How will climate change affect
benthic primary producers and
consumers?
An experimental study on periphyton and aquatic snails
Zandra Fagernäs
Degree Thesis in Biology 15 ECTS
Bachelor’s Level
Report passed: 2014-08-29
Supervisor: Pär Byström
How will climate change affect benthic primary producers and consumers?
An experimental study on periphyton and aquatic snails.
Zandra Fagernäs
Abstract
The global climate is predicted to go through great changes in the 21st century, which will
have impacts on ecosystems all over the world. Aquatic ecosystems will be affected by higher
annual temperatures and increased runoff from surrounding terrestrial areas. The increased
runoff will cause more terrestrial organic matter (TOM) to reach the waters, which will
elevate levels of dissolved organic carbon and nutrients. The higher temperature, changed
water color and increased nutrient concentration are together bound to affect aquatic
systems, but exactly how the systems will respond is yet unclear. The aim of this study was to
investigate how periphyton and benthic grazers will react to higher temperatures and
elevated amounts of TOM in the water. This was done by measuring production of
periphyton and growth rates of the snail species Gyraulus acronicus when placed in
treatments with higher temperature, more TOM or a combination of these two. Higher
temperature was found to have a negative effect on periphyton production, while increased
amounts of TOM alone had a positive effect, and the combination of these two lowered
production. The results on snail performance were in most cases non-significant, but the
results still suggest that possible future effects of more TOM and higher temperature on the
snails will be negative.
Key words: climate change, periphyton, Gyraulus acronicus, temperature, TOM
Table of contents
1.
2.
Introduction............................................................................ 1
Material and methods..................................................... 2
2.1.
2.2.
2.3.
2.4.
Experimental system.................................................................... 2
Study organisms............................................................................. 3
Snail....................................................................................................... 3
Periphyton............................................................................................. 3
Experimental design and setup.................................................. 4
Statistical analysis.......................................................................... 4
3.
Results.......................................................................................... 5
3.1.
Snails
2.2.1.
2.2.2.
3.2.1.
3.2.2.
3.2.3.
......................................................................................... 5
Survival............................................................................................... 5
Growth rate........................................................................................ 6
Total biomass..................................................................................... 6
Resource production...................................................................... 7
Particulate organic carbon............................................................... 7
Chlorophyll-a...................................................................................... 7
Periphyton biomass........................................................................... 8
4.
Discussion................................................................................... 9
4.1.
4.2.
4.3.
Primary production........................................................................ 9
Snails.................................................................................................. 10
Conclusions....................................................................................... 11
3.1.1.
3.1.2.
3.1.3.
3.2.
5.
Acknowledgements............................................................ 11
6.
References................................................................................. 12
Appendix..................................................................................................... 14
1. Introduction
In the 21st century, the climate on Earth is predicted to go through large changes. The
temperature is expected to have increased 1.8-4°C globally by the end of the century, which
will have dramatic consequences on ecosystems all over the world (Swedish Commission on
Climate and Vulnerability 2007). Climate change is predicted to have larger effects in present
colder environments (Rosa et al. 2013), for example in Sweden the temperature is expected
to rise 3-5°C until 2080 compared with the period 1960-1990 (Swedish Commission on
Climate and Vulnerability 2007). The precipitation is expected to increase, which will lead to
a higher annual runoff from surrounding terrestrial areas to freshwater ecosystems (Swedish
Commission on Climate and Vulnerability 2007). Freshwater ecosystems will be especially
vulnerable to alterations caused by warming and increased runoff, since they are rather
fragmented and isolated, and already experience extensive of stress from human activities
(Woodward et al. 2010).
The rise in temperature and increased precipitation will affect aquatic systems in several
ways, such as decreasing the periods of ice cover and causing a more stable thermocline in
the summer (IPCC 2013). Increased runoff will also lead to a higher amount of dissolved
organic carbon (DOC) and nutrients in the water (Kritzberg et al. 2014). This will make the
water browner, which will lead to reduced light penetration (Kritzberg et al. 2014). The light
conditions are furthermore affected by other factors, such as stratification and cloud cover,
which are as well expected to be altered due to the changing climate (Winder and Sommer
2012). Vertical mixing is also an important factor for many aquatic organisms, since it
changes nutrient availability and light conditions, and a more stable thermocline would alter
this mixing process (Winder and Sommer 2012).
The food webs and productivity of freshwater ecosystems are bound to change due to the
altered conditions, but exactly how they will change is yet unclear. Increased input of
nutrients to the water can increase primary production (Karlsson et al. 2009), but higher
DOC concentrations may also make primary producers light limited by impairing the light
climate (Karlsson et al. 2009; Nicolle et al. 2012; Lefébure et al. 2013). In browner waters,
periphyton biomass has indeed been shown to be depressed (Vis et al. 1998; Mormul et al.
2012). Light conditions will to a large extent determine the response of aquatic food webs
when the climate changes, since light-saturated photoautotrophs can increase their primary
production in higher temperatures, but not light-limited ones (Winder and Sommer 2012).
Benthic primary producers are often more limited by light than nutrients, since they acquire
nutrients mainly from the lake sediments (Ask et al. 2009), and an increased amount of DOC
might thereby only affect their production negatively. Climate change is suggested to shift the
balance between algal and cyanobacterial primary production towards being more bacteriadominated (Swedish Commission on Climate and Vulnerability 2007; Kosten et al. 2012;
Winder and Sommer 2012; Lefébure et al. 2013). The plankton community will also change,
as smaller individuals are expected to be favored and species will respond differently to the
altered conditions (IPCC 2013).
Climate change does however not affect all organisms in the same way (Burgmer et al. 2007).
Higher temperatures increase the metabolism of organisms and communities (Rosa et al.
2013), but have been found to increase heterotroph consumption more than primary
production (Allen et al. 2005; Winder and Sommer 2012). Elevated water temperatures are
thereby expected to lead to higher algal growth rates, but not necessarily higher algal
biomass, since grazing pressure is also expected to increase as a response to higher metabolic
rates (Baulch et al. 2005). This might lead to that the biomass pyramids in aquatic
ecosystems shift to be more top-heavy (Shurin et al. 2012). The metabolic theory of ecology
also suggests that increasing temperature should decrease body size, as the metabolic
demands per unit biomass increase with temperature, which favors small individuals over
large (Allen et al. 2002).
1
The changes in the algal community will also have effects on higher trophic levels (Karlsson
et al. 2009) in addition to direct effects they will experience from climate change (Burgmer et
al. 2007). For example benthic herbivores are expected to have an increased metabolic rate
due to higher water temperature (Allen et al. 2005) and some of them have also been shown
to increase in abundance (Baulch et al. 2005). But as brownification of waters is predicted to
depress periphyton abundance, the reduced amount of food will have negative effects on the
aquatic herbivore community.
The aim of this study was to experimentally test how benthic primary producers and
consumers will respond to future climate changes. More specifically, the growth rates of
periphytic algae and the snail Gyraulus acronicus were measured in small enclosures
positioned in a large scale experimental pond facility, where water temperature and/or the
amount of terrestrial organic matter (TOM) in the water are manipulated. The main
hypotheses tested were:
1)
2)
3)
4)
5)
Primary production will increase in higher temperatures
Increased TOM will increase primary production near the surface
Increased TOM will decrease primary production on the bottom
Snail growth rates will increase in higher temperatures
Snails will be affected by TOM in the same way as periphyton
2. Material and methods
2.1.
Experimental system
The study was conducted at the EXEF (Umeå University Experimental Ecosystem Facility)
pond in Umeå. The pond is divided into twenty sections, each 7.7*12.5 meters. Maximum
depth in the sections is 1.6 meters. Eight of these sections are heated to about 3°C warmer
than the other sections (Figure 1), and eight sections receive an input of natural river water
with a high amount of terrestrial organic matter (TOM), whereas other sections receive
similar amounts of clear tub water. This gives four different treatments with four replicates
each; a) ambient conditions, b) heated, c) increased TOM and d) heated with increased TOM.
The four sections in the middle are used as buffers between the heated and not-heated
sections. The pond has one fish species, three-spined stickleback (Gasterosteus aculeatus), as
top consumer and primary producers and consumers natural for lakes and ponds in Sweden.
Temperature, light conditions and water chemistry are continuously measured in each of the
sections (Table 1).
20
18
TOM
16
14
TOM
12
Buffer
10
Buffer
8
Heat
TOM
6
Heat
4
Heat
TOM
2
Heat
19
17
TOM
15
13
TOM
11
Buffer
9
Buffer
7
Heat
TOM
5
Heat
3
Heat
TOM
1
Heat
Figure 1. Schematic picture of the EXEF-pond. “Heat” means that the water is ca 3°C warmer, and “TOM” that the
water has a higher amount of terrestrial organic matter.
2
Table 1. Data from the different treatments. Temperature and photosyntetically active radiation (PAR) are
averages from 11 June to 21 July 2014, measured at 12:00 each day at 70 cm depth. Decrease in PAR is measured
from 25 cm to 125 cm depth, data from 17 July 2014. Dissolved organic carbon (DOC), total phosphorus (TP), total
nitrogen (TN) and pH are averages from May to September 2013. All values are mean ± 1 SE. Source: P. Byström,
unpublished data.
Temperature (°C)
Ambient
17.59 ± 0.3
Treatment
Heat
20.40 ± 0.1
TOM
17.24 ± 0.1
Heat, TOM
20.11 ± 0.2
PAR (μmol/m2sec)
489.28 ± 63.7
516.65 ± 25.9
121.66 ± 16.2
227.26 ± 19.6
Decrease in PAR (%)
70.09 ± 2.1
77.24 ± 6.5
84.00 ± 2.3
85.29 ± 4.2
DOC (mg/l)
TP (μg/l)
TN (μg/l)
pH
4.4 ± 0.6
19.0 ± 2.4
277.4 ± 8.7
8.1 ± 0.1
3.6 ± 0.2
13.1 ± 2.3
244.6 ± 43.2
8.6 ± 0.1
11.4 ± 0.2
24.8 ± 1.1
438.5 ± 11.6
7.3 ± 0.1
9.4 ± 0.3
16.9 ± 3.0
359.6 ± 63.6
7.6 ± 0.1
2.2.
2.2.1.
Study organisms
Snail
Gyraulus acronicus (Férrusac, 1807) is a freshwater pulmonate snail species (Olsson 1988)
belonging to the family Planorbidae. The shell of an adult snail is 5-8 mm wide, 1.5-1.8 mm
high and has a pale brown color with a red, yellow or grey tone (Hubendick 1949). As a
pulmonate snail, G.acronicus breathes by filling a vessel rich cavity with air (Brönmark and
Hansson 1998). The species is found in most freshwater habitats, preferring lakes and slowrunning rivers (Økland 1990). It is found on solid or loose substrates or on macrophytes
(Hubendick 1949) in waters with varying color and turbidity (Økland 1990). The species is
found in large parts of Europe and Asia (Økland 1990), in Europe in an area stretching from
the British Isles to the Baltic States and from the Alps to northern Scandinavia (JNCC 2010).
G. acronicus is an important food source for many freshwater fish species, for instance brown
trout (Økland 1990). Other predators on the snail are leeches, flatworms and aquatic insect
larvae (Brönmark and Hansson 1998). Freshwater snails mainly feed on detritus and
periphytic algae (Brönmark and Hansson 1998).
2.2.2.
Periphyton
Periphyton is here defined according to Brönmark and Hansson (1998) as all microalgae
growing on any kind of substrate. This substrate can be anything from inorganic surfaces to
organic debris to living organisms (Bellinger and Sigee 2010). Periphytic algae are an
especially important food source for many invertebrates in clear waters with low nutrient
status (Brönmark and Hansson 1998). The species composition of periphyton varies
seasonally (Allan 1995) and periphytic algae often form mixed biofilms with bacteria,
invertebrates and fungi (Bellinger and Sigee 2010). There are many algal species that spend
part of their life as planktonic and part as benthic (Bellinger and Sigee 2010). Bare surfaces in
freshwaters are first colonized by bacteria, followed by diatoms (Brönmark and Hansson
1998). Finally the surfaces are colonized by filamentous species, which then become the
dominating algae, since they are the superior competitors for light (Brönmark and Hansson
1998).
The three major groups of periphyton are diatoms, green algae and cyanobacteria. Most
diatoms are periphytic (Brönmark and Hansson 1998), and they are often the most species
rich group in periphyton, but do not necessarily comprise the largest biomass (Allan 1995).
They are consumed by protists and invertebrates and function as a carbon sink, since if not
consumed they cannot be decomposed by bacteria and other decomposers (Reece et al. 2011).
3
Diatoms often dominate at high levels of pH, regardless of the nutritional status of the water
(Brönmark and Hansson 1998). Seasonal changes in light availability do not seem to have a
great impact on diatom abundance (Allan 1995).
Green algae are a very morphologically diverse group (Brönmark and Hansson 1998) and can
be singular, multicellular or form colonies (Reece et al. 2011). Since they contain chlorophylla and –b, most of them have a bright green color (Bellinger and Sigee 2010). At high amounts
of light, filamentous green algae are often dominating (Allan 1995), and they can also
dominate in very nutritious waters (Bellinger and Sigee 2010).
Cyanobacteria are the only prokaryotes that can perform oxygen-forming photosynthesis,
and some species are capable of fixating nitrogen (Reece et al. 2011). They have a higher
optimal growth temperature than other plankton groups and are more shade-tolerant
(Kosten et al. 2012). Bacteria have been shown to be the superior competitors for nutrients
when temperatures or the amount of organic matter are increased (Lefebure et al. 2013).
Benthic cyanobacteria form biofilms, which consist of cells and extracellular secretions that
attach the cyanobacteria to the substrate and function as a medium for nutrient transport
(Noffke et al. 2003).
2.3.
Experimental design and setup
Growth rates of periphyton and snails were measured in net cages (12*13.5*16 cm) with a
mesh size of 0.3*0.5 mm. The cages were placed at two different depths (0.7 m and on the
bottom 1.4 m), one snail cage and one control cage without snails at each depth. All cages
contained tiles (9 x 9 cm) as growing substrate for algae. The control cages had two tiles, so
that measurements could be made both at the start and the end of the experiment, and the
snail cages contained one tile each. The cages were positioned into the ponds on 16 May and
the snails were put in the cages on 11 June. Start masses were calculated from a start sample
of 68 snails. Mean size at start for the snails was 4.5±0.2 mm and average weight was 5.238
mg. Five snails were put in each cage, which is approximately the density they have naturally
in the experiment pond (P. Byström, unpublished data). When the snails were placed in the
cages, the algal biomass on each tile was measured using a BenthoTorch. The BenhoTorch is
an instrument developed by bbe Moldaenke GmbH, which is used to measure benthic algal
biomass and community composition in the field. It emits light pulses of different
wavelengths and measures the fluorescence response of the algae, which it then automatically
calculates into microalgal biomass (Carpentier et al. 2013).
One tile was removed from each control cage on 11 June in order to measure chlorophyll and
particulate organic carbon (POC). The snails were left to grow in the pond until 21 July. The
length and dry mass of each snail was then measured, and the algal biomass was again
measured on all tiles with a BenthoTorch. The algae were scraped from each tile and filtered.
Half of the filtered algae were used to measure the amount of particulate organic carbon
(POC) on the tiles. These filters were first dried for 18 hours in 60°C, and then measured with
an IL 500 TOC-analyzer. The rest of the filtered algae were used to measure chlorophyll-a,
and were left to dry in room temperature for 24 hours, after which they were frozen down for
a couple of weeks. The filters with the algae were then dissolved in 95% ethanol, and the
amount of chl-a was measured with a spectrophotometer.
2.4.
Statistical analysis
Growth rate (Gw) for snails was calculated as Gw=((ln(m2)-ln(m1))/t)*100%, where m1 is the
start biomass of the snails, m2 is end biomass, and t is the amount of days the snails spent in
the cages. Survival was calculated as (n2/n1)*100%, where n1 is the amount of snails placed in
the cage, and n2 the amount of snails found alive in the cage at the end of the experiment.
Total biomass of snails in each cage was also calculated. Production rates (Pr) were
4
calculated for all measures of primary production (Chl-a, POC and periphyton biomass) as
Pr=((ln(t2)-ln(t1))/t)*100%, where t1 was the value at the first measurement time and t2 at
the second.
All data were tested for normality with an Anderson-Darling normality test. The data sets
that didn’t have a normal distribution were transformed and tested again. Since all data sets
showed to be normally distributed after this procedure, they were analyzed with ordinary
one-, two- or three-ways ANOVA with climate treatments (temperature, TOM) and depth as
factors. In appendix A results from all statistical test are presented, while in the result section
only p-values of significant (p<0.05) and close to significant (p<0.1) results are presented.
3. Results
3.1.
Snails
3.1.1.
Survival
The snails had the highest survival on the bottom in ambient conditions (95 %) and the
lowest on the bottom when only the amount of TOM was elevated (50 %) (Figure 3). The
survival of snails showed a significant negative relation to elevated amounts of TOM
(F=4.900, p=0.037), also when only looking at cages that were positioned on the pond
bottom (F=8.311, p=0.014) (Figure 3). TOM had a significantly stronger negative effect on
snail survival in ambient temperature than in elevated temperatures (F=4.900, p=0.037),
and this was also the case when looking only on shallow cages, although the effect was only
close to significant (F=4.119, p=0.065). Increased amounts of TOM had a close to
significantly stronger negative effect on snail survival at the pond bottom than in shallow
cages (F=3.600, p=0.070) (Figure 3). No other significant effects of temperature or TOM
were found in either depth (p>0.10, in all cases).
120
Survival (%)
100
80
60
Bottom
Shallow
40
20
0
Ambient
Heat
Heat, TOM
TOM
Figure 3. Average survival (±1 SD) for snails in each treatment on the pond bottom and 70 cm below the surface.
5
3.1.2.
Growth rate
The snails had the highest growth rates in shallow cages in the ambient treatment (0.440
%/d) and the lowest at the bottom when both temperature and TOM were elevated (-0.087
%/d) (Figure 2). No significant or close to significant effects of treatments or cage position
could be detected (p>0.1o, in all cases)
0,7
0,6
Growth rate (%/d)
0,5
0,4
0,3
Bottom
0,2
Shallow
0,1
0
-0,1
Ambient
Heat
Heat, TOM
TOM
-0,2
-0,3
Figure 2. Average growth rates (±1 SD) for snails in each treatment on the bottom and 70 cm below the surface.
3.1.3.
Total biomass
The snails had the highest average total biomass in shallow cages in ambient conditions (31.4
± 2.1 mg) and the lowest on the bottom when only TOM was increased (13.4 ± 3.4 mg)
(Figure 4). TOM had a significant negative effect on total biomass (F=4.672, p=0.041), and
the total biomass on the pond bottom had also a significant negative relation to TOM
(F=6.187, p=0.029). In the shallow cages the total biomass was close to significantly
negatively affected by temperature (F=3.799, p=0.075) (Figure 4). TOM had an almost
significantly stronger negative effect on total biomass in ambient temperature than in
elevated temperature (F=4.066, p=0.055). No other effects of temperature or TOM on total
biomass were found (p>0.10, in all cases).
40
35
Biomass (mg)
30
25
Bottom
20
Shallow
15
10
5
0
Ambient
Heat
Heat, TOM
TOM
Figure 4. Average total biomass (±1 SD) in each treatment on the bottom and 70 cm below pond surface
6
3.2.
Resource production
3.2.1.
Particulate organic carbon (POC)
On the bottom, the average production of POC was highest when only TOM was elevated (2.6
%/d) and lowest when both TOM and temperature were elevated (1.056 %/d) (Figure 5). In
shallow cages the production was also highest when only TOM was elevated (4.2 %/d), but
lowest when only temperature was elevated (2.0 %/d) (Figure 5).
The production of POC was close to significantly higher in shallow cages than on the bottom
(F=4.114, p=0.054) (Figure 5). In shallow cages there was a close to significant negative effect
of increased temperature on POC production (F=3.957, p=0.070). No other effects of
temperature or TOM could be detected (p>0.10, in all cases).
6
Production (%/d)
5
4
Bottom
3
Shallow
2
1
0
Ambient
TOM
Heat
Heat, TOM
Figure 5. Average production (±1 SD) of particulate organic carbon in each treatment.
3.2.2.
Chlorophyll-a
At the pond bottom the highest production of chlorophyll-a was in the treatment where only
TOM was increased (5.1 %/d) and the lowest production was found when only temperature
was elevated (3.2 %/d) (Figure 6). In shallow cages the highest average production was in the
treatment with only elevated TOM (6.4 %/d) and the lowest when only temperature was
elevated (2.6 %/d) (Figure 6).
Overall temperature had a close to significant negative effect on the production of
chlorophyll-a (F=4.278, p=0.050) (Figure 6). When only looking at shallow cages,
temperature also had an almost significant negative effect on production (F=3.454,
p=0.088). No other significant effects of TOM or temperature were found in either depth
(p>0.10, in all cases).
7
9
8
Production (%/d)
7
6
5
Bottom
4
Shallow
3
2
1
0
Ambient
TOM
Heat
Heat, TOM
Figure 6. Average production (±1 SD) of chlorophyll-a in each treatment.
3.2.3.
Periphyton biomass
The production of periphyton in shallow control cages was highest in the treatment with only
increased TOM (4.4 %/d) and lowest when only temperature was elevated (0.2 %/d) (Figure
7). The average production on the pond bottom was highest when only the amount of TOM
was elevated (0.5 %/d) and lowest when both temperature and TOM were elevated (-1.3 %/d)
(Figure 7).
In the control cages, the production of periphyton was significantly higher in shallow cages
than at the bottom (F=18.618, p<0.001). The effects of increased amounts of TOM were
significantly stronger in shallow cages than at the bottom (F=4.651, p=0.041) (Figure 7).
Close to the pond surface, production had a significant negative relation to temperature
(F=5.256, p=0.041) and on the bottom, there was a close to significant negative effect of
temperature (F=3.250, p=0.097) (Figure 7). The effects of TOM were not significant in either
depth (p>0.10, in both cases).
7
6
Production (%/d)
5
4
3
Bottom
2
Shallow
1
0
-1
Ambient
TOM
Heat
Heat, TOM
-2
-3
Figure 7. Average production (±1 SD) of periphyton in control cages in each treatment.
8
Periphyton decreased in most treatments in cages containing snails (Figure 8). The highest
rate of change was found in shallow cages when only temperature was elevated (0.3 %/d) and
the strongest decrease on the pond bottom when both temperature and TOM were elevated (2.4 %/d) (Figure 8).
The rate of change was significantly higher in bottom cages (F=6.233, p=0.020), and
increased amounts of TOM had a significantly stronger negative effect on the bottom than
close to the surface (F=7.643, p=0.011) (Figure 8). In the bottom cages, a close to significant
negative relation to elevated amounts of TOM was found (F=3.238, p=0.097). No other
effects of temperature or TOM were found (p>0.10, in all cases).
2
1,5
Rate of change (%/d)
1
0,5
0
-0,5
Ambient
TOM
Heat
-1
Heat, TOM
Bottom
Shallow
-1,5
-2
-2,5
-3
-3,5
Figure 8. Rate of change (±1 SD) of periphyton in cages with snails.
4. Discussion
4.1.
Primary production
Contrary to what was expected, the results of this study show that production rates of
periphyton were negatively related to water temperature. The negative effect of higher
temperature is especially evident close to the surface, where all measures of production (POC,
chl-a and periphyton biomass) showed signs of lower production in elevated temperature. An
explanation to this negative relation might be that the algal respiration increases more with
temperature than production does (Rosa et al. 2013). The algae in this system might
furthermore already live close to their optimal growth temperature, so an increase in
temperature makes the conditions suboptimal for them (Thomas et al. 2012). The fact that
the effects of increased temperature were particularly strong in shallow cages can simply be
explained by that production rates were overall higher close to the surface, where the primary
producers had access to more light than on the pond bottom.
No significant effects of increased amounts of terrestrial organic matter (TOM) on primary
production were detected, but still all the highest values of primary production were found in
the treatment where only TOM was elevated. Some support is thus provided to hypothesis 2,
that increased TOM will increase production near the pond surface. The lack of clear effects
may be due to the counteracting effects of increased nutrient concentration stimulating algal
production and decreased light availability lowering production (Karlsson et al. 2009). In the
cages with snails, periphyton biomass increased in shallow cages in the treatment with only
elevated TOM, which means that production was high enough to sustain a grazer population
9
and still increase the algal biomass. This suggests that TOM might have a positive relation to
primary production, even if it cannot be statistically proved from the results of this study. The
positive relation is most likely because of the higher nutrient concentration found in the
treatments with river water (Table 1). The tiles were in cages, so they had no contact with the
bottom sediment, and the only source of nutrients for the algae was thereby the surrounding
water. As the surrounding water contained more nutrients in the treatments with elevated
TOM, the algae were able to increase their production. In nutrient limited systems, a higher
amount of TOM is indeed expected to increase production (Karlsson et al. 2009). Other
studies have shown that primary production decreased in browner water (Nicolle et al. 2012;
Kritzberg et al. 2014), but in those experiments the amount of nutrients was not higher in the
brown water treatments.
A higher input of TOM is also expected to make the primary producers light limited by
changing the water color, and thereby impairing the light climate (Karlsson et al. 2009; IPCC
2013; Lefébure et al. 2013). This does however not seem to be the case in this particular
system, which suggests that the amount of TOM that is added is too low to make the primary
producers light limited, even on the pond bottom. The pond is rather shallow, so enough light
for primary production still reaches the bottom, although more light is absorbed in the water
column (Table 1). This speaks against hypothesis 3, that primary production on the pond
bottom would decrease with elevated amounts of TOM.
The combination of elevated temperature and increased amounts of TOM does however seem
to have a negative effect on primary production. In many of the measures for production, the
lowest rates were found in the treatment with both increased temperature and more TOM.
Even though no significant differences could be found, these results still indicate that the
interplay of these two factors might be unfavorable for periphyton. The negative effects of
increased temperature thereby seem to be stronger than the positive effects of increased
nutrient concentration. The fact that periphyton seem to be negatively affected by the
interplay of rising temperatures and increased amounts of TOM in the water, suggests that
future climate change will be disadvantageous for them. This will have effects also higher up
in the food chain, since benthic algae are an important food source for many aquatic grazers.
One peculiar thing found in the results from the periphyton production measurements is that
there were negative production rates on the pond bottom in the control cages, where no
snails were present. This may be explained by the fact that as the BenthoTorch measures
biomass of photoactive algae, actual growth rates of algae may be depressed at the very high
temperatures observed at the time of last sampling occasion (average temperature in heated
enclosures on 11 June was 20.8°C, on 21 July 25.9°C). The summer of 2014 was exceptionally
warm, which might have decreased growth rates of some algal groups, especially towards the
end of the experiment. Still the values of chlorophyll and POC increased, suggesting that
production rates were positive over the entire experimental period.
4.2.
Snails
Although snail growth wasn’t significantly affected by temperature, a trend towards a
negative relation to higher temperatures was present. The highest growth rates were found in
ambient temperature both on the bottom and close to the surface, and the lowest were found
in elevated temperatures. In shallow cages, there was also an almost significant negative
relationship between total biomass and temperature. This speaks against hypothesis 4, that
warmer water would increase snail growth. Since periphyton is negatively affected by higher
temperatures, it is logical that snails are affected in the same way, but somewhat surprising
that no significant effects were found. The snails were expected to have a higher need for food
in elevated temperatures, since their metabolism increases (Rosa et al. 2013), but they still
show only weak signs of growing less in warmer treatments, where food is produced at a
lower rate. An explanation for this might be that the density of snails in the cages was so low
10
that they had more than enough food to satisfy their needs as their metabolism increased. It
might also be that higher temperatures increased foraging capacities, which to some extent
compensated for the increased metabolic demands (Lefébure et al. 2014). The remarkably
warm summer of 2014 might moreover have made the conditions in all treatments
suboptimal for the snails. Other studies on aquatic invertebrates have found contrasting
results; positive relations between growth rate and temperature have been found for e.g.
midges (Gresens 1997), copepods (Campbell et al. 2001) and snail larvae (Lima and Pechenik
1985). In these experiments the food production was however not affected by temperature,
which might explain why the results were the opposite of those found in this study. A review
by Atkins (1995) found that in the majority of studies on aquatic ectotherms, increased
temperature caused a reduction in body size, as indicated also by the results of this study.
Increased amounts of TOM appear to have negative effects on snails, since elevated TOM
lowered the total snail biomass found on the pond bottom. In the treatments that had both
elevated amounts of TOM and higher temperature, this could likely be explained by a lower
production rate of periphyton. In the sections with only increased amounts of TOM, where
periphyton production was in fact elevated, it is probably only a consequence of that survival
was lower. Survival was overall negatively affected by TOM at the bottom, but why this was
the case is not easily explained, especially as in the treatment with only elevated TOM the
food production was high and the snails should not have died of starvation. In the treatment
with both elevated TOM and temperature, this might be the case, as the lower production
rate of periphyton might have lowered the carrying capacity of the cages. Hypothesis 5 is both
spoken for and against by these results, since the snails respond in the same way as
periphyton in the treatment where both temperature and TOM are elevated, but not in the
one where only TOM is elevated.
Since tendencies for decreased growth rates and in some cases significantly lower survival
and total biomasses of snails were found in response to increased temperature and/or TOM,
it can be suggested that predicted climate change effects may affect snail populations
negatively.
4.3.
Conclusions
What can be concluded from this experiment is that the future rise in temperature will
probably have a negative effect on periphyton communities in aquatic ecosystems, while
increased amounts of terrestrial organic matter might have a positive effect in shallow
ecosystems. However, these two changes are expected to happen simultaneously as a
consequence of the global climate change, and together they had a negative effect on benthic
primary production. Production rates of benthic algae might thereby be decreasing in the
future. A negative effect on benthic grazers is predicted, based on the negative effects of
climate change on their food resources. Although the results on snail performance were in
most cases non-significant, the results suggest that possible future effects of elevated
temperature and increased amounts of TOM on snails will be negative.
5. Acknowledgements
First and foremost I would like to thank my supervisor Pär Byström, for giving me the
opportunity to do this study, and for helping and advising me with everything. It has been a
really interesting and educational experience! I would also like to thank Francisco
Vasconcelos, Jenny Ask, Anders Jonsson, Ryan Sponseller and everyone else who helped me
in different ways. Last I would like to thank my mother for proofreading my texts and endless
encouragements.
11
6. References
Allan, J.D. 1995. Stream ecology. Chapman & Hall, London. 388 pages.
Allen, A.P., Brown, J.H. and Gillooly, J.F. 2002. Global biodiversity, biochemical kinetics,
and the energetic-equivalence rule. Science, 297:1545-1548.
Allen, A.P., Gillooly, J.F. and Brown, J.H. 2005. Linking the global carbon cycle to individual
metabolism. Functional Ecology, 19:202-213.
Ask, J., Karlsson, J., Persson, L., Ask, P., Bytröm, P. and Jansson, M. 2009. Terrestrial
organic matter and light penetration: Effects on bacterial and primary production in lakes.
Limnology and Oceanography, 54:2034-2040.
Atkins, D. 1995. Effects of temperature on the size of aquatic ectotherms: Exceptions to the
general rule. Journal of Thermal Biology, 20:61-74.
Baulch, H.M., Schindler, D.W., Turner, M.A., Findlay, D.L., Paterson, M.J., Vinebrooke, R.D.
2005. Effects of warming on benthic communities in a boreal lake: Implications of climate
change. Limnology and Oceanography, 50:1377-1392.
Bellinger, E.G. and Sigee D.C. 2010. Freshwater algae: identification and use as bioindicators.
John Wiley & Sons, Chichester. 285 pages.
Brönmark, C. and Hansson, L-A. 1998. The biology of lakes and ponds. Oxford university
press, New York. 216 pages.
Burgmer, T., Hillebrand, H. and Pfenninger, M. 2007. Effects of climate-driven temperature
changes on the diversity of freshwater macroinvertebrates. Oecologia, 151:93-103.
Campbell, R.G., Wagner, M.M., Teegarden, G.J., Boudreau, C.A. and Durbin, E.G. 2001.
Growth and development rates of the copepod Calanus finmarchicus reared in the
laboratory. Marine Ecology Progress Series, 221:161-183.
Carpentier, C., Dahlhaus, A., van de Giesen, N. and Maršálek, B. 2013. The influence of hard
substratum reflection and calibration profiles on in situ fluorescence measurements of
benthic microalgal biomass. Environmental Science Processes & Impacts, 15:783-793.
Hubendick, B. 1949. Våra snäckor: Snäckor i sött och bräckt vatten. Albert Bonniers Förlag,
Stockholm. 100 pages.
Gresens, S. 1997. Interactive effects of diet and thermal regime on growth of the midge
Pseudochironomus richardsoni Malloch. Freshwater Biology, 38:365-373.
IPCC Working Group II. 2013. Chapter 4. Terrestrial and inland water systems. Fifth
Assessment Report.
JNCC, Joint Nature Conservation Committee. 2010. Gyraulus acronicus version 2. UK
priority species data collation. Noffke, N., Gerdes, G. and Klenke, T. 2003. Benthic
cyanobacteria and their influence on the sedimentary dynamics of peritidal depositional
systems (siliciclastic, evaporitic salty, and evaporitic carbonatic). Earth-Science Reviews,
62:163-176.
Karlsson, J., Byström, P., Ask, J., Ask, P., Persson, L. and Jansson, M. 2009. Light limitation
of nutrient-poor lake ecosystems. Nature, 460:506-510.
Kosten, S., Huszar, V.L.M., Becares, E., Costa, L.S., van Donk, E., Hansson, L-A., Jeppesenk,
E., Kruk, C., Lacerot, G., Mazzeo, N., de Meester, L., Moss, B., Lurling, M., Noges, T.,
Romo, S. and Scheffer, M. 2012. Warmer climates boost cyanobacterial dominance in
shallow lakes. Global Change Biology, 18:118-126.
Kritzberg, E., Granéli, W., Björk, J., Brönmark, C., Hallgren, P., Nicolle, A., Persson, A. and
Hansson L-A. 2014. Warming and browning of lakes: consequences for pelagic carbon
metabolism and sediment delivery. Freshwater Biology, 59:325-336.
Lefébure, R., Degerman, R., Andersson, A., Larsson, S., Eriksson, L-O., Bamstedt, U. and
Bytröm, P. 2013. Impacts of elevated terrestrial nutrient loads and temperature on pelagic
food-web efficiency and fish production. Global Change Biology, 19:1358-1372.
Lefébure, R., Larsson, S. and Byström, P. 2014. Temperature and size-dependent attack rates
of the three-spined stickleback (Gasterosteus aculeatus); are sticklebacks in the Baltic Sea
resource-limited? Journal of Experimental Marine Biology and Ecology, 451:82-90.
12
Lima, G.M. and Pechenik, J.A. 1985. The influence of temperature on growth rate and length
of larval life of the gastropod, Crepidula plana Say. Journal of Experimental Marine
Biology and Ecology, 90:55-71.
Mormul, R.P., Algren, J., Ekvall, M.K., Hansson, L-A. and Brönmark, C. 2012. Water
brownification may increase the invasibility of a submerged non-native macrophyte.
Biological Invasions, 14:2091-2099.
Nicolle, A., Hallgren, P., von Einem, J., Kritzberg, E.S., Granéli, W., Persson, A., Brönmark,
C. and Hansson, L-A. 2012. Predicted warming and browning affect timing and magnitude
of plankton phenological events in lakes: a mesocosm study. Freshwater Biology, 57:684695.
Noffke, N., Gerdes, G. and Klenke, T. 2003. Benthic cyanobacteria and their influence on the
sedimentary dynamics of peritidal depositional systems (siliciclastic, evaporitic salty, and
evaporitic carbonatic). Earth-Science Reviews, 62:163-176.
Olsson, T.I. 1988. The effect of wintering sites on survival and reproduction of Gyraulus
acronicus (Gastropoda) in a partly frozen river. Oecologia, 74:492-495.
Reece, J., Urry, L., Cain, M., Wasserman., S, Minorsky, P and Jackson, R. 2011. Campbell
biology. Pearson educations, San Fransisco. 1309 pages.
Rosa, J., Ferreira, V., Canhoto, C. and Graca, M.A.S. 2013. Combined effects of water
temperature and nutrients concentration on periphyton respiration - implications of
global change. International Review of Hydrobiology, 98:14-23.
Shurin, J.B., Clasen, J.L., Greig, H.S., Kratina, P. and Thompson, P.L. 2012. Warming shifts
top-down and bottom-up control of pond food web structure and function. Philosophical
Transactions of the Royal Society B-Biological Sciences, 367:3008-3017.
Swedish Commission on Climate and Vulnerability. 2007. Sweden facing climate change –
threats and opportunities. Edita Sverige AB, Stockholm. 679 pages.
Thomas, M.K., Kremer, C.T., Klausmeier, C.A. and Litchman, E. 2012. A Global Pattern of
Thermal Adaptation in Marine Phytoplankton. Science, 338:1085-1088
Vis, C., Cattaneo, A. and Hudon, C. 1998. Periphyton in the Clear and Colored Water Masses
of the St. Lawrence River (Quebec, Canada): A 20-Year Overview. Journal of Great Lakes
research, 24:105-117.
Winder, M. and Sommer, U. 2012. Phytoplankton response to a changing climate.
Hydrobiologia, 698:5-16.
Woodward, G., Perkins, D.M. and Brown, L.E. 2010. Climate change and freshwater
ecosystems: impacts across multiple levels of organization. Philosophical Transactions of
the Royal Society B-Biological Sciences, 365:2093-2106.
Økland, J. 1990. Lakes and snails: Environment and Gastropoda in 1500 Norwegian lakes,
ponds and rivers. Universal book service /Dr. W. Backhuys, Oestgeest. 516 pages.
13
Appendix
Appendix A. Table with results from ANOVAs.
Response
variable
Data set
Factors
D.f.
F
p
Snail growth rates
Whole set
Snail growth rates
Bottom cages
Temperature
TOM
Depth
Temperature*TOM
Temperature*depth
TOM*depth
Temperature*TOM*depth
Temperature
TOM
Temperature*TOM
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
1, 12
1, 12
1, 12
1.234
2.170
1.017
0.004
0.072
0.496
0.007
1.054642
0.327496
0.011608
0.278
0.154
0.323
0.953
0.791
0.488
0.933
0.324697
0.577701
0.91598
Snail growth rates
Shallow cages
Temperature
TOM
Temperature *TOM
1, 12
1, 12
1, 12
0.323298
2.158638
0.323298
0.580118
0.167493
0.580118
Snail survival
Whole set
Snail survival
Bottom cages
Temperature
TOM
Depth
Temperature*TOM
Temperature*depth
TOM*depth
Temperature*TOM*depth
Temperature
TOM
Temperature*TOM
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
1, 12
1, 12
1, 12
0.900
4.900
0.400
4.900
1.600
3.600
0.400
0.04918
8.311475
1.229508
0.352
0.037
0.533
0.037
0.218
0.070
0.533
0.828225
0.013755
0.289231
Snail survival
Shallow cages
TOM
Temperature
Temperature*TOM
1, 12
1, 12
1, 12
0.050847
2.491525
4.118644
0.82539
0.140445
0.065192
Snail total biomass
Whole set
Snail total biomass
Bottom cages
Temperature
TOM
Depth
Temperature*TOM
Temperature*depth
TOM*depth
Temperature*TOM*depth
Temperature
TOM
Temperature*TOM
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
1, 12
1, 12
1, 12
1.974
4.672
1.427
4.066
2.401
1.175
0.177
0.012283
6.187215
1.495733
0.173
0.041
0.244
0.055
0.134
0.289
0.678
0.913585
0.028567
0.244804
Snail total biomass
Shallow cages
Temperature
TOM
Temperature*TOM
1, 12
1, 12
1, 12
3.799182
0.505315
2.730298
0.075039
0.49076
0.124366
POC production
Whole set
Temperature
TOM
Depth
Temperature*TOM
Temperature*depth
TOM*depth
Temperature*TOM*depth
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
2.331
0.073
4.114
0.911
0.119
1.185
0.889
0.140
0.789
0.054
0.349
0.734
0.287
0.355
14
POC production
Bottom cages
TOM
Temperature
Temperature*TOM
1, 12
1, 12
1, 12
0.593001
0.448848
1.155979
0.456154
0.515568
0.303444
POC production
Shallow cages
TOM
Temperature
Temperature*TOM
1, 12
1, 12
1, 12
0.756605
3.957197
0.000152
0.401457
0.069959
0.990367
Chl-a production
Whole set
Temperature
TOM
Depth
Temperature*TOM
Temperature*depth
TOM*depth
Temperature*TOM*depth
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
4.278
0.091
0.306
0.059
2.088
0.249
0.039
0.050
0.765
0.585
0.811
0.161
0.622
0.846
Chl-a production
Bottom cages
TOM
Temperature
Temperature*TOM
1, 12
1, 12
1, 12
1.505875
0.912409
0.004822
0.243301
0.358323
0.945785
Chl-a production
Shallow cages
TOM
Temperature
Temperature*TOM
1, 12
1, 12
1, 12
0.010852
3.453523
0.053896
0.918752
0.087809
0.820329
Periphyton
production
Control cages
Temperature
TOM
Depth
Temperature*TOM
Temperature*depth
TOM*depth
Temperature*TOM*depth
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
0.953
0.046
18.618
2.608
0.974
4.651
0.023
0.339
0.831
0.000
0.119
0.333
0.041
0.881
Periphyton
production
Bottom control
cages
TOM
Temperature
Temperature*TOM
1, 12
1, 12
1, 12
0.031887
3.249671
0.214245
0.861254
0.09659
0.651742
Periphyton
production
Shallow control
cages
TOM
Temperature
Temperature*TOM
1, 12
1, 12
1, 12
2.024153
5.256144
0.238636
0.180288
0.040737
0.633998
Periphyton
production
Snail cages
Temperature
TOM
Depth
Temperature*TOM
Temperature*depth
TOM*depth
Temperature*TOM*depth
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
1, 24
1.606
0.510
6.233
1.472
0.038
7.643
2.931
0.217
0.482
0.020
0.237
0.847
0.011
0.100
Periphyton
production
Bottom snail cages
TOM
Temperature
Temperature*TOM
1, 12
1, 12
1, 12
3.238159
0.669967
2.510377
0.097117
0.429018
0.139084
Periphyton
production
Shallow snail cages
TOM
Temperature
Temperature*TOM
1, 12
1, 12
1, 12
0.67801
0.528878
2.680875
0.426335
0.481027
0.127497
15
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