Effects of temperature and
terrestrial carbon on fish growth
and pelagic food web efficiency
Robert Lefébure
Department of Ecology and Environmental Science
Umeå University
901 87 Umeå
Umeå 2012
Copyright©Robert Lefébure
ISBN: 978-91-7459-412-6
Printed by: Print & Media
Umeå, Sweden 2012
2
To Annie
3
Men wanted for hazardous journey! Small wages, bitter cold, long months of complete
darkness, constant danger, safe return doubtful. Honor and recognition in case of success.
-
Sir Ernest Shackleton
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LIST OF PAPERS
This thesis is a summary and discussion of the following papers, which are referred to by their
roman numerals.
I.
Lefébure R., S. Larsson and P. Byström, 2011. A temperature dependent growth
model for the three-spined stickleback (Gasterosteus aculeatus), Journal of Fish
Biology, 79: 1815-1827
II.
Lefébure R., P. Byström and S. Larsson, 2012. Temperature and size dependent
attack rates of the three-spined stickleback (Gasterosteus aculeatus); are sticklebacks
in the Baltic Sea food-limited? (Submitted Manuscript)
III.
Degerman R., R.Lefébure, P. Byström, U. Båmstedt , S. Larsson, L-O. Eriksson and
A. Andersson, 2012. Bottom up and top down control of pelagic food web
efficiencies. (Manuscript)
IV.
Lefébure R, R.Degerman, P. Byström, S. Larsson, A. Andersson , L-O Eriksson and
U.Båmstedt, 2012. Impacts of elevated terrestrial nutrient loads and temperature on
pelagic food web efficiency and fish production. (Submitted Manuscript).
Paper I has been reprinted with kind permission from the publisher
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Table of Contents
ABSTRACT
7
INTRODUCTION
8
Effects of terrestrial carbon on planktonic food web dynamics
8
Effects of temperature on planktonic food webs
10
Physiological changes in fish in response to temperature
10
THE BALTIC SEA AND PREDICTED IMPACTS OF CLIMATE CHANGE
12
THE THREE - SPINED STICKLEBACK, GASTEROSTEUS ACULEATUS
13
AIM
14
MATERIALS AND METHODS
15
MAIN RESULTS
18
CONCLUSIONS
20
The thermal response of the three-spined stickleback; implications of climate change for sticklebacks in the
Baltic Sea
20
Impacts of climate change on pelagic food web structure and function; implications for fish production in
the Baltic Sea
21
THANKS
23
REFERENCES
24
AUTHOR CONTRIBUTIONS
28
6
ABSTRACT
Both temperature and terrestrial dissolved organic carbon (TDOC) have strong impacts on aquatic
food web dynamics and production. Temperature affects vital rates of all organisms and terrestrial
carbon has been shown to alter the dynamics of phytoplankton and bacterial production and affect the
trophic structure of planktonic food webs. As climate change predictions for the Baltic Sea suggests
future increases in both terrestrial carbon run-off and increases in temperature, the aim of thesis was to
adopt a system-ecological approach and study effects of these abiotic variables, not only on
interactions within planktonic food webs, but also on the growth and consumption rates of one of the
most common zooplanktivorous fish in the Baltic Sea, the three-spined stickleback Gasterosteus
aculeatus. Results showed that three-spined sticklebacks display a high degree of resilience against
increasing temperatures, as both growth rates as well as consumption rates on zooplankton were high
at temperatures well over 20 °C. Furthermore, it was shown that the minimal resource densities
required to sustain individual and population growth, actually decreased with increasing temperatures,
implying that sticklebacks around their optimum temperature for growth at 21 °C will actually have an
increased scope for growth. As stickleback population densities have increased over the last decade in
the Baltic Sea and are now suggested to out-compete other coastal fish species for shared zooplankton
resources, the results presented in this thesis suggest that increased water temperatures would only
serve to increase sticklebacks competitive advantage. As the structuring role of this small
zooplanktivore on pelagic communities might be considerable, further studies investigating
competitive interactions as well as patterns of population abundances are definitely warranted. TDOC
was overall shown to stimulate bacterial production and the microbial food web. Because of the longer
trophic pathways required to transport carbon from bacterial production to higher trophic levels, the
addition of TDOC always reduced food web transfer efficiency. However, it became apparent that the
full effect of TDOC additions on pelagic food webs was complex and depended heavily not only on
the existing trophic structure to which the carbon was introduced, but also on ambient temperature
levels. When three-spined sticklebacks were part of food webs with significant TDOC inputs, the
presence of fish, indirectly, through predator release of lower trophic levels, amplified the magnitude
of the effects of carbon addition on bacterial production, turning the base of the system significantly
more heterotrophic, which ultimately, impacted negatively on their own production. However, when a
pelagic food web containing sticklebacks was simultaneously subjected to realistic increases in
temperature and TDOC concentrations, food web efficiency and fish production increased compared
to present day conditions. These results were explained by a temperature dependent increased
production potential of zooplankton, sustained by an increased production of heterotropic
microzooplankton via TDOC additions, which lead to higher fish production. Although the increased
number of trophic linkages in heterotrophic food webs should have reduced energy transfer efficiency,
these negative effects seem here to have been overridden by the positive increases in zooplankton
production as a result of increased temperature. These results show that heterotrophic carbon transfer
can be a viable pathway to top-consumers, but also indicates that in order to understand the full effects
of climate change on trophic dynamics and fish production, abiotic variables cannot be studied in
isolation.
7
INTRODUCTION
Effects of terrestrial carbon on planktonic food web dynamics
Due to technological advances that allowed for the identification of microbes in marine
ecosystems, including viruses, bacteria, algae and heterotrophic protists (such as ciliates and
flagellates), the image of the pelagic food web (See Fig 1) has undergone drastic change in
recent decades. Initially, this compartment of the food web was called a “microbial loop”
(Pomeroy, 1974) while it has now become more customary to call it a “microbial food web”
to describe the combination of trophic interactions at this basal microbial level (Azam et al,
1983).
Fig. 1. Generalized view of the pelagic food web, including interactions on the microbial level and
their role in recycling DOC (Modified from Sommer et al, 2002).
Simplified, the microbial food web describes lower level trophic pathways in aquatic
environments and its main function is to recycle dissolved organic carbon (DOC) back into
higher levels of the food web via the incorporation of DOC into bacterial biomass. It has been
shown that bacteria are particularly efficient at assimilating this carbon, thanks chiefly to their
small size and large surface-to-volume ratio, which allows them to absorb nutrients at very
low concentrations (Vaccero et al, 1977; Larsson and Hagström, 1979). This gives them a
competitive advantage over phytoplankton and as a result promotes their production (Azam et
al, 1983). However, they are too small to be captured by mesozooplankton and planktonic
larvae. Instead, these cells are consumed by heterotrophic protists, such as flagellates and
8
ciliates, which in turn can be preyed upon by larger organisms and thus, DOC is made
available to higher levels of the food chain (Azam et al, 1983).
DOC in aquatic environments either derives from within the system or through the
transportation of organic matter from the terrestrial watershed, via rivers. Carbon of terrestrial
origin is labeled terrigenous dissolved organic carbon (TDOC) or allochtonous dissolved
organic carbon (ADOC), in contrast to DOC produced within the system; the autochthonous
supply (Eby, 2004). This in-situ carbon production can come from several sources, such as the
excretion of waste products by aquatic animals and microbes or by the breakdown and
dissolution of organic particles (Cole et al, 1982; Strom et al, 1997). The main autochtnonus
source of DOC production in the ocean is from photosynthetic algae (Cole et al, 1982).
During carbon fixation by algae undertaking photosynthesis, a fraction of carbon is released
as dissolved organic carbon (e.g. Larsson and Hagström, 1979; Wangersky, 2000). This
release goes on to be used by bacteria in the microbial loop (Larsson and Hagström, 1979;
Azam et al, 1983). As bacteria are efficient in assimilating carbon (Larsson and Hagström,
1979), the extracellular release by phytoplankton is considered to be one of the primary
sources for bacterial growth, with bacterial production values usually averaging about 20 % of
the total basal primary production (Cole et al, 1988).
The ability of bacteria to use carbon of terrestrial origin to supplement their growth was
initially overlooked, most likely because early concepts of aquatic microbial ecology arose
from research conducted on open oceans and not coastal or inland waters (Tranvik, 1992).
However, it is now accepted that humic riverine organic carbon contains readily available
carbon and that when a pelagic system is influenced by sources of terrestrial dissolved organic
carbon (TDOC), the microbial food web can play an increasingly larger role in determining
overall carbon production at the base of the food web, through bacterial heterotrophic
production (Tranvik 1988; Jansson et al, 2000; Jansson et al, 2007). In addition, it has been
shown that it can support growth of bacteria to such a degree that it can even uncouple them
from the need for autochthonous DOC from phytoplankton (Tranvik, 1992; Blomqvist et al,
2001; Sandberg et al, 2004; Berglund et al, 2007).
If a pelagic system is driven primarily by bacterial production, the carbon produced at the
base of the food web will have to pass through the entire microbial food web, chiefly
mediated by heterotrophic protists such as flagellates and ciliates, before reaching top
consumers (Azam et al, 1983; Breteler et al, 1999). The increase in food chain length
ultimately means that less energy is available for higher trophic levels, a consequence of a
loss of carbon of about 70 – 90 % at each additional step in the food web, due amongst other
things to respiration and sloppy feeding (Straile, 1997; Strom et al, 1997; Sommer et al,
2002). These food web dynamics are characterized and measured as food web efficiency or
ecological efficiency and is defined as the ratio between the productivity at the highest trophic
level and the productivity at the base level (Rand and Stewart, 1998). In a study estimating
food web efficiency in two contrasting food webs (one phytoplankton-based and one
bacterial-based) in the Baltic Sea, it was shown that the FWE was 22% in the phytoplanktonbased food web and 2% in the bacterial-based food web. This discrepancy was explained by
the 1–2 extra trophic levels in the bacterial-based food web through which carbon had to pass
(via flagellates and ciliates) before reaching mesozooplankton (Berglund et al, 2007).
In aquatic systems with high inputs of TDOC, other factors are of consequence for the
dynamics between bacterial and phytoplankton productivity. In the photic zone, the
relationship between phyto- and bacterioplankton is one of constant competition for inorganic
nutrients (Blomqvist et al, 2001). Because of their high uptake capacity for nutrients,
9
bacterioplankton are believed to triumph, and if present in sufficient numbers, might out
compete phytoplankton (Azam et al, 1983; Blomqvist et al, 2001). Furthermore, a major
share of TDOC is made up of coloured substances, decreasing light availability (and quality)
required for photosynthesis, which may lead to detrimental conditions for phytoplankton
(Klug et al, 2002). Thus, the potential effects of ADOC on primary producers and on
phytoplankton–bacterioplankton relationships are numerous, with increasing consensus being
built that organic carbon can indeed play an important role in determining the structure and
function of pelagic food webs (Blomqvist et al, 2001; Berglund et al, 2007; Jansson et al,
2007).
Effects of temperature on planktonic food webs
Temperature affects all levels of the pelagic food web due to its intrinsic role in all vital rates
of the food web organisms. At the base of the food web, temperature can influence ratios of
bacterial and phytoplankton growth, higher temperature favoring bacteria, therefore altering
the heterotrophic: autotrophic production ratio (Müren et al, 2005; Hoppe et al, 2008). With
increasing temperatures, the species composition of phytoplankton communities have also
been shown to change from a dominance of relatively large diatoms and dinoflagellates at low
temperatures to a dominance of small algae (pico- and nano-plankton) at higher temperatures
(Andersson et al, 1994). In addition, increased temperatures favour the productivity of
heterotrophic protists, like flagellates and ciliates, and at higher trophic levels both
development times and total biomass of zooplankton are affected (Heinle and Flemer 1975;
Dippner et al, 2000). Therefore, with increasing temperatures, a pelagic system can move in
increasing degrees towards heterotrophy, implying that moderately elevated seawater
temperatures may affect the entire ecosystem functioning by favoring bacterial productivity
and altering the balance between autotrophy and heterotrophy (Müren et al, 2005).
Physiological changes in fish in response to temperature
Of all the abitioc factors, changes in ambient water temperature has the largest effect on
physiological properties in fish (Brett, 1979). Since fish in general are ectotherms, increases
in ambient temperatures will lead to increases of their metabolic rates (Elliot, 1976) and these
will translate to a need to increase their consumption rates to meet these demands (Jobling,
1995). Therefore, temperature will have a strong impact on predator prey interactions as it
will affect all aspects of the predation cycle, including encounter rate, prey avoidance
capacity, capture success and handling time (Persson, 1986; Persson et al, 1998; Wahlström et
al, 2000; Englund et al, 2011).
Temperature will also affect all aspects of fish physiology and dictate fundamental properties
of the energy budget, metabolic demands, digestion rates and assimilation efficiencies
(Werner, 1994; Jobling, 1995; Persson et al, 1998; Byström et al, 2006; Englund et al, 2011).
Just as temperature affects consumption rates, growth rates of fish are intimately connected to
ambient temperature levels. For most fish species increases in growth rates with increasing
temperatures will be seen, up to a certain point, only to decline abruptly once the critical limit
10
of the species is reached (Brett 1979; Elliot, 1994; Jobling, 1995). The temperature peak at
which growth is maximized is called the “optimum temperature for growth” and is usually a
few degrees lower than the temperature at which food intake is the greatest. There are large
variations in the optimum temperature for growth between species. Many salmonids, for
instance, have their temperature optima in the range of 12 – 17 °C (e.g. Elliott and Hurley,
1995; Elliott and Hurley, 1997) in contrast to cyprinids which have optima of 20 °C or higher
(Jobling, 1995). In addition, ontogenetic intra-specific differences also exist, with juveniles
often having higher optima for growth than adults (Jobling, 1995). This shows that species are
adapted to different temperature tolerance ranges and that typically energy allocation towards
growth will decline once temperatures approach the range extremes (Brett, 1979). However,
patterns of growth are strongly correlated to the available food supply and restricted feeding
possibilities will have a marked influence on growth rates at any observed temperature.
Production E (P) = E( IN) – E (OUT)
The most detailed experimental studies on the effects of temperature and food ration on fish
growth have been carried out on salmonids, e.g. Atlantic salmon Salmo salar (Forseth et al,
2001), brown trout Salmon trutta (reviewed in Elliot, 1994) and Arctic charr Salvelinus
alpinus (Larsson and Berglund, 1998). These allow scientists to determine at which
temperature food conversion is the most efficient, whilst simultaneously allowing for
predictions of temperature related optimal growth at any given ratio level (Fig. 2).
4
3
2
1
Temperature (ºC)
Fig. 2. Influence of temperature on growth (production) of fish held under different conditions of food
restriction. (1) unlimited food supply, (2) slight restriction (3) moderate restriction and (4) low level of
food supply. The arrowheads indicate the temperatures at which growth rates will be greatest under the
different regimes. (Modified from Jobling, 1995).
Under conditions of limited food availability there will be marked changes in the relationship
between growth and temperature as opposed to under unrestricted food supply conditions. In
the latter scenario, increased temperature would lead to increased growth up to the optimum
and a subsequent decline towards a lethal point. However, if food is a limiting factor, a shift
of the optimum growth towards increasingly lower temperatures will be seen. This shift
11
occurs because higher temperatures lead to higher metabolic rates in fish, thereby increasing
their food demand as required to maintain a constant body weight, lessening their available
scope for growth (Elliot, 1976; Brett, 1979; Jobling, 1995). Therefore, at low food
allowances, it is more beneficial to be at low temperatures, where metabolism is low thus
leaving a greater surplus of energy available for growth. Inversely, at high temperatures with
low food availability, the high metabolic demands of the fish will lead to fish losing weight
and eventually starving to death (Brett et al, 1969; Elliot, 1976; Jobling, 1995).
As temperature influences rates of ingestion, metabolic rates and growth rates; increasing our
understanding of these physiological properties in fish becomes paramount if we are to
understand the effects of climate change, both at the individual (Elliot, 1994) and population
level (Ohlberger et al, 2001) and also the impacts on food web dynamics such as predatorprey interactions (Hairston and Hairston, 1993).
THE BALTIC SEA AND PREDICTED IMPACTS OF CLIMATE CHANGE
The Baltic Sea, with a surface area of 415 000 km2, is one of the largest and most studied
brackish water bodies in the world. The catchment area of the Baltic Sea covers 1.74 million
km2 and includes territory from a total of fourteen countries (HELCOM, 2007; Kautsky and
Kautsky, 2000). About 80% of the river runoff and 85% of the net precipitation enters through
the Gulf of Bothnia, northern Baltic Sea. Due to this gradient in fresh-water inflow the Baltic
Sea is commonly divided into three distinct basins, going from the Bothinan Bay in the north,
to the Bothnian Sea and finally the Baltic Proper in the south. This inflow controls the low
salinity of the Baltic Sea waters, which range from about 2 PSU (Practical Salinity Units) in
the northern Bay of Bothnia to about 10 PSU in the southern Baltic proper (Kautsky and
Kautsky, 2000). Additionally, the high fresh water inflow, water runoff from various
terrestrial environments, also explains between 71% and 97% of the variability in dissolved
nutrients (nitrogen, phosphorus, silicon) input, as well as concentrations of total organic and
inorganic carbon in the Baltic Sea (HELCOM, 2007).
Current climate change predictions for the northern Hemisphere suggest both an increase in
sea surface temperature of on average 4 °C and increased terrestrial nutrient runoff from
rivers due to increased annual levels of precipitation (Meier, 2006; HELCOM, 2007; IPCC,
2007). Consequently, the future environment of the Baltic Sea is predicted to look very
different from present conditions. These changes to ambient conditions will affect all levels of
the pelagic food web, altering conditions for bacteria and phytoplankton, as well as affecting
fish populations. In order to gain a better understanding of the effects of climate change on
pelagic food webs in the Baltic Sea, a system-ecological approach has therefore to be adopted,
where concurrent effects of temperature and DOC are studied on the planktonic food web,
zooplanktivorus fish and interaction effects these parts of the food web exert on each other.
12
THE THREE - SPINED STICKLEBACK, GASTEROSTEUS ACULEATUS
The typical stickleback is a small streamlined fish with a wide distribution in both marine and
fresh waters of the northern hemisphere (Wootton, 1984) (Fig 3). The typical adult
stickleback will reach about 11 cm in length and is distinguished by its bony armor with three
prominent dorsal spines, the first two of which are large, serrated and isolated from the dorsal
fin (Bell and Foster, 1994).
Fig. 3. Global distribution of the three-spined Stickleback (Gasterosteus aculeatus). Red areas indicate
higher relative likelihood of occurrence (Froese and Pauly, 2007).
Generally sticklebacks take 2-3 years to mature and experience only one breeding season
before dying (Wootton, 1984). As males come into reproductive condition, typically the eye
and body take on a blue tinge and the ventral surface of the head and trunk become red. The
stickleback males build a benthic nest where they care for the eggs by oxygenating them
whilst simultaneously protecting them from rival males. After the eggs are laid, the females
take no further part in rearing of the young (Bell and Foster, 1994). In the Baltic Sea, after the
spawning period, G. aculeatus migrate from the littoral spawning grounds into the open
ocean, this usually occurs around August-September (Lemmetyinen and Mankki, 1975).
Although it is one of the main planktivorous species in the Baltic Sea (Jurvelius et al,, 1996),
its ecological role has long been overlooked because of its lack of commercial importance.
However, three-spined stickleback dynamics and their role in the ecosystem, have received
recent attention since it has been suggested that population abundances have increased
substantially in the last decade (Ljunggren et al, 2010; Eriksson et al, 2011). This increase in
abundance has been attributed to a decrease in piscivours predators causing a predator release
scenario for small fish species such as three-spined stickleback (Ljunggren et al, 2010;
Eriksson et al, 2011). In addition, it has been suggested these increases have now led to
sticklebacks out-competing other coastal fish species for shared zooplankton resources
(Eriksson et al, 2009; Ljungren et al, 2010).
13
Even-though they are a well-studied fish species in both behavioural and evolutionary
ecological terms (Bell and Foster, 1994; Huntingford and Gomez, 2009), their function and
role in ecosystems is less well defined and important baseline parameters, such temperature
dependent growth and attack rates, remain unknown. As three-spined sticklebacks occupy
both in-shore and off-shore habitats of the entire Baltic Sea during their life cycle, coupled
with increasing population numbers, the establishment of baseline parameters for growth and
foraging capacity are clearly vital if we are to understand their full ecological role in the
Baltic Sea. In addition, due to their ecological relevance, wide distribution, general small size
and proven adaptability in laboratory environments they are ideal candidates for laboratory
investigations into effects of climate change in pelagic food webs (Bell and Foster, 1994).
AIM
The aims of this thesis were two-fold. Firstly, we set out to establish baseline parameters of
temperature and size dependent growth (Paper I) as well as foraging capacity for G. aculeatus
(Paper II). Once these had been established, a better understanding of the role of the
stickleback in the Baltic Sea, currently and in a future climate change scenario, would be
gained.
Secondly, we aimed to investigate the impacts of allochtonous dissolved organic carbon
(ADOC) on food web dynamics in a marine system to better elucidate patterns of carbon
transfer from the microbial food web to zooplanktivorous fish (Paper III). Finally, by building
on results from previous papers, we aimed to test the impact of terrestrial dissolved organic
carbon (TDOC) and temperature alteration, as predicted in relevant climate change scenarios,
on pelagic food web efficiency and fish production (Paper IV).
More specifically for each paper we wanted:
Paper I
- to parameterize a growth model describing the temperature dependent growth capacity
and range of G. aculeatus under unlimited food conditions. In addition, we wanted to
test whether growth rates measured using commercial pellets could be applied to more
natural conditions by investigating differences in growth potential between fish fed
invertebrate prey or pellets and finally, to investigate whether maximum growth
potential was dependent on seasonality.
Paper II
-
to first estimate the size and temperature dependent attack rates of the three-spined
stickleback through a series of laboratory experiments using the calanoid copepod
Eurytemora affinis as prey. Secondly, by using these estimates, literature data on size
and temperature dependent consumption capacities, metabolic rates and a time series
of zooplankton biomass for all three basins in the Baltic Sea, we wanted to investigate
past and present consumption rates and resource limitation thresholds which may have
supported the suggested increase in population abundances, as well as provide an
estimate of the critical resource density (CRD), i.e. the minimal resource density
required to sustain metabolic needs for this species.
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Paper III
-
to investigate the role of allochtonous dissolved organic carbon (ADOC) on pelagic
food web structure and efficiency. Currently, there is very little information available
on how ADOC influences aquatic systems beyond the planktonic food web, and the
interactive effects of an external carbon source and/or the addition of another trophic
level (top consumer) are poorly established. To this end, a full-factorial experiment
was set up in a large-scale mesocosm facility, with four treatments where food web
transfer efficiencies and production potentials were measured in pelagic systems
dominated by either bacteria or phytoplankton at the basal level and zooplankton or
fish (three-spined stickleback) as the top consumer.
Paper IV
-
to investigate the effects of natural TDOC, increased temperature and their combined
effect on ratios of heterotrophy/autotrophy and marine food web efficiency, in a
factorial large-scale mesocosm experiment. The aim was to measure pelagic food web
function and structure under predicted climate change scenarios and to contrast these
findings to present day conditions. More specifically we investigated the effects of
these environmental drivers on (i) ratios of bacterial and phytoplankton productivity
(ii) changes in species compositions and abundances in the food web (iii) impacts on
growth of zooplanktivorous fish and (iv) the effects on food web efficiency in the four
contrasting experimental treatments.
MATERIALS AND METHODS
For all experiments, G. aculeatus juveniles were collected with a beach seine from a coastal
area outside of Umea Marine Science Centre, in the Gulf of Bothnia, Sweden. Fish were then
kept in 400 l holding tanks at 10 °C with continuous water flow-through and fed daily with
commercial pellets or with a culture of Eurytemora affinis, a calanoid copepod common to the
area, depending on the experiment.
For papers I and II an indoor aquarium system was used (Fig. 4. A), built specifically to allow
for experiments on growth and consumption rates to be carried out at up seven different
experimental temperatures simultaneously. Fourteen aquaria (120 l) were arranged in
temperature control systems (2 aquaria per temperature) and supplied with partly re-circulated
20µm filtered sea water. In each aquarium, 5 smaller plastic tanks (5 l) or 2 larger tanks (10 l)
could be submerged. This allowed for either 10 fish per temperature to be reared singly during
the growth experiments (Paper I) or capture rates to be measured on 4 fish per temperature
(Paper II).
15
A
B
Fig. 4. A) Picture of the aquarium experimental facility. B) Picture of the indoor mesocosm facility at
Umeå Marine Science Centre
Fish were always initially placed at a neutral temperature common to all aquaria (15 °C). The
experimental temperatures were then obtained by increasing or decreasing the temperature by
approximately 1 °C h-1. During this acclimatisation phase, fish were always fed ad lib rations
of food. Once set to the desired temperature, electronic thermostats (Nobelektronik, Älmhult,
Sweden) were used to regulate water temperatures. Temperatures never fluctuated beyond
±0.5 °C from the set value. The plastic tanks were perforated to allow for constant water
exchange with the surrounding, temperature-controlled water in the aquaria. Light levels were
adjusted to a 12 h light/12 h dark photo period. To counteract potential effects of increasing
ammonium concentration and to replenish water lost by evaporation, 20 l of filtered (20 μm)
sea water was added daily to each temperature system. Aquarium air pumps supplied oxygen
to each 120 l aquaria tank.
In paper I, growth was measured on juvenile sticklebacks with a continuous supply of
commercial pellets as food. In addition, a growth study was conducted in the winter to test for
seasonal differences in growth patterns and also a study was done testing for differences in
growth rates between commercial pellets and invertebrate prey (chironomids). The different
growth trials lasted between 10-14 days.
In paper II, individual fish were placed singly in the 10 l tanks, and held at 15 °C. In order to
measure capture rates on zooplankton, fish were first kept at the experimental temperature for
24 hours and fed ad lib rations of zooplankton. Before the start of each feeding trial, fish were
then deprived of food for 24 h before experiments to standardize hunger level. At the start of
each trial, the desired zooplankton density was introduced from above and the water was
carefully stirred so that the zooplankton were evenly distributed. During this time fish were
kept in a small net to prevent them from feeding whilst zooplankton was being distributed in
the aquaria. Fish were then released from their enclosures and the trial started once the fish
had captured one E. affinis, and lasted until it had successfully captured three subsequent
prey. All experiments were carried out with one size class of E. affinis (0.7 mm ± 0.04, mean
± 1 SD), at 6 different prey densities (1, 2, 4, 8, 16 and 32 prey/l) and at 3 different
temperatures (15, 21 and 24 °C).
16
In papers III and IV, experiments were conducted at the Umeå Marine Research Centre indoor
mesocosm facility (Fig. 4. B). This facility consists of twelve polyethylen mesocosms, each
with a volume of 2000 l, a diameter of 73 cm and a depth of 5 m. These can be filled
simultaneously with unfiltered coastal water (5 PSU) from the northern Baltic Sea (63°34´N,
19°54´E) using a peristaltic pump system. By using unfiltered water, a natural assemblage of
all planktonic organisms is evenly distributed to the mesocoms, which can thereafter be
manipulated, either by altering ambient conditions, such as nutrients and temperature, or by
changing the food web structure, by adding zooplanktivorous fish. In both experiments,
treatment allocation was randomized between the 12 mesocosms. Air was gently bubbled
(~20 ml/s) into the first 4 m of water in each mesocosm to create a well-mixed water column.
Light was provided by 150 W metal halogen lamps (MASTERColour CDM-T 150W/942
G12 1CT) suspended over each individual tank and set to 12 h light/12 h dark regime.
Temperature was regulated by a heating-cooling system containing circulating glycol and
temperatures did not fluctuate more than ± 0.5 °C/day. For both experiments, biological
variables at all levels of the food web were measured continuously, which includes production
of bacteria and phytoplankton at the base of the food web, biomass measurements of all
planktonic organisms, as well as fish growth. In addition, environmental variables, such as
nutrient concentrations, water colour and ambient light were monitored throughout
experiments.
In paper III four experimental treatments, each triplicate replicated, were established in order
to test for differences in food web efficiency between systems with contrasting structure at the
basal production level and with food webs of differing length. Basal production was
manipulated by adding either nitrogen and phosphorous to promote a phytoplankton based
food web, or by adding carbon in the form of glucose in addition to nitrogen and phosphorus,
to promote a food web mainly based on bacteria. Trophic positions at the top of the food web
was manipulated by having either naturally occurring zooplankton as top predator or by the
addition of zooplanktivorous fish, juvenile three-spined sticklebacks.
In paper IV we wanted to simulate the effects of river-bound carbon input, decreased light
conditions, as well as increased temperature on the pelagic food web. To achieve a carbon
input, which as closely as possible represented natural conditions, we created a natural,
colored humic soil solution. This terrestrial dissolved matter (TDM) would add not only
TDOC to the system, but also organic and inorganic N and P, along with humic acids and
other colored substances. Using the mesocosm facility we then created four experimental
treatments, each with three replicates, with TDM additions and temperature increase as
treatment variables and natural pelagic food webs containing all trophic levels from bacteria
to zooplanktivorous fish. The treatments were chosen to reflect current, relatively low
(TDML) and predicted high (TDMH) inputs of terrestrial organic and inorganic nutrients to the
marine environment via rivers and/or an elevation in water temperature (TDML T; TDMH T).
DOC concentrations were raised by 30% in our climate change scenario, based on simulations
predicting future, river-bound nitrogen export to the Baltic Sea (Eriksson-Hägg, 2010, Wikner
and Andersson in press). Temperature was raised by 4 °C based on current climate change
predictions (Meier 2006: Helcom, 2007: IPCC, 2007).
17
MAIN RESULTS
Paper I
The results in this study showed that the generic model for temperature dependent maximum
fish growth by Elliott et al, (1995) could be applied to describe experimentally derived growth
data for G. aculeatus. This is the first time a base-line model over the whole temperature
range suitable for growth in this species has been established. Optimal temperature for growth
was estimated to be 21.7 °C and based on the estimates of lower and upper temperature limits
for growth three-spined sticklebacks seem to be able to grow in conditions as low as 3.5 °C
and up to 30 °C. The comparisons between commercial pellets and natural prey suggested no
difference in growth potential between these two prey items and therefore our model
predictions can be applied to natural systems. Still, we observed a strong seasonal effect on
growth rates, with an average of 60% higher growth rates achieved at the optimum
temperature in summer compared to the winter. This finding reduces the applicability of the
model derived in this study to spring and summer seasons, but highlights that caution should
be exerted when extrapolating results from experimentally derived conditions to natural
populations and that the potential presence of seasonal effects warrants further investigation.
Paper II
The results presented in this paper provided estimates of both the size and temperature
dependent attack rate of the three-spined stickleback. We showed that three-spined
sticklebacks appear to be tolerant of increases in ambient temperatures and, when approaching
their optimum temperature of growth, just over 21 °C, their tolerance for decreasing resource
levels will actually increase their potential scope for growth, due to a decrease in CRD at
these temperatures. As higher summer temperatures should benefit stickleback populations,
the impacts of climate change on this species and its competitive interactions with other
species, definitely warrants further investigation.
Furthermore, our estimates of consumption capacities showed that despite increasing densities
in the Baltic proper (BP), sticklebacks in offshore areas have experienced relatively low levels
of resource limitation over the investigated time period. However, in the coastal zones of the
BP, resource levels have in recent years declined and approached CRD for a 1g stickleback,
indicating that sticklebacks under these conditions would not be able to sustain their
metabolic rates during the summer months. This may suggest that, at least in the coastal area
where sticklebacks reproduce, populations are starting to reach levels were their densities will
not increase further in the BP. In contrast, sticklebacks in the coastal zones of both the
Bothnian Bay (BB) and Bothinan Sea (BS) have not been markedly resource limited during
this last decade and have been able to feed close to maximum capacity, in addition to fish in
these corresponding offshore areas having experienced a significant decrease in resource
limitation over recent years. These results suggest that the off-shore habitats in BB and BS,
devoid of pelagic predators, have during recent years been areas with good growth potential
for migrating stickleback populations, but also that the suggested recent rise in stickleback
densities in the BS might have been facilitated by this lack of resource limitation.
18
Paper III
Results showed that ADOC additions significantly increased bacterial production (BP),
yielding a higher total basal production than treatments without carbon addition. As a result of
the increased heterotrophic production, food web efficiencies were lowered in the systems,
regardless of the top consumer. However, in terms of absolute production at the top of the
web, a top-consumer dependent response of ADOC additions was seen. In systems with
zooplankton as top-consumer, ADOC seems to have acted as a subsidy to the production of
heterotrophic protists, giving copepods a food source in addition to phytoplankton, resulting
in a higher total zooplankton production compared to NP treatments. However, when fish was
top-consumer, their production was instead lowered. The high energy loss at the top trophic
level in fish dominated food webs is suggested to be due to top-down effects, which, via
predator release of the lowest trophic levels, indirectly increased BP in the presence of ADOC
without stimulating primary production (PP) and stimulated PP in absence of ADOC. Since
the majority of energy in systems where fish and ADOC additions interacted was localized to
the microbial food web, higher energy losses occurred as carbon had to pass through several
additional trophic levels before reaching fish. Our results therefore suggests, that depending
on ADOC inputs into the system, cascading effects of planktivorous fish will dictate both the
magnitude of BP and PP production and the BP:PP ratios, causing feedbacks in the food web,
which ultimately influence their own production. Moreover, a climate change increase of
ADOC inputs may induce a shift towards heterotrophy in aquatic systems, which would
according to this study, cause decreased fish production in areas expressing high BP: PP
ratios.
Paper IV
It was shown that both increases in temperature and increased concentrations of TDOC will
independently affect the pelagic food web by stimulating bacterial production, and to varying
extents, the trophic levels of the planktonic food web. Neither factor on their own produced
effects that cascaded to the top of the food web, thus fish production or food web efficiency
were not influenced. However, when these two treatment effects were combined a
significantly higher fish production and food web efficiency was achieved in our simulated
climate change scenario as compared to present day conditions. The results indicate that the
combined effect lead to a temperature dependent increased production potential of
zooplankton, which was sustained by the increased production of heterotropic
microzooplankton stimulated by TDOC additions. The increased zooplankton biomass in turn
lead to higher fish production and increased food web efficiency. Although the increased
number of trophic linkages in the heterotrophic food webs should have reduced the energy
transfer efficiency, these negative effects seem here to have been overridden by the positive
increases in zooplankton production as a result of increased temperature. In terms of climate
change, predicted increases in temperature and TDOC input might therefore yield positive
effects on FWE and total production in higher trophic levels in present low productive
systems, but further studies need to be conducted to determine the generality of such a
statement. Furthermore, the results presented here strongly suggest that in order to fully
understand the effects of climate change on pelagic food web transfer efficiency, abiotic
variables cannot be studied in isolation.
19
CONCLUSIONS
The thermal response of the three-spined stickleback; implications of climate change for
sticklebacks in the Baltic Sea
The results presented in this thesis have highlighted several aspects of stickleback behavior
influenced by varying temperature and provided crucial baseline estimates of thermal
response to both consumption rates and growth, estimates which until now were missing. The
results in Paper I underscore the eurythermal nature of this species and clearly shows that
being adapted to a wide range of temperatures most likely underlies the sticklebacks
documented high capacity to adapt to new environments, which has allowed it to colonize
various habitats including shallows, warm tidal pools and the open oceans (Wootton, 1984;
Bell and Foster, 1994). Furthermore it shows a strong temperature dependent growth response
up to over 21 °C. This sharp peak in optimum response is actually higher than temperatures
usually experienced by the stickleback even in the midst of summer. In terms of growth, if
climate change increases average water temperatures, the three-spined stickleback might
therefore not be as adversely affected as other species.
Conclusions from paper II further highlight the tolerance of sticklebacks to increasing
temperatures. Even at the relatively elevated temperature of 24 °C stickleback foraging
capacity does not only function normally, but appears to be significantly faster compared to
lower temperatures. Furthermore, by measuring the CRD, i.e. the resource densities a species
needs to maintain basic metabolic needs, it was shown that these levels decreased with
increasing temperatures. This result seems at first glance to be counter-intuitive, as metabolic
demands increase with increasing temperature, necessitating an increased consumption to
meet those demands, which in turn is facilitated by and often dependent on higher resource
levels (Elliott 1977; Jobling 1995). However, it became evident that attack rates for the threespined stickleback had a much steeper increase with temperature than routine metabolism, in
turn decreasing CRD at higher temperatures. Therefore, based on our results, increased
temperatures may, in accordance with increased metabolic demands and digestion capacity,
lead to an overall increased consumption, but the levels actually needed to sustain individuals
will be lowered, thus increasing their scope for growth at higher temperatures.
It has been suggested that three-spined stickleback population densities in the Baltic Sea have
increased substantially in the last decade (Ljunggren et al, 2010; Eriksson et al, 2011) and that
competition from sticklebacks for shared zooplankton resources may affect recruitment of
other fish species e.g. perch Perca fluvitialis in the Baltic proper (Eriksson et al, 2009;
Ljungren et al, 2010). Although the results from this thesis cannot conclusively state that this
is occurring based on our attack rate estimates, it is clear that their competitive advantage will
only increase with increasing temperatures, as a combination of lower CRD and increased
growth potential will lead to substantially higher scope for growth of stickleback populations.
However, as the attack rate of a consumer is the net outcome of foraging related capacities of
both the consumer and its prey, the species specific temperature scaling of attack rate with
temperature, could likely vary substantially between consumers and for different prey types
and sizes (Englund et al, 2011 and references therein).
Our results also provide estimates on the levels of resource limitations which sticklebacks
have experienced over the last decade, which may have facilitated the reported increased
20
population densities. We showed that sticklebacks in the Baltic proper, where the suggested
population increase is supposed to be the strongest, have in recent years started to experience
higher degrees of resource limitation. This means population levels here might not increase
any further as they have started to reach their CRD. However, in both the coastal zones of the
Bothnian Bay and Bothnian Sea, sticklebacks have not been markedly resource limited during
the last decade and have been able to feed close to maximum capacity. Furthermore, degrees
of resource limitation seem to have decreased in these offshore habitats, indicating that these
areas, devoid of pelagic predators, would have provided areas of good growth potential for
migrating stickleback populations. A recent assessment of coastal test fishing programs has
indicated that spawning population of sticklebacks have increased over the last 5 years in the
Bothnian Sea (Byström unpublished compilation). Since both in-shore and off-shore areas of
the Bothnian Bay and Bothinan Sea seem to have provided good habitats for growth in recent
years, it plausible that we will see further increases in stickleback population numbers in these
basins and consequently patterns of negative relationships between sticklebacks and coastal
fish species seen today in the Baltic proper might soon be replicated in the more northern
basins.
As the impacts of climate change on fish populations are hard to deduce, having established
the baseline parameters of growth and foraging capacity in this species will at least provide a
starting point from which future patterns of competitive interactions and population
fluctuations can be deduced. Overall, since the physiological prowess of the three-spined
stickleback seems to provide it with a high degree of resilience against increasing
temperatures, the ecological role of this species in the Baltic Sea, today and in the future, is a
topic which definitely warrants further investigation.
Impacts of climate change on pelagic food web structure and function; implications for
fish production in the Baltic Sea
The results of paper III clearly show that allochotnous carbon (ADOC), i.e. originating from
outside the pelagic system, does have a structuring role on the pelagic food web. This will
mainly be expressed in decreased reliance of marine bacteria on autochthonous carbon
(originating from within the system) produced by phytoplankton. This will lead to increased
bacterial production and shift the ratio of bacterial to phytoplankton produced carbon at the
base of the food web. However, in the presence of planktivorous fish, this relationship is
strengthened and we saw ratios shifting even further in favor of bacterial production, leading
to a severe reduction in fish growth, compared to when fish were living in food webs
dominated by phytoplankton. The increased reliance on the microbial food web in these
systems suggested that depending on ADOC inputs into the system, cascading effects of
planktivorous fish will dictate both the magnitude of bacterial and primary production along
with their ratio, causing feedbacks in the food webs, which ultimately influenced their own
production. The results of this study thus clearly demonstrate that introducing ADOC to a
food web dominated by zooplanktivourous fish will impact fish production negatively, due to
the inefficiency of the microbial food web in providing energy to higher trophic levels.
However, the results in paper IV showed that a reduction of FWE induced by ADOC can be
offset by increases in temperature and that the combined effect of both factors can actually
lead to increased production of fish with a consequent higher transfer efficiency. This was due
to an increased temperature dependent production potential of zooplankton, leading to higher
food availability for fish, which in turn also had a higher production potential with the
21
temperature increase. Since temperature and ADOC interacted in a way that we did not
foresee, in addition to top-down effects profoundly altering the structure of the food web, it
becomes obvious that the full effects of climate change will be hard to predict.
If we are to extrapolate on these results beyond our study systems, we have to look at several
factors which may have influenced our findings. The Baltic Sea is firstly a unique system in
that its three main basins in a north-south gradient are very different from each other in terms
of abiotic variables, such as nutrient levels and salinity but also in terms of species
compositions, which differ markedly from the southern Baltic Proper to the northern Bothnian
Bay (Kautsky and Kautsky, 2000). The study area where we have been working in the
Bothnian Sea is an oligotrophic system, compared to the Baltic Proper, which is highly
eutrophic. Previous work has indicated that the effects of TDOC on pelagic systems would be
highly dependent on the existing nutrient regimes in the water and that its effects might be
stronger under oligotriohic conditions (Carpenter et al, 2005). As the effects of TDOC have
not been tested here under different stoichiometric conditions, we do not currently know how
the effects of increased river-bound carbon input might affect pelagic food web function and
structure in the Baltic proper or other marine areas with similar conditions. However, it could
be postulated that, in systems with high phytoplankton production, the reliance of bacteria on
ADOC will be lessened, as the carbon produced by phytoplankton would provide a much
better substrate for growth (Carpenter et al, 2005). Therefore, the amount of ADOC which
needs to be introduced to a eutrophic system before the ratio of BP: PP significantly shifts in
favor of bacteria, might be a lot more than the 30% increase we simulated in paper IV.
Furthermore, the choice of using the three-spined stickleback as a zooplanktivorous fish in
these study systems will also have a bearing on the presented results. As shown here, the high
resilience to increasing temperatures displayed by sticklebacks definitely implies that effects
of food availability and increased temperature will uniquely affect this species and effects
seen for sticklebacks might not translate directly to other species. Had our experimental
treatments instead been tested on performance of e.g. herring (Clupea harengus), which has
been shown to potentially be more sensitive to higher temperatures (Fey, 2001), it is likely
that the outcome of our experiments would have been very different.
In conclusion, as both terrestrial carbon and temperature have profound effects on all levels of
the pelagic food web, from influencing the competition for inorganic nutrients and production
potentials of phytoplankton and bacteria, to determining development times of zooplankton
and finally dictating production levels of fish, the full effects of climate change on the pelagic
food web and fish production are hard to untangle. As the body of evidence on the effects of
climate change accumulates it becomes apparent that only through increased knowledge will
we be able to prepare for how climate change will alter our common ocean environments and
hopefully the results put forward in this thesis will go some small way towards accomplishing
that goal.
22
THANKS
First and foremost I would like to thank my advisors and all the staff at the Umeå Marine
Science Centre for all the help and support they have given me. A big thanks goes of course to
my thesis collaborator Richard Degerman. I have really enjoyed working with you and I will
miss our discussions of crazy experimental mesocosm designs. Agneta and Ulf, without your
help, my comprehension of marine plankton life would have been today what it was when I
started this Ph.D, basically non-existent. Thank you for interesting discussions and also for all
the financial support over the years. Stefan, thanks for agreeing to give me a job in the first
place and although I am sorry you could not stick with me to the end, I am glad that I could
finish what we started together and the overall scientific design of this thesis would not have
been possible without you. Finally, I wish to especially thank Pär Byström for all the
enormous support and hard hours you have put in to make sure this thesis reached completion.
If you had not agreed to supervise me this last year, this thesis would not have been possible
to finish. I cannot express enough thanks for this and working together with you and
exchanging ideas has truly been a rewarding experience.
Thanks to my family for all the support they have given me throughout the years and who
always encouraged me to travel and never restricted my freedom to explore. Also, by
allowing me to spend most of our early summer holidays under-water with a snorkel, played a
big part in instilling my love for the ocean environment. I also wish to thank granddad for
taking me out on numerous fishing trips as a kid which started my interest in fish and fishing.
Last I want to thank my wife Annie for always supporting me, being a great partner in travels
and in life and who always makes me want to do better.
23
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27
AUTHOR CONTRIBUTIONS
Contribution/Paper
I
II
Original concept
RL,SL, PB
RL,SL, PB
Experimental design
RL, SL
RL, SL, PB
Data collection
RL
RL
Data analysis
RL, SL, PB
RL, PB
Interpretation of results
and manuscript
preparation
RL, PB, SL
RL, PB
III
IV
RD* and RL*,
AA, SL, UB,
LOE
RD, RL, SL, AA,
UB, LOE
RD*, RL *
RL and RD*, AA,
SL, UB, LOE
RD*, RL*, AA,
PB, UB
RL*, RD*, PB,
AA, UB
RD, AA, RL, PB,
UB
RL, PB, AA, RD,
UB
RL, RD, AA, SL,
UB
RL*, RD *
AA, Agneta Andersson, LOE Lars-Ove Eriksson PB, Pär Byström, RD, Rickard Degerman, RL,
Robert Lefébure, SL, Stefan Larsson, UB, Ulf Båmstedt * Both authors contributed equally to the
original concept, data collection and data analysis.
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