Download Productivity and carbon transfer in pelagic food webs

Productivity and carbon transfer in
pelagic food webs
in response to carbon, nutrients and light
Carolyn Faithfull
Department of Ecology and Environmental Science
Umeå University
Umeå 2011
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Copyright ©: Carolyn Faithfull
ISBN: 978-91-7459-191-0
Cover: Carolyn Faithfull
Printed by: Print and Media
Umeå, Sweden, 2011
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List of Papers
This thesis is a summary of the following papers, which will be referred to by
their roman numerals.
I.
II.
III.
IV.
C.L. Faithfull, A.-K. Bergström, T. Vrede. Effects of nutrients and
physical lake characteristics on bacterial and phytoplankton
production – a meta-analysis. Submitted manuscript.
C. L. Faithfull, M. Huss, T. Vrede and A.-K. Bergström (2011).
Bottom–up carbon subsidies and top–down predation pressure
interact to affect aquatic food web structure. Oikos, 120: 311–320.
C. L. Faithfull, M. Huss, T. Vrede J. Karlsson and A.-K. Bergström
Transfer of bacterial production based on labile carbon to higher
trophic levels in an oligotrophic pelagic system. Submitted
manuscript.
C.L. Faithfull, A. Wenzel, A.-K. Bergström, T. Vrede. Lower
bacterial production and phytoplankton edibility reduces
crustacean zooplankton biomass at low light. Manuscript.
Paper II is reproduced with permission from the publisher
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Table of Contents
Abstract
6
Introduction
7
Why are nutrients, carbon and light important for production in lakes?...... 7
Consequences of changes in bacterial and phytoplankton production for
higher trophic levels in pelagic food webs ........................................................... 8
Objectives of the thesis
11
Methods
12
Meta-analysis......................................................................................................... 12
Mesocosm experiments ......................................................................................... 13
The use of glucose as a labile carbon source ..................................................... 14
Stable isotopes........................................................................................................ 14
Major results and Discussion
15
Factors affecting the absolute rates of phytoplankton and bacterial
production............................................................................................................... 15
Factors affecting the relative rates of phytoplankton and bacterial
production............................................................................................................... 16
How do phytoplankton affect higher trophic levels? ....................................... 18
How does increased bacterial production affect higher trophic levels? ....... 19
The importance of the intermediate step from bacteria to zooplankton ...... 20
Interaction effects of YOY perch grazing and carbon (glucose) on the
pelagic food web .................................................................................................... 21
The effects of carbon (glucose) addition and increased bacterial production
on young-of-the-year fish biomass ..................................................................... 22
Conclusions
22
Acknowledgements
24
References
24
Thanks
32
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Abstract
Some of the major problems we face today are human induced changes to
the nitrogen (N), phosphorus (P) and carbon (C) cycles. Predicted increases in
rainfall and temperature due to climate change, may also increase dissolved
organic matter (DOM) inflows to freshwater ecosystems in the boreal zone. N,
P, C and light, are essential resources that most often limit phytoplankton (PPr)
and bacterial production (BP) in the pelagic zone of lakes. PPr and BP not only
constitute the total basal C resource for the pelagic aquatic food web, but also
influence ecosystem function and biogeochemical cycles.
In this thesis I studied how N, P, C and light affect the relative and absolute
rates of PPr and BP, along a wide latitudinal and trophic gradient using
published data, and in two in situ mesocosm experiments in a clear water
oligotrophic lake. In the experiments I manipulated bottom-up drivers of
production and top-down predation to examine how these factors interact to
affect pelagic food web structure and function.
The most important predictors of PPr globally (Paper I) were latitude, TN,
and lake shape. Latitude alone explained the most variation in areal (50%) and
volumetric (40%) PPr. In terms of nutrients PPr was primarily N-limited and
BP was P-limited. Therefore bacteria and phytoplankton were not directly
competing for nutrients. BP:PPr was mostly driven by PPr, therefore light, N,
temperature and other factors affecting PPr controlled this ratio. PPr was
positively correlated with temperature, but not BP, consequently, higher
temperatures may reduce BP:PPr and hence the amount of energy mobilised
through the microbial food web on a global scale.
In papers II and III interaction effects were found between C-additions and
top-down predation by young-of-the-year (YOY) perch. Selective predation by
fish on copepods influenced the fate of labile C-addition, as rotifer biomass
increased with C-addition, but only when fish were absent. Interaction effects
between these top-down and bottom-up drivers were evident in middle of the
food web, which is seldom examined in this type of study. Although the energy
pathway from bacteria to higher consumers is generally longer than from
phytoplankton to higher trophic levels, increased BP still stimulated the
biomass of rotifers, calanoid copepods and YOY fish. However, this appeared to
be mediated by intermediate bacterial grazers such as flagellates and ciliates.
Light was an important driver of crustacean zooplankton biomass (paper
IV), but the light:nutrient hypothesis was inadequate to predict the mechanisms
behind the decrease in zooplankton biomass at low light. Instead, it appeared
that reduced edibility of the phytoplankton community under low light
conditions and reduced BP most strongly affected zooplankton biomass. Thus,
the LNH may not apply in oligotrophic lakes where PPr is primarily N-limited,
Daphnia is rare or absent and mixotrophic phytoplankton are abundant.
N, P, C and light manipulations have very different effects on different parts
of the pelagic food web. They influence the relative rates of PPr and BP, affect
phytoplankton community composition, alter the biomass of higher trophic
levels and change pathways of energy transfer through the pelagic food web.
This thesis adds valuable information as to how major changes in these
resources will affect food web structure and function under different
environmental conditions and future climate scenarios.
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Productivity and carbon transfer in pelagic food webs in
response to carbon, nutrients and light
Introduction
Why is carbon, nutrients and light important for production in
lakes?
One of the environmental problems we face today is the anthropogenic
alteration of the global biogeochemical cycles of nitrogen (N), phosphorus (P),
and carbon (C), which have increased in magnitude by c. 100%, c. 400%, and c.
13%, respectively, from pre-industrial levels (Falkowski et al. 2000).
Additionally, with future climate change and enhanced air temperatures, inputs
of terrestrial dissolved organic matter (DOM) to lakes is predicted to increase in
the boreal zone (Tranvik and Jansson 2002; Karlsson et al. 2005; Roulet and
Moore 2006). Hence, quantifying the combined effects of climate change and
alteration of biogeochemical cycles on DOM, nutrient (N, P, C) concentrations
and light availability, and how these changes in turn affect the microbial food
web and higher trophic levels in the pelagic zone of lakes, has become a major
subject of recent research (Carpenter et al. 2005; Cole et al. 2006; Karlsson et
al. 2009). In freshwater ecosystems N, P, and C, along with light availability are
essential resources that most often limit phytoplankton (PPr) (N, P, light) and
bacterial production (BP) (N, P, C) in the pelagic zone of lakes (Tranvik 1988;
Jones 1992; Elser et al. 2007). These elements are also structural components of
phospholipids (P and C), amino acids (N and C), carbohydrates (C), and nucleic
acids (C, N, and P), which are required by all organisms for survival and growth
(Sterner and Elser 2002). The relative and absolute rates of PPr and BP not only
constitute the total basal C resource for the pelagic aquatic food web (Fig. 1), but
also influence ecosystem function and biogeochemical cycles (del Giorgio and
Peters 1994; Jansson et al. 2007). Hence, it is important to describe and
understand what determines the production of bacteria and phytoplankton and
their relative proportions; especially with regard to how this affects energy and
nutrient transfer to higher trophic levels such as zooplankton and fish.
Like all photosynthetic organisms, light is essential for phytoplankton, and
planktonic PPr represents the autotrophic proportion of basal production in the
pelagic food web. Historically nutrient limitation of PPr has been considered to
be mainly driven by P availability in freshwater ecosystems (Schindler 1977).
However, this can differ along a gradient from oligotrophic to eutrophic lakes
(Downing and McCauley 1992), across lake size (mean depth and area) (Kalff
2003), and along a gradient of atmospheric N deposition (Elser et al. 2009). In
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fact, N-limitation of PPr has been recorded in many areas (Downing and
McCauley 1992; Bergström and Jansson 2006; Abell et al. 2010). Additionally,
physical factors which have previously been found to affect PPr include latitude
and temperature (Vrede et al. 1999; Flanagan et al. 2003). PPr tends to decrease
with increasing latitude in northern hemisphere lakes (Håkanson and Boulion
2001; Flanagan et al. 2003). This pattern may be controlled by mean annual
temperature, variation in solar angle or photosynthetically active radiation
(PAR), terrestrial productivity or atmospheric N deposition rates (Campbell and
Aarup 1989; Håkanson and Boulion 2001; Bergström and Jansson 2006).
BP represents the heterotrophic portion of pelagic basal production (Jones
1992). It is generally acknowledged that when there is little terrestrial input of
C, BP can be regulated by the amount of internally produced C by
phytoplankton, as a by-product of photosynthesis (Kirchman 1994). Terrestrial
DOM, thus, functions as an external energy and C source for bacteria (Tranvik
1988). Additionally, due to the high affinity of bacteria for P they are good
competitors for P compared to phytoplankton (Mindl et al. 2005). However, due
to the high cell P content of bacteria they are often P-limited in natural systems
(Vadstein 2000), and, hence, produce less C per unit P than phytoplankton. The
availability of terrestrial DOM releases bacteria from dependence on
phytoplankton as a C and energy source, thus allowing them to outcompete
phytoplankton under oligotrophic conditions (Jansson 1998; Vadstein 2000).
Large amounts of C can be lost in bacterial respiration depending on the
bioavailability of the C resource and bacterial growth efficiency (McCallister and
del Giorgio 2008). It follows that enhanced DOM input to lakes may be
accompanied by a reduction in basal energy production, caused by decreased
PPr due to competition between bacterioplankton and phytoplankton for
limited inorganic nutrients or increased respiration by bacteria (Drakare 2002;
Jansson et al. 2003). Alternatively, DOM may serve as a subsidy for the food
web by increasing BP, without affecting PPr, thus supplementing basal energy
production and the pool of C available as energy for the pelagic food web
(Jansson et al. 2007).
Consequences of changes in bacterial and phytoplankton
production for higher trophic levels in pelagic food webs
From a bottom-up perspective, the strength by which external terrestrial C fuels
the pelagic food web will depend on the transfer of C via bacteria to higher
trophic levels (Fig. 1). This depends upon several factors, i.e., the magnitude of
BP (Karlsson et al. 2007), the feeding mode of grazers (Grey et al. 2001;
Persaud et al. 2009), and the number and strength of links in the food chain
(Hairston 1993; Karlsson et al. 2004). Thus, increased energy production at the
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base of the food web, either driven by increased PPr or BP on external Csources, is expected to increase the growth rates or biomass of higher trophic
levels (Legendre and Rassoulzadegan 1995; Work et al. 2005; De Laender et al.
2010). In turn, the fraction of bacterial or phytoplankton C that is transferred to
cladocerans and copepods appears to be proportional to the relative rates of BP
and PPr (i.e. the BP:PPr ratio) (Karlsson et al. 2007). Crustacean zooplankton
(i.e. copepods and cladocerans), which are the key link between basal
production and fish in the pelagic food web (Fig. 1), differ in their feeding mode
and size selectivity of prey.
Figure 1. A simplified pelagic food web model based on our experimental system.
Bacterial production is driven principally by terrestrial DOM, phytoplankton carbon (C)
exudates and phosphorus (P). Bacteria are consumed by mixotrophs, ciliates and
cladocerans, and bacterial-C can also end up in copepod and fish biomass via copepod
grazing on mixotrophs and ciliates. Light and nitrogen (N) are the primary drivers of
phytoplankton in this model, and phytoplankton are in turn grazed by cladocerans,
copepods and potentially some of the larger ciliate and rotifer taxa. Planktivorous fish
(young-of-the-year perch) preferentially graze on copepods but can also consume
cladocerans. Grey arrows are elemental fluxes, black arrows indicate predation and
arrow thickness indicates coupling strength between the different compartments. Parts
of the food web which each paper deals with are shown with grey boxes.
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Since copepods are inefficient grazers on small particles such as bacteria
(Zöllner et al. 2003), bacterial C must be transferred through the microbial food
web via protozoans, with associated energy losses at each additional trophic
level, to reach copepod consumers (Fig 1) (Jansson et al. 2007). In contrast,
bacterial C may be more efficiently transferred in food webs dominated by
cladocerans (and rotifers) that are able to feed directly on small particles. Thus,
we would expect the structure of the zooplankton community to affect how
efficiently bacterial C is transferred through the food web, as fewer trophic
levels would result in fewer opportunities for respiratory C losses (Pace and Cole
2000; Sommer and Sommer 2006). Increased BP may also affect the structure
of the zooplankton community, by increasing the biomass of bacterial grazers,
and increased BP:PPr tends to increase the average number of trophic levels in
the food web, due to small bacterial grazing protists becoming more abundant
(Berglund et al. 2007).
PPr is assumed to be more directly available for higher trophic levels than BP, as
many phytoplankton taxa fall within an edible size range for both cladocerans
and copepods (Cyr and Curtis 1999). Phytoplankton are also considered to be a
high quality food source compared to bacteria (with the notable exception of
cyanobacteria), as they contain essential fatty-acids and sterols required by
zooplankton, that bacterioplankton lack (Brett and Müller-Navarra 1997).
However, the quantity as well as the quality of PPr may change with
manipulations of light, nutrients and C. Light availability may not only affect the
magnitude of PPr, but also the C:nutrient ratio of phytoplankton cells, and
therefore the quality of phytoplankton as food for higher consumers. When light
availability is high, but nutrients are limiting, phytoplankton tend to have high
C:nutrient ratios, as the excess available C can be stored within phytoplankton
cells (Elser et al. 2003). Thus, phytoplankton are said to be stoichiometrically
flexible (flexible C:nutrient ratios). However, phytoplankton taxa can differ in
their stoichiometric flexibility, and some taxa may release excess C to help
maintain a relatively fixed stoichiometry (Obernosterer and Herndl 1995). The
stoichiometric flexibility of phytoplankton can lead to a mismatch between
producer supply and grazer demand for nutrients, as grazers such as metazooplankton have relatively fixed stoichiometric ratios compared to
phytoplankton (Hessen 1992). As a consequence of this, although
phytoplankton biomass may be high under high light conditions, the quality of
this biomass as a food source for higher trophic levels may be low due to high
C:nutrient ratios (Sterner et al. 1998). This can result in low consumer growth
rates and respiration of excess C (Hessen and Anderson 2008).
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Subsequently, changes in the absolute rates of PPr, BP, BP:PPr, and the
stoichiometry of this production may affect higher trophic levels, such as
flagellates, ciliates, rotifers, crustacean zooplankton and even planktivorous
young-of-the-year (YOY) fish in the pelagic food web. However, these bottomup effects on higher trophic levels may also be mediated by top-down affects by
consumers. For instance, selective predation by YOY perch (Perca fluviatilis) on
copepods may change C-transfer efficiency in the food web (Bertolo et al. 2000),
due to the ability of copepods to selectively graze on high quality prey. DOM
inflows and light intensity may also alter whole lake fish production, with the
pelagic food web becoming more important in DOM rich lakes (Karlsson et al.
2009). Little work has been conducted on the effects of BP and the BP:PPr ratio
on fish production, although studies from marine systems suggest that BP may
be an important C source for planktivorous fish depending on season (De
Laender et al. 2010).
Objectives of the thesis
This thesis consists of four papers (I–IV below) which focus on the effects of N,
P, C (glucose), DOM, and light intensity on the relative and absolute rates of PPr
and BP, and the subsequent consequences for higher trophic levels in pelagic
freshwater ecosystems. The aims of the four papers are as follows:
I
II
III
IV
To investigate how the relative and absolute rates of BP and PPr are
influenced by elemental (N, P and C) and physical (lake morphology,
latitude and temperature) factors in lakes along a wide latitudinal and
trophic gradient.
To test how the combined effects of a bottom-up C subsidy (glucose)
and top-down predation by YOY perch affect PPr and BP and the
pelagic community composition in an oligotrophic clear water lake.
To assess the relative influence of phytoplankton C and external C
sources on higher trophic levels.
To examine how N, P, C (glucose) and light manipulations affect the
quantity and nutritional quality of basal production, and in turn how
this influences crustacean zooplankton biomass in an oligotrophic
clear water lake.
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Methods
Data was collected from published studies for a meta-analysis (Paper I). Two
sets of mesocosm experiments using different food web configurations and
elemental manipulations were conducted in an oligotrophic clear water lake in
Northern Sweden (Papers II, III, IV).
Meta-analysis
To obtain an overview of how the absolute and relative rates of PPr and BP are
affected by light, nutrients and C along a latitudinal and trophic gradient,
published data was collected from field studies for 300 lake years and 249
independent experimental studies (Fig. 2).
Figure 2. World map showing locations of experimental studies and field studies
obtained from literature sources or by pers. comm. Reproduced from paper I.
In order to deal with the problem of multicollinearity for both our explanatory
and response variables, both multiple regression and hierarchical partitioning
methods were used. Hierarchical variance partitioning jointly considers all
possible models in a multiple regression data set, which allows the identification
of variables that are independently correlated with a response variable, even
when multicollinearity is present (Murray and Conner 2009). The field data was
analysed to determine how the explanatory variables (N, P, DOM, latitude,
temperature, lake morphology) influenced areal and volumetric BP, PPr and
BP:PPr ratios. Areal measurements take into account lake euphotic depth and
morphometry, thus, producing a water column average, whereas volumetric
measurements were taken in the epilimnion, but standardised for euphotic
depth/lake depth. For the experimental studies Hedge’s g (Lipsey and Wilson
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2001) was used as the effect size metric to compare and combine the treatment
effects. Positive effect sizes indicated a positive response to the treatment.
Mesocosm experiments
Mesocosm experiments are a half-way house between a controlled laboratory
environment and a natural ecosystem. The advantages of using mesocosms are
that they are in situ and should therefore be subject to the same conditions as
the lake, but can be manipulated with nutrient or C additions and shaded to
reduce incidence light (Petersen and Englund 2005). Treatments applied to
mesocosms can also be replicated to increase statistical power, which tends to
be costly and difficult with natural ecosystems (Carpenter 1989). Mesocosms
have been shown to represent ecological processes with reasonable accuracy
enabling these findings to be scaled up to natural systems (Spivak et al. 2011),
and in our own study we found the size of the experimental unit did not
systematically affect the experimental outcomes (Paper I). However, there are
also disadvantages to using mesocosms. Mesocosms have walls, enabling
periphyton growth, which can potentially change the structure of basal
production in the system (Schindler 1998; Petersen et al. 1999), and in our case
they were closed at the bottom, preventing any sediment water interactions. For
our purpose, however, we required a system that could be replicated, was large
enough to include YOY fish, but to exclude predation on the fish, and contained
a natural pelagic planktonic community. In papers II and III we used large 18
m3 mesocosms, and crossed three levels of glucose addition and three levels of
YOY perch density in a full factorial design. This gave us 9 treatments, which
were applied in triplicate to the mesocosms. For the experiment in paper IV we
used smaller mesocosms (2.8 m3), and crossed glucose, inorganic N and
inorganic P addition with shading in a full factorial design to give 16 treatments,
replicated twice to give 32 mesocosms.
The first experiment in the large mesocosms ran for 45 d in summer 2007 and
was sampled before treatment addition and three times over the course of the
experiment. A natural pelagic community including all components of the food
web up to zooplankton was present at the start of the experiment. YOY perch
were added after the first sampling date and glucose was added twice a week for
the duration of the experiment. The second experiment using smaller
mesocosms ran for 22 d in summer 2009 and was sampled three times: before
treatment addition, after 7 d incubation with N, P, glucose and light
manipulations, then zooplankton were added at natural lake densities, and the
mesocosms were sampled again after a further 14 d incubation.
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In both experiments we had an ambitious sampling regime. In situ we measured
temperature, oxygen concentration and light intensity. Chemical parameters
such as dissolved inorganic, organic and particulate C, total, dissolved and
particulate N and P, and chlorophyll-a concentrations were measured. Sestonic
particulate N, P and C were size fractionated (>100 µm, 100-30 µm, 30-10 µm,
10-1.6 µm and <1.6 µm) for paper IV. Biomass and abundance of bacteria,
phytoplankton, flagellates, ciliates, rotifers and zooplankton taxa were obtained
using the Utermohl settling technique and standard counting methods. BP and
PPr were measured using the leucine (protein production in bacteria) and C14
(rate of C formation due to photosynthesis) isotope methods, respectively.
Stable isotope samples for dissolved inorganic C, particulate organic C, YOY
perch biomass, Bosmina sp., Holopedium gibberum and Eudiaptomus gracilis
were collected and measured for paper III.
The use of glucose as a labile carbon source
Natural DOM contains not only C, but also N, P and coloured substances that
reduce light availability for photosynthesis (Jansson 1998; Klug 2005). In
previous studies with natural DOM additions, it has been impossible to separate
the effects of nutrients, C and light on BP and PPr (Klug 2005; Berglund et al.
2007). In order to tease apart the mechanisms of terrestrial DOM effects, we
chose to focus on the effects of C subsidies alone on the pelagic food web for
papers II and III, and to manipulate N, P, C and light in a full-factorial design
for paper IV. Consequently, we used glucose as an alternative C source to DOM,
as it is readily bioavailable for bacterioplankton but has a negligible effect on
light and nutrient conditions. Obviously glucose is not a direct substitute for
DOM, as it is highly labile and terrestrial DOM varies greatly in bioavailability,
depending on age and source (Tranvik 1988; Berggren et al. 2009). However,
labile C is not an ecologically unimportant C source, as it is continually renewed
in the water column due to inflows of low molecular weight allochthonous C
(originating from terrestrial sources) (Berggren et al. 2010b), or in lake
processes, such as photo-chemical degradation of allochthonous C (Jones 1992;
Moran and Zepp 1997), phytoplankton extracellular C release (Sundh and Bell
1992) or enzymatic degradation of complex DOM molecules (Docherty et al.
2006).
Stable isotopes
In paper III we used the distinct stable isotopic signature of glucose compared
to natural C sources to determine the fraction of bacterial C transferred to
cladocerans, copepods and YOY perch. Measuring stable isotopes of C and N has
become a popular method to trace energy flows through food webs, and glucose
is δ13C enriched (δ13C = -11.6‰) compared to natural organic C sources (δ13C =14
27 to -43‰) found in Northern Swedish lakes (Karlsson et al. 2003). By
comparing the δ13C signals of zooplankton taxa and YOY perch in treatments
with and without glucose addition we could calculate the amount of bodily C in
these taxa originating from glucose. Because glucose was undetectable in the
mesocosms after addition and BP was stimulated by glucose addition, we
assumed that all glucose ending up in higher trophic levels was transferred
through bacteria. We used δ15N and a trophic fractionation constant of 3.4‰
(Post 2002) to calculate the trophic levels of cladocerans, copepods and YOY
fish.
Major results and Discussion
Factors affecting the absolute rates of phytoplankton and bacterial
production
The most important predictors of areal and volumetric PPr globally (Paper I)
were latitude, TN, and lake shape. Latitude alone explained the most variation
in areal (50%) and volumetric (40%) PPr. Much of this variation was accounted
for by temperature, as latitude became important when we excluded
temperature from the models. PPr can vary with many factors that are
correlated with latitude i.e., mean annual temperature, variation in solar angle
or photosynthetically active radiation (PAR), terrestrial productivity or
atmospheric N deposition rates (Campbell and Aarup 1989; Håkanson and
Boulion 2001; Bergström and Jansson 2006). The combination of these factors
into the single variable latitude probably gave latitude such a high predictive
power for PPr. TN was also an important predictor of areal (15%) and
volumetric PPr (29%). Research has shown that in areas with low atmospheric
N deposition (such as at high latitudes) N strongly limits PPr, especially in
unproductive lakes (Vitousek and Howarth 1991; Bergström and Jansson 2006;
Elser et al. 2009). In the experimental meta-analysis and in paper IV we also
found that PPr was most strongly N-limited. Positive synergistic effects of
combined N- and P-addition on PPr were evident in the nutrient enrichment
experiments, since single enrichment of either N or P likely induces limitation
by the other element (Elser et al. 2007; Bergström et al. 2008).
DOM concentrations can negatively influence PPr (Paper I) (Jansson et al.
2003). However this varied greatly, as the experimental meta-analysis showed a
positive effect of DOM on volumetric PPr, and volumetric PPr in the field data
set was unaffected by DOM. One explanation for this is that DOM reduced light
levels for photosynthesis in lakes (Jones 1992), but not in the experiments.
Generally all the experiments used in the meta-analysis kept light intensities
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constant, but the experiments that had the lowest PPr and highest BP:PPr
reduced light levels (Berglund et al. 2007). In paper IV we reduced the average
incidence light at 1 m depth in the mesocosms from 91.7 to 58.0 µmol m-2 s-1,
but this had no effect on the magnitude of PPr. Instead the phytoplankton
community shifted towards golden algae (Dinobryon sp.) and dinoflagellates
(gymnoids), which have pigmentation better adapted to low light conditions
(Johnsen and Sakshaug 1996), the ability to migrate within the water column to
reach optimal light intensities (Clegg et al. 2003) and can even ingest bacteria as
an alternative energy source, thus, outcompeting obligate phototrophs at low
light intensities (Bird and Kalff 1987; Hitchman and Jones 2000; Floder et al.
2006).
The main determinant of volumetric BP and areal BP across the field data set,
the meta-analysis of experimental studies and in paper IV was P. This reflects
earlier studies that have shown bacteria are most often P-limited (Vrede et al.
1999; Vadstein 2000). DOM was positively correlated with BP in the field and
experimental studies, and with both areal and volumetric BP, as has been well
documented in the literature for temperate lakes (Tranvik 1988; Jones 1992). In
papers I, II and III, glucose addition increased BP, although this increase was
not significant in paper IV. N-addition had no effect on BP. Volumetric rates of
BP were positively correlated with PPr along a wide trophic gradient (Paper I),
and bacteria also appeared to depend on phytoplankton as a C source in paper
IV. In paper IV BP was lower at low light levels, which could have been due to a
decrease in autochthonous C release by phytoplankton, which is an important C
substrate for bacterial growth (Baines and Pace 1991).
Factors affecting the relative rates of phytoplankton and bacterial
production
In the meta-analysis (Paper I) glucose addition did not negatively affect PPr as
we might expect if bacteria and phytoplankton are competing for nutrients and
bacteria are no longer dependant on phytoplankton as a C source. This coupled
with the fact that PPr did not change with glucose addition in papers II or IV
(Fig. 3), suggests that we cannot generalize that bacteria outcompete
phytoplankton for nutrients when there is an external C source. Indeed in
papers I and IV BP and PPr were P and N limited respectively and therefore do
not appear to be competing for the same limiting nutrient (Fig. 3). Alternatively,
it appears that other properties of the system, such as trophic state (Jones
1992), nutrient stoichiometry (Danger et al. 2007), light limitation (Jones 1992)
and the proportions of autotrophic and mixotrophic phytoplankton biomass
(Bergström et al. 2003) may regulate the interactions between PPr and BP.
16
Although positive relationships between BP and temperature have been found
in the laboratory and across natural systems (White et al. 1991), this
relationship was not evident in the experimental studies or the field data set
(Paper I). Other studies have found that BP still occurs at very low temperatures
(<10–4ºC), and temperature only tends to limit BP when other factors such as
nutrient and C concentrations are not limiting (Laybourn-Parry et al. 2004;
Berggren et al. 2010a).
Figure 3. Changes in elemental
additions (± 1SE) of carbon (C),
nitrogen (N), phosphorus (P) and
shading (S) combined (n=16), for a)
phytoplankton production (PPr), b)
bacterial production (BP) and c) the
BP:PPr ratio. Initial measurements and
after 6 and 22 d incubation are shown.
Stars indicate treatment additions that
were significantly different (p < 0.05)
from mesocosms without that treatment
addition according to the ANOVA
results. Modified from paper IV.
Increased bacterial respiration relative to BP has been found when
manipulating temperature in the laboratory, however, bacterial communities in
situ tend to be adapted to in situ conditions, and this adaptation may occur
within days (Adams et al. 2010; Berggren et al. 2010a). Consequently, it seems
unlikely that BP will increase relative to PPr during climate warming, due to
rapid adaptation of the bacterial community. Given the positive relationship
with PPr and temperature and the negative correlation with BP:PPr and
temperature found in paper I, one can predict that when considering lakes along
a wide trophic gradient, temperature increases due to climate change could
17
decrease the importance of energy mobilized through the microbial food web.
However, this finding probably only applies as a general pattern over a wide
trophic and latitudinal gradient, as for example, studies from the Baltic sea have
predicted that BP and therefore BP:PPr will increase with increased
temperature (Müren et al. 2005; Hoppe et al. 2008).
BP:PPr appears to be most strongly regulated by changes in PPr rather than
changes in BP (Paper I) (c.f. del Giorgio and Peters 1994), therefore at high
latitudes and low TN:TP ratios BP makes up a larger part of the available basal
production. This has been shown for oligotrophic lakes in low atmospheric Ndeposition areas in Northern Sweden (Karlsson et al. 2002; Bergström et al.
2003). Consequently, the microbial food web may be more important for energy
transfer to higher trophic levels at low TN:TP ratios and at high latitudes.
Additionally, we found that in experimental studies manipulating the BP:PPr
ratio, may be best done by changing factors that effect PPr, such as N
concentration, or light intensity (Papers I, IV).
How do phytoplankton affect higher trophic levels?
It is generally acknowledged that phytoplankton are high quality food for
zooplankton, and the ‘bread and butter’ of a zooplankton diet. However, many
phytoplankton taxa can become poor quality food if they are grown under high
light and low nutrient conditions according to the light:nutrient hypothesis
(LNH) (Sterner and Elser 2002; Elser et al. 2003). In this case zooplankton
growth can become nutrient limited, even though the biomass of phytoplankton
may be more than enough to meet their energy needs. In lower light conditions
phytoplankton may have lower C:nutrient ratios, but lower growth rates,
therefore zooplankton would tend to be energy limited (Sterner et al. 1997;
Sterner and Elser 2002). We tested the LNH in paper IV by manipulating light
levels and nutrient concentrations. We found that although seston C:P and C:N
(10–30 µm) ratios decreased somewhat in the lower light treatments, this had
no affect on zooplankton biomass. Indeed, edible C:P seston (0.7–30 µm) ratios
were already low before light manipulation in this experiment, and did not
change significantly with light manipulation as predicted by the LNH, possibly
due to the abundance of mixotrophs in the phytoplankton community
(Katechakis et al. 2005).
In fact zooplankton biomass was much lower in the shaded treatments, which
we would expect to be an effect of lowered PPr. However, PPr did not vary with
light. Instead, at low light levels the phytoplankton community shifted towards
species that are adapted to low light conditions, such as Dinobryon sp.
(Chrysophytes) and gymnoids (Dinoflagellates). Therefore, one of the
18
explanations we offer to explain this pattern is that the change in phytoplankton
species composition changed the edibility of the phytoplankton community.
Dinobryon sp. forms large branching colonies which may be an induced defense
against zooplankton grazing (Hessen and van Donk 1993), and the biomass of
gymnoids was negatively correlated with all zooplankton taxa biomasses (except
Bosmina). Some mixotrophs and other dinoflagellates have been found to be
toxic (Kubanek et al. 2007), or to employ behavioral defenses against
zooplankton grazing (Selander et al. 2011), thus, reducing energy transfer to
zooplankton when they are abundant (Katechakis et al. 2005). However, this
has not been documented so far for gymnoids in oligotrophic lakes. Therefore,
although food quality in terms of C:nutrient ratios appeared to be unimportant
for zooplankton in this experiment, phytoplankton community composition
might be an important food quality variable for zooplankton (Paper IV).
Another possible explanation for lower zooplankton biomass in shaded
treatments is reduced BP, which is discussed below.
How does increased bacterial production affect higher trophic
levels?
Changes in food web structure and function with glucose-C addition at first
seemed few and insignificant (Papers II, III, IV). Flagellate, ciliate, and most
crustacean zooplankton taxa biomasses were not affected by glucose addition.
This was hypothesised to be due to a large proportion of the glucose C being
respired by bacteria when C:nutrient ratios were high (Paper II) and bacterial
growth efficiency was low (Jansson et al. 2006). However, when fish were
absent, rotifer and calanoid copepod biomass increased with glucose addition
(Papers II, III). There was no direct relationship between rotifer or calanoid
biomass and BP or PPr. According to the stable isotope results in paper III,
cladocerans (Bosmina sp. and H. gibberum) consumed the most glucose (and
therefore BP), however, cladoceran biomass did not increase with increased BP.
Bosmina sp. and H. gibberum can incorporate bacterial C either directly
(Hessen 1985; Vaqué and Pace 1992) or indirectly through flagellate or small
ciliate grazing (DeMott and Kerfoot 1982; Persson 1985).
Calanoid copepod biomass increased with glucose addition (Paper III), even
though copepods cannot graze on small particles such as bacteria (Hansen et al.
1994; Burns and Schallenberg 1996). However, the enriched δ13C and δ15N
signals of calanoid copepods and YOY perch suggest that bacterial consumers
(i.e. flagellates and ciliates) were contributing to a proportion of their diet, thus,
acting as a conduit for nutrients and energy to higher trophic levels (Fig. 4).
Indeed, although calanoid copepod biomass was not correlated with an
increased incorporation of glucose C or BP, it was positively correlated with the
19
biomass of large ciliates (such as Strombilidium sp.). Thus, in glucose
treatments copepods may have been stimulated by increased availability of
bacterivorous ciliates, as ciliates may perform trophic upgrading i.e. de novo
synthesis of PUFA or preferentially retain rare nutrients (Klein Breteler et al.
1999; Bec and Desvilettes 2009).
and
δ15N
Figure
4.
δ13C
concentrations (mean ± 1 SE, n = 3
per treatment) for crustacean
zooplankton taxa and young-of-theyear (YOY) perch over three levels of
glucose addition, no addition (open
symbols), low (420 µg glucose-C L-1 )
addition (grey symbols) and high
(2100 µg C L-1) addition (black
symbols). Less negative δ13C values
represent more glucose incorporated
(through bacterial production), and
higher δ15N indicates higher trophic
position. Reproduced from paper
III.
In paper IV we also found evidence that increased BP had a positive effect on
crustacean zooplankton biomass. Zooplankton biomass and BP were lower in
shaded treatments. All zooplankton taxa (except for calanoid copepods) were
also positively correlated with BP. Although bacteria have high concentrations
of P and therefore zooplankton may offset P-limitation by bacterial grazing in
some taxa, this did not appear to be the case, as edible C:P seston ratios were
lower than C:P ratios previously reported that limit zooplankton growth
(Sterner and Elser 2002; Katechakis et al. 2005). Consequently, trophic
upgrading by intermediate trophic levels may also have been an important
mechanism for BP transfer to higher trophic levels in this experiment (Bec and
Desvilettes 2009).
The importance of the intermediate step from bacteria to
zooplankton
Bacteria do not contain polyunsaturated long chain fatty acids (PUFA) or sterols
that are essential to animals (Brett and Müller-Navarra 1997; Martin-Creuzburg
et al. 2005). Since a diet poor in PUFA results in slow growth and reproduction
of crustacean zooplankton (Brett et al. 2009), the growth of cladocerans in
paper III may at least have been partially determined by the availability of
PUFA and not only by the total amount of C available. Copepods may have been
stimulated by an increased availability of bacterivorous ciliates, as ciliates may
20
perform trophic upgrading (Klein Breteler et al. 1999). However, although
cladocerans can also consume bacterivorous flagellates and small ciliates, they
do not seem to benefit from bacterial based food to the same extent as copepods
in our experiments. This could be because the proportion of bacterial grazing
protists consumed by Bosmina sp. and H. gibberum were not sufficient to
improve the quality of the bacterial resource through trophic upgrading.
Bosmina sp. and H. gibberum are generally considered to be unselective grazers
with regard to food quality (Cyr and Curtis 1999; Hambright et al. 2007) and
therefore unlikely to selectively graze on high quality protists.
In contrast calanoid copepods are selective grazers and can discriminate
between poor and high quality food (Cowles et al. 1988; Burns and Schallenberg
2001). Alternatively, the bacterial grazing protists consumed by Bosmina sp.
and H. gibberum may not be as efficient trophic upgraders as the protists
consumed by calanoid copepods, as different species of protists differ in their
abilities to synthesise fatty acids (Klein Breteler et al. 1999; Bec et al. 2010).
Although the microbial pathway can possibly off-set biochemical limitation of
zooplankton growth, we suggest that this off-set may benefit different
zooplankton taxa depending on the abilities of their prey to improve food
quality and the ability of the zooplankton taxa to select prey. All zooplankton
taxa in paper IV appeared to benefit from increased BP, where nutrients were
also added in addition to glucose C to stimulate bottom-up production
(Karlsson et al. 2007). But this was not the case in papers II and III, where
glucose was added alone. Increased bacterial respiration due to decreased
bacterial growth efficiency during acute nutrient limitation (P) may limit the
amount of bacterial C that is transferred to higher trophic levels in papers II and
III (Jansson et al. 2006).
Interaction effects of YOY perch grazing and carbon (glucose) on
the pelagic food web
It has been argued previously that top-down and bottom-up forces (such as fish
grazing and labile-C addition, respectively) often have strong direct effects that
can become weaker with distance from the origin (McQueen et al. 1986; Brett
and Goldman 1997), especially in natural planktonic communities where
distinct trophic levels are difficult to define and omnivory is abundant (Persson
1999). Thus, in an experimental system where both top-down and bottom-up
factors are manipulated simultaneously, one could expect interaction effects to
become evident in the middle of the food web. This is exactly what was found in
paper II, as rotifers were the only taxa to exhibit a statistically significant
interaction between treatments, i.e., rotifer biomass increased with glucose
concentration, but only when fish were absent. Rotifers are located in the
21
middle of the food web, with crustacean zooplankton as potential predators
and/or competitors, and ciliates, flagellates, phytoplankton and
bacterioplankton as potential prey. However, in published studies interaction
effects are rare between top-down and bottom-up drivers (Brett and Goldman
1997; Gruner et al. 2008), but this may be an experimental artefact. Most
studies measure the response of the basal trophic level (bacteria and
phytoplankton) and the upper trophic levels (crustacean zooplankton and fish)
to bottom–up and top–down drivers without measuring the responses of the
trophic levels between these two extremes (but see Pace et al. 1998).
The effects of carbon (glucose) addition and increased bacterial
production on young-of-the-year fish biomass
BP differently affected YOY perch depending on fish stocking density. BP was
positively correlated with YOY perch survival and population growth rates at
high fish density, but negatively correlated with individual fish growth (Paper
III). This effect of bacteria appears to be an indirect bottom-up effect mediated
via the microbial food web, resulting in increased prey quality, as calanoid
copepods increased with glucose addition and are a favored prey of YOY perch
(Huss et al. 2007). Given density-dependent growth, increased fish survival can
in turn explain the lower individual growth rates observed with increasing BP at
high fish density, i.e., YOY perch were more resource limited when survival
rates were high (Persson et al. 2000). The availability of the favored prey (i.e.
calanoid copepods) appears to be the most important determinant of YOY perch
growth rate. However, given that BP only influenced fish survival and
population growth at high densities, it appears that the ‘quality effect’ of
resources only appears once preferred resources are limited.
Conclusions
Paper I shows that the rates of BP and PPr are often determined by different
drivers (i.e. BP by C and P and PPr by N and latitude), and this was consistent
across field and experimental studies. However, the ratio of BP:PPr is mostly
driven by changes in PPr, and is difficult to manipulate in experiments, as
volumetric BP is also positively correlated with PPr. PPr, but not BP was
positively correlated with temperature. Therefore increased temperatures and N
availability due to climate change could lead to higher PPr and lower BP:PPr,
potentially decreasing the importance of energy mobilized through the
microbial food web on a global scale. Few studies were available from Africa,
Asia and the tropics. Tropical systems may be particularly important, as the few
22
studies conducted suggest that resource limitation paradigms from northern
temperate lakes may not apply (Farjalla et al. 2009).
In paper II increased BP and top-down predation by YOY fish interacted to
affect the biomass of rotifers, which are located in the middle of the food web.
This study illustrates that top-down and bottom-up drivers may have
interacting effects that become evident in the middle of the food web, which are
often missed in studies where only changes in basal production and metazooplankton biomasses are considered.
Although increases in BP due to labile-C (glucose) addition (Paper III) did not
appear to directly affect crustacean zooplankton production, increased BP may
increase the growth rates or abundances of bacterial consuming protists, which
have the potential to transform bacterial C into a better quality food resource for
zooplankton. Consequently, increases in BP may fuel higher trophic levels when
intermediate grazers are present and are consumed by crustacean zooplankton.
Higher BP was associated with increased survival and population growth of YOY
perch when stocked at high densities, which suggested that BP had a density
dependant effect on fish growth. The role of ‘trophic upgraders’ in transferring
bacterial C to higher trophic levels may be important and requires further study
to determine the effects of environmental changes on the mechanisms and
ecological role of these taxa.
In Paper IV reduced light intensity decreased the biomass of crustacean
zooplankton. It was not possible to predict the mechanisms behind this result
using theory derived from the LNH. Instead changes in the rate of BP and the
edibility of the phytoplankton community composition at low light intensities
appeared to affect zooplankton biomass in this experiment. Thus, although the
LNH may be useful for hypothesis testing, it may be inadequate in predicting
the mechanisms behind changes in crustacean zooplankton biomass with
changes in light and nutrient availability in oligotrophic lakes, where PPr is
primarily N-limited, Daphnia is rare or absent and mixotrophic phytoplankton
are abundant. Instead, the mechanisms behind reduced edibility of the
phytoplankton community under low light conditions and the importance of
bacteria as an energy source for crustacean zooplankton requires further
investigation.
23
Acknowledgements
Many thanks to Ann-Kristin Bergström and Tobias Vrede for comments on this
thesis summary. The research in this thesis was conducted as part of the strong
research environment Lake Ecosystem Response to Environmental Change
(LEREC) and was supported by grants from the Wallenberg foundation, the
Göran Gustafsson foundation, the Kempe foundation and the Swedish Research
Council for Environmental and Spatial Planning (FORMAS).
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Thanks
Of course this thesis could not have been written without the help of quite a few
different people and my time as a PhD would definitely have not been the same
without the presence of a lot of different people.
Firstly thank you to Anki and Tobias, you have both been everything a PhD
could want in a supervisor, even to the point of being too helpful Tobias! I have
enjoyed all our discussions, fika and working with you both very much.
Especially I have to thank you for all the extra reading you have done in the last
month before the thesis was printed, unfortunately it ending up being a bit of a
sprint! Also thanks to Lennart, Mats, Janne, Göran, Sebastian, Jenny, Karin and
Christoph for helpful discussions and comments on various manuscripts.
Field work would not nearly have been as enjoyable, or have run as smoothly
(ha!), without the help of very many people: Mårten, Emma G, Blair, Daniel,
Jon, Tobias, Carola, Anna, Sara, Arne, Anneli and Elsa. Thank you so much!
You all did a great job, and often came to help at very short notice. Especially
huge thanks to Magnus, Anja and Peter, who all worked extremely hard, often to
exhaustion! (well maybe not Magnus…).
Ingrid Forsmark and Kerstin Lundholm are indispensible to most PhDs, Ingrid
found me somewhere to live when I first came here and tirelessly answered
questions about banking, Swedish ID numbers and cards, insurance, contracts
etc and has supplied many letters and certificates, to prove I really am here as a
PhD student and not trying to illegally migrate to Sweden (or?)
Many people have said that I was brave to come to Sweden, having no idea what
the people were like, the climate was like, or even exactly where it really was…
But maybe it was more hopeful optimism, that with 50 PhD students at the
department, there would be at least one or two that would be cool to hang out
with…. So thank you to all the oldies (Åsa B, Åsa G, Otilia, David, Jörgen, Ante,
Patrik, Mia, Carolina, Viktoria, Darius, Mahsa, Robert, Rickard, Fredrik, Martin
B, Tim, Henrik, Viktor, André etc.) and the newbies (Hélène, Wojciech, Eliza,
Lenka, Lovisa, Francisco, Marina, Sophia, Daniella, Joanna, Erik, Gustaf (phew,
there are so many of you!)), you have by far lived up to my expectations plus
some! Now, late at night, getting all sentimental I find myself thinking back to
all the stuff that has happened over the past five years…
To Karin for crazy dancing, skiing under the northern lights and being the best
office mate anyone could wish for. To Melanie for teaching allocation, long chats
(or rants), and in general keeping me sane. To my co-authors; Magnus for
refining my ideas into something better and Anja for working like a Trojan in
the lab and field. To Arne, Esther, Kristin, Anders, Tobias van K, Irina, Magnus,
Melanie, Karin, Anna D, Javier, Katie, Martin, Folmer, Otilia and Elina for ski
trips and Lotta and Gunnar for dragging me behind a snowmobile with skis (still
nothing has beat that yet in Sweden). To Emma G and her Grandma for
knitting, bread, berries and bears! To Pieter for giving us interesting stories to
tell, Christoph for beer, Martin for wine and yummy dinners, the post docs
32
(Genoveva, Andrea, Anouschka, Johanna, Helena, Kathrin, Larisa, Katie +
Micke) for not being old and boring (yet!), Anja, Kenyon, Owen and now
Daniella for keeping the pub alive, Toni for interesting trips abroad interspersed
with drinking and Very Important Research. Jenny for Papa D, yummy fikas
and Per for towing and car advice. And painting is no longer the same without
Melanie, Magnus and Martin’s inspiration. And to everyone who believes in
fika, bbqs and ‘potluck’ (as we say in NZ) dinners – how do you all get so good at
cooking?!
For some reason training has become important to me, so I have to thank
Kristin, Emma W, Elin F, Eva L, Agneta O, Peter, Andrea, Karin, coconut Erik,
Janne, Anna H, two Vårruset teams, ‘Darwin’s drängar’ and anyone else who
has managed to drag me out (or been dragged out) skiing, kayaking, running,
mountain biking, hiking, swimming or to iksu at some point. Anna Dietrich,
Barbara, Baz and Birte thanks for your ‘Kår’ work (you are appreciated!). To the
other Anna D for being totally unswedish, and to all the PhDs who have ever
said ‘YES!’ to teaching allocation (Good luck Eliza!). To Johan O, Ulla CG, Åsa
LO, Elisabeth, Tomas and Tommy, thank you for the chance to teach, and
learn... especially about plants, invertebrates, mushrooms and R, and the
quickest way to drill 64 holes in Pipparbölesjön.
Till Annika, Leif och Ante, ni har varit min adopterade familj i Sverige, och jag
hoppas ni kommer att forsätta att vara det för många år framöver!
To Mum and Dad, thank you for all your support in its many forms over the
years, and I hope one day I will convince you that climate change is real!
Michelle and Rex, thank you for all your emails, pictures, postcards and phone
calls, you make me so homesick – I guess that didn’t really help with thesis
writing, but at least it stops me from forgetting how wonderful NZ is and how
much I am missing. Thank you to Grandma and Grandad and Grandma and
Poppa for always asking about my research, and believing that I am doing
something good (even though I am hopeless at explaining what that good thing
might be)! I miss you all and can’t wait to see you in December.
And finally thanks to Peter, for always being there and always being yourself.
33