detta. Det är många miljömässiga variabler som ändras från norr till söder i Östersjön, däribland salthalten, vilket näringsämne som begränsar algtillväxt och antalet isfria dagar. Detta gör att algproduktionen ökar 10 gånger från norr till söder, medan bakterieproduktionen bara ökar 2 gånger i samma gradient. Jag visade att flödeseffektiviteten, dvs. mängden kol som transporteras mellan nivåerna, är som högst i Bottenhavet (området med mellanhög produktion) och lägst i Egentliga Östersjön (området med högst produktion). Faktorer som påverkar flödet av energi är hur stor andel bakterier jämfört med alger som finns och vilka djurplankton som dominerar. Vissa djurplankton kan äta bakterier direkt medan andra inte kan äta så små organismer utan behöver ytterligare nivåer i näringsäven innan kolet kan tas upp. Vilka alger som finns är också viktigt. Vissa alger kan exempelvis vara giftiga, vilket minskar kolflödet. Dessutom är storleksstrukturen på algsamhället och vilka djurplanktonarter som finns viktigt. Djurplanktonen kan föredra att äta vissa storlekar av alger, eller inte ha förmåga att äta annat än alger av en viss storlek. Med anledning av resultatet i den första studien ville jag studera hur flödet av energi kommer att påverkas av en eventuell klimatförändring, där temperaturen i vattnet samt andelen bakterier jämfört med andelen alger förväntas öka. För att testa detta så jämfördes två olika temperaturer och två olika typer av basföda, bakterier och alger. Resultaten visar att den direkta effekten av en ökad temperatur är en högre produktion av djurplankton och ett högre kolflöde mellan nivåerna i näringsvävarna i vattnet. 22

23 Klimatförändringen förväntas dock även ha indirekta temperatureffekter. Exempelvis har tidigare studier visat att algerna troligen kommer bli mindre och vissa algarter kommer att ersättas av andra arter. Hur detta kommer att påverka djurplanktonen beror till stor del på vilka arter av djurplankton som finns i vattnet och i vilket utvecklingsstadium de befinner sig i. Om algerna blir mindre kommer en lägre andel föda att nå de bottenlevande djuren, eftersom små organismer sjunker långsammare till botten än stora. En ökad andel bakterier kommer att minska kolflödet, både i vattnet och ner till djuren på botten. Dessutom kommer både djurplankton och den bottenlevande märlkräftan, Monoporeia affinis, att minska i vikt. En av de vanligaste djurplanktonen i norra Östersjön är hoppkräftan Limnocalanus macrurus. I den sista studien valde jag att studera denna art i detalj, genom att under en säsong undersöka vad den har ätit och hur mycket energi den har lagrat i kroppen. Jag använde mig av DNA-analyser för att undersöka vad som fanns i hoppkräftans mage. L. macrurus lagrar på sig energi under året och använder en stor del av denna energi under vintern, då den förökar sig. L. macrurus är en allätare som oftast lever på andra djurplankton. I juli, då det finns mycket alger föredrar den dock dessa. Jag såg även tendenser till att hoppkräftan eventuellt hade ett kannibalistiskt födosätt, dvs. ätit av sin egen art. 23

24 Tack! Nu har jag jobbat i 5 år med att skriva ett antal vetenskapliga artiklar, men den här delen är nog den svåraste. Det finns så otroligt många personer jag vill tacka och säga att jag tycker om. Men jag vill börja med att tacka mina handledare, Ulf och Agneta. Ulf, dig vill tacka för att jag har fått chansen att både göra ett exjobb och doktorera inom det område jag brinner mest för; marinbiologi. Dessutom har du varit väldigt öppensinnig och låtit mig utvecklas på mitt sätt. Jag vet att jag inte riktigt har följt planen som var utsatt för mig, men du har snarare tyckt att det var bra att jag har haft egna idéer. Att ha fått samarbeta med många olika personer har gjort att jag har lärt mig mycket och vuxit som person. Agneta, du har varit mer än en biträdande handledare för mig. Jag har verkligen uppskattat alla diskussioner och utmaningar och den entusiasm du visar för mina resultat. Tack! Personalen på UMF, stort tack för all hjälp och för att ni har sett till att det har varit värt att åka de där 4 milen för att komma till jobbet. Nina och Lars som har hjälp mig med MÅNGA figurer, Kattis för hjälpen med photoshop, Erik som fanns där i förvirringen kring syremätaren, alla på marin miljö (Amund, Anna, Johanna, Gun, Nina, Siv, Chatarina, Petra) för all hjälp både i fält och på labb och för att ni gjorde båtresorna (trots kuling) väldigt trevliga, jag kommer att sakna att vara ute på havet med er! Stort tack till Johanna för hjälpen (både i form av arbete och socialt umgänge) med zooplankton räkningarna. Torunn för den härliga norska person du är. Tack till alla doktorander på UMF; Ignacio, Rose, Robert och Richard för den avslappnade stämningen och speciellt till Peder och Anna för alla icke forskarrelaterade samtal och alla morgonkaffestunder. Båtfolket, dvs Erik, Mikael, Jonas, jag kommer att sakna att vara inpackad som en sardin på Lotty med er. Stort tack också för all hjälp på labb med att bygga ihop saker och se till att saker funkar som det ska. Ni är bäst! Janne, jag har verkligen uppskattat att få dyka med dig, du är en härlig människa och din entusiasm över att få syn på en grön fladdrande sak på botten har verkligen smittat av sig Tack Peter för all hjälp med ciliat, flagellat och bakterie-analyser! Alla jag har samarbetat med i Stockholm; Ulf, Susanna, tack för bra kommentarer på mitt första manus. The copepod girls (Towe, Elena, Claire och Hedvig), oj vilken givande vecka vi hade ihop; 2 artiklar och en väldans massa skoj! Ann-Kristin, jag har verkligen uppskattat vårt samarbete! Tack för att du tog så väl hand om mig i Stockholm, trots ögoninflammation mm. Tack till Bernt och Leif för all hjälp i fält, och för att jag blev så varmt välkommen (trots att jag kommer från Norrland). Tack till DNA-killarna i Norge; Bernt och Christofer. Jag vet att jag var jobbig med mina mail som kom tätare och tätare, men ni har gjort ett otroligt jobb och jag har uppskattat att jobba med er. 24