Download Does an evolutionary change in the water sowbug Asellus aquaticus

Department of Physics, Chemistry and Biology
Final Thesis
Does an evolutionary change in the water sowbug
Asellus aquaticus L. alter its functional role?
Md. Maidul Islam Choudhury
LiTH-IFM- Ex--11/2419--SE
Supervisor : Anders Hargeby, Linköping University
Examiner : Bo Ebenman, Linköping University
Department of Physics, Chemistry and Biology
Linköpings universitet
SE-581 83 Linköping, Sweden
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Presentation Date
Department and Division
IFM Biology
27.05.2011
Publishing Date (Electronic version)
07.02.2012
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ISRN: LiTH-IFM- Ex--11/2419--SE
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Publication Title
Does an evolutionary change in the water sowbug Asellus aquaticus L. alter its functional role?
Author(s)
Md. Maidul Islam Choudhury
Abstract
The ecology behind evolutionary diversification is a well studied area of research, whereas the effects
of evolution on ecosystems get little attention. In line with ecological theory, evolutionary
diversification of a species could influence different ecosystem aspects such as food web composition,
energy flow, nutrient cycling etc. The main objective of this study was to investigate whether two
diverging ecotypes (reed and chara) of Asellus aquaticus differ regarding their role in two aquatic
ecosystem processes: decomposition of terrestrial leaves and grazing of periphyton. Their role in
ecosystem process as well as treatment effects on fitness, measured as growth and survival, were
investigated in a laboratory experiment with various levels of intra-specific competition and
inter-specific interactions with the amphipod Gammarus pulex. The isopods were collected from two
Swedish lakes: Lake Tåkern and Lake Fardume. These two lakes represent different history of ecotype
divergence. The experimental design consisted of 2-L aquaria, each providing elm leaves (Ulmus
glabra), oak leaves (Quercus roburleaves) and periphyton as food sources. Ten treatments with five
replicates were applied for each lake and the experiment lasted for four weeks. The study showed that
there was no significant difference between chara and reed ecotype in their functional role. However,
the rate of ecosystem processes per individual decreased in competitive interactions. In high density,
decomposition per dry weight consumer was low and total algae biomass was high at the end of four
weeks due to intra-specific competition. Moreover, ecosystem processes were lowest in inter-specific
competition between Gammarus pulex and each ecotype. Present study also shows that ecotypes from
the different lakes, having different history, had different responses to mortality and growth.
Keywords
Asellus aquaticus, eco-evolutionary dynamic, ecosystem process, Gammarus pulex, intra-specific,
inter-specific.
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Abstract ………………………………………………………………………………..
Introduction ……………………………………………………………………………
2.1
Objective of the project ……………………………………………………….
Material and methods ...………………………………………………………………..
3.1
Study organisms …...………………………………………………………….
3.2
Periphyton …………………………………………………………………….
3.3
Leaves ………………………………………………………………………...
3.4
Experimental set-ups ………………………………………………………….
3.5
Measurements of periphytic algae biomass, decomposition and animal
interactions ……………………………………………………………………
3.5.1
Algae biomass ……………………………………………………….
3.5.2
Decomposition ………………………………………………………
3.5.3
Species interactions …………………………………………………
3.6
Statistical analysis …………………………………………………………….
Results …………………………………………………………………………………
4.1
Periphytic algae biomass ……………………………………………………...
4.2
Leaf decomposition …………………………………………………………...
4.3
Mortality ………………………………………………………………………
4.4
Growth ………………………………………………………………………..
Discussion ……………………………………………………………………………..
5.1
Preiphytic algae biomass ……………………………………………………...
5.2
Leaf decomposition …………………………………………………………...
5.3
Mortality ………………………………………………………………………
5.4
Growth ………………………………………………………………………..
Conclusion …………………………………………………………………………….
Acknowledgement …………………………………………………………………….
References ……………………………………………………………………………..
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1 Abstract
The ecology behind evolutionary diversification is a well studied area of research, whereas
the effects of evolution on ecosystems get little attention. In line with ecological theory,
evolutionary diversification of a species could influence different ecosystem aspects such as
food web composition, energy flow, nutrient cycling etc. The main objective of this study was
to investigate whether two diverging ecotypes (reed and chara) of Asellus aquaticus differ
regarding their role in two aquatic ecosystem processes: decomposition of terrestrial leaves
and grazing of periphyton. Their role in ecosystem process as well as treatment effects on
fitness, measured as growth and survival, were investigated in a laboratory experiment with
various levels of intra-specific competition and inter-specific interactions with the amphipod
Gammarus pulex. The isopods were collected from two Swedish lakes: Lake Tåkern and Lake
Fardume. These two lakes represent different history of ecotype divergence. The experimental
design consisted of 2-L aquaria, each providing elm leaves (Ulmus glabra), oak leaves
(Quercus roburleaves) and periphyton as food sources. Ten treatments with five replicates
were applied for each lake and the experiment lasted for four weeks. The study showed that
there was no significant difference between chara and reed ecotype in their functional role.
However, the rate of ecosystem processes per individual decreased in competitive
interactions. In high density, decomposition per dry weight consumer was low and total algae
biomass was high at the end of four weeks due to intra-specific competition. Moreover,
ecosystem processes were lowest in inter-specific competition between Gammarus pulex and
each ecotype. Present study also shows that ecotypes from the different lakes, having different
history, had different responses to mortality and growth.
Key words: Asellus aquaticus, eco-evolutionary dynamic, ecosystem process, Gammarus
pulex, intra-specific, inter-specific.
2 Introduction
Evolutionary Biology mainly focuses on the ecological explanation of evolutionary
diversification, whereas the effects of evolution on ecosystems get little attention (Thompson
1998, Fussmann et al. 2007, Yoshida et al. 2003). Although, some ecologists in 1950s and
1960s formally hypothesized the influence of evolution on ecology, it took time for biologists
to test these influences specifically. Industrial melanism in peppered moths (Biston betularia)
is perhaps the best well known example of ecological influence on evolution (Pelletier et al.
2009). Previous studies on various systems, such as sparrows in North America (Johnston &
Selander 1964), mice in islands (Berry1964), Caribbean Anolis lizard (Losos 2009),
Galapagos finches (Grant and Grant 2008) or African cichlids (Seehausen et al. 2008)
concentrated on how environmental factors regulate the speciation and adaptation of species.
Moreover, recent studies (Schluter 2000; Seehausen et al. 2008) revealed that adaptive
radiation is influenced by ecological factors. However, Luke et al 2009 showed that adaptive
radiation also significantly affects the ecosystem over a short period of time. In line with
ecological theory, evolutionary diversification of a species can shape different ecosystem
aspects such as predator–prey interactions, community composition, food web structure,
energy flow, nutrient cycling, productivity etc. (Luke et al 2009; Pelletier et al. 2009; Loreau
et al. 2001; Schluter 2000; Seehausen et al. 2008 ;Abrams 2000; Palkovacs and Post 2009).
To regret, generally, little attention is paid to the influence of evolution on ecology at
short-time scale. Pelletier et al. 2009 mentioned two general reasons behind it: the challenges
of measuring feedbacks between evolution and ecology; scientists’ assumption that
evolutionary process is too slow to exert changes in ecological processes. However, many
empirical studies on contemporary evolution and eco-evolutionary dynamics have recently
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presented, for example, on the Darwin finches (reviewed by Hairston et al. 2005), Trinidadian
guppies (Palkovacs et al. 2009), Alewives study (Post & Palkovacs 2009), Populus tree
(Bailey et al. 2009) and interaction between rotifer and algae (Yoshida et al. 2003; Jones et
al. 2009), that evolution can occur in nature within short time-scale which has potential to
change the ecosystem processes.
Like most biological processes genes, the evolution of phenotypic traits and
demographic rates are interacting as an integrated system (Pelletier et al. 2009). Changes in
one part can influence many levels (Coulson et al. 2006a) of the system. This can be
expressed in many ways (e.g. Coulson et al. 2006a; Fussmann et al. 2007; Bailey et al. 2009;
Post & Palkovacs 2009), but the main theme is a relationship among fitness, phenotype and
genes which could be illustrated as a simple eco-evolutionary dynamics (Fig. 1). Natural
selection and population dynamics are intimately associated (Coulson et al. 2006b; Pelletier et
al. 2009). For example, if natural selection translates into changes in phenotypic traits (e.g.
body size, pigmentation), that will effect population through reproduction, survival or growth.
Thus, in turn, natural selection will influence population dynamics. Finally, many ecosystems
services e.g. decomposition, nutrient cycling and, primary productivity are modified due to
changes in the numbers of individuals, their utilization of available resources and efficiency
of resource utilization (Thompson 1998) and interaction with other species in the food web .
Accordingly, laboratory experiments and field studies of natural population suggest habitat
quality mediated genetic variance (reviewed in Hoffmann & Merilä 1999; Charmantier &
Garant 2005).
Evolutionary changes of
phenotypic traits
(e.g. body size, color)
Ecosystem aspects
(Decomposition, primary
production, intra and
interspecific interactions)
Population dynamics
(e.g. Reproduction,
survival, growth)
Figure 1: Conceptual framework of eco-evolutionary dynamics.
In freshwater ecosystems there is a wide range of interactions between individuals and
species for instance in macroinvertebrate communities (Wellborn 2002; Wellborn et al.
1996). Beside predation, competition itself has potential to affect species composition or
community structure and species identity (Brown 1982). In high density, individuals within a
species compete with each other for available resources (e.g. food) whereas inter-specific
competition occurs in presence of more than one species. An interference effect results from
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heavy intra-specific competition among the individual within a species as well as interspecific competition between two or more species. In this case, increased density of
interacting animals reduces the feeding or grazing rate. (Brown et al 1994, Soluk 1993). On
the contrary, interaction hypothesis (Jonsson and Malmqvist 2000) states that intra-specific
competition will be reduced in an addition of another species which in turn, will decrease the
biomass of shared resources in great extent. Same scenario can be obtained from facilitation
where one or more species is benefited from foraging together (Wilson et al 1999, Jonsson
and Malmqvist 2003). So, intra- and inter-specific interactions have not only negative effect
but also positive effect on growth, survival or fecundity. However, the result of competition is
hard to predict because of its dependency on type of interaction and involved species
(Hertonsson 2010).
Recent studies show that the freshwater isopod Asellus aquaticus (Crustacea) differ
locally in pigmentation within two Swedish lakes, Lake Tåkern and Lake Krankesjön
(Hargeby et al. 2004; 2005; Eroukhmanoff et al. 2009). Both lakes have experienced
periodical shift between submerged vegetation dominance and phytoplankton dominance
(Blindow et al. 1993). In these lakes, isopods show lighter pigmentation in submerged
vegetation dominated by stoneworts (Chara spp.) whereas, in adjacent stands of reed
(Phragmites australis) and great fen sedge (Cladium mariscus L.) dark isopods are abundant.
In addition, the bright A. aquaticus population is smaller in size than that of dark population
(Eroukhmanoff et al. 2009). These different phenotypes resulted from evolutionary responses
to local differences in natural selection. Hargeby et al. 2004 showed that this phenotypic
difference has a genetic basis where diet and chromatophore adjustment to background color
play a minor role. Moreover, they summarized that this genetic difference occurred during the
colonization in a novel habitat, a situation that is known to promote adaptive evolution. In
addition, rapid parallel divergence in the source habitat (reed stands) as well as phenotypic
convergence in novel habitat (stonewotrs habitat) were also documented in these two lakes
(Eroukhmanoff et al. 2009). In general, microevolutionary changes can occur in nature over
short time-scales (Reznick and Ghalambor 2001).
Lake Tåkern and Krankesjön shifted from phytoplankton dominant state to
macrophyte state during the last 20 years and two ecotypes (reed ecotype and stoneworts
ecotype) of Asellus emerged within this time-scale (Hargeby et al. 2004). However, similar
differentiation has also been noted in other lake, Lake Fardume, with a different history
(Hargeby et al. 2004). Lake Tåkern experienced alternative stable state during its lake-history.
It became phytoplankton dominant (turbid stage) during 1995-1997 (Blindow et al. 1998) and
again colonized by Chara spp. (clear water stage) in 1999 (Hargeby et al. 2004). However,
Lake Fardume does not experience such periodic shift. It is always in clear water stage during
its lake-history. Moreover, genetic distance between the populations of two ecotypes of
Asellus is higher between Lake Tåkern and Fardume than within the lakes (Eroukhmanoff et
al. 2009). So, in this study Lake Tåkern and Lake Fardume were selected for isopods
collection because of their different lake history. This will also provide an opportunity to
examine whether lake of origin has any signature in functional role as well as fitness of the
both ecotypes of Asellus.
Asellus aquaticus is a general freshwater isopod found in shallow lakes, ponds and
slowflowing waterbodies in Europe and Asia (Whitehurst, 1991; Verovnik et al., 2005).
Asellus are commonly detritivores (Smock and Harlowe 1983) and feed on decaying leaves
(Zimmer and Bartholme´ 2003). This food source is likely to be important in reed habitat,
where bottom substrate is mainly decaying parts of emergent vegetation (Hargeby et al.
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2005). However, isopods colonized in stonewort habitat are more likely to feed on epiphytic
algae e.g. periphyton (Arakelova 2001). If these expectations of local differences in feeding
are true, the colonization in new habitat changed the functional role of the isopods, from
detritivores to mesograzers.
2.1 Objective of the project
The main objective of this project was to identify whether the evolutionary diversification of
Asellus aquaticus affects its ecological function. My hypothesis was that these two ecotypes
differ in their role as a grazer of epiphyton, or detritivore on coarse detrititus such as leaves.
The role was tested both as the ecotype was living alone and in co-existence with other
ecotype and with another macroinvertebrate, amphipod Gammarus pulex.
3 Materials and methods
Lake Tåkern (58o 21´ N, 14o 50´ E) and Lake Fardume träsk(57o46´ N, 18o54´E) are located
in Sweden. Both lakes are shallow and Lake Fardume is more oligotrophic in nature. Data on
water chemistry is available on the web at http//www.ma.slu.se. Isopods were collected randomly from the following locations: in Lake Tåkern chara ecotype was collected from 58 o35´
04´´ - 14 o 78´07´´ and reed ecotype from 58 o 33´21´´-14 o 81´88´´; in Lake Fardume chara
ecotype was collected from 57 o 78´47´´ - 18 o 91´28´´ and reed ecotype from 57 o 78´03´´-18 o
91´07´´.
3.1 Study organisms
Two ecotypes (Reed and Chara) of Asellus were collected from both lakes. Amphipod
Gammarus pulex was collected from near by stream of Linköping University. No specific
empirical study has done about the food of these two ecotypes of Asellus. Although it is
assumed that reed ecotype is predominantly detritivore and periphyton is regarded as
important food source for chara ecotype. So, my assumption was that chara ecotype acts as
grazer whereas, reed ecotype is detritivore. However, the amphipod Gammarus pulex is both
grazer and detritivore (Gladhill et al. 1993). In each lake, reed ecotypes were collected from
reed stands while chara ecotypes from adjacent stonewort stand. All experimental animals
were collected by means of hand net.
Macroinvertebrates were kept in the laboratory in separate aerated aquaria filled with
water from Lake Tåkern, supplied with periphyton and dead leaves as food. All experimental
animals kept at least 3 week before the experiment start in order to adapt to the laboratory
conditions.
3.2 Periphyton
Tiles of (100x100) mm size were prepared to act as a refuge and substrate for periphyton. In
order to offer shelter to the test animals the tiles were elevated approximately 10mm by fixing
small silicon rubber tube with silicon glue. In each tube sufficient opening was made by
means of cutting to avoid death of isopods due to trapping inside the tube. Four weeks prior to
the experiment start one tile was placed in each experimental aquarium. Initially, periphyton
was collected from plants from Lake Tåkern and the surface of rocks from the stream where
Gammarus pulex was collected. Periphyton was then mixed into an algae inoculum that was
added to each experimental aquarium along with fluid fertilizer (Blomstra, Cederroth,
Sweden; P:N:1:5) to the concentration of 50μg P l-1 and 250 μg N l-1 (Hertonsson 2010). As
the periphyton stopped growing before the start of the final experiment, the aquarium-water
was replaced by filtered (400 µm mesh) lake water from Tåkern. The idea was to maintain
more natural condition in term of water quality and nutrient. At the end of the experiment
8
periphyton on tiles was cleaned with a soft toothbrush and rinsed with dechlorinated tap water
into separate containers then filtered onto a Whatman GF/C filter (pore size 1.2µm).
Chlorophyll a was analysed according to the methodology of Jespersen and Christoffersen
(1987) with extraction with ethanol and absorbance measured at 750 and 665 nm by means of
a Hitachi spectrophotometer (model: U-2000).
3.3 Leaves
Elm leaves (Ulmus glabra) and oak (Quercus roburleaves) leaves were collected recently
fallen to the ground in September and November respectively, and dried in 60oC for 48 h.
Then they were soaked so that they would not float and shad the periphyton covered tile. One
week before to the experiment start, 0.99 (±0.03) g(DW) elm and 0.38 (±0.03) g (DW) oak of
soaked leaves were added to each experimental aquarium. Oak leaves were added to provide
secondary food source as they decay slowly compare to elm leaves. At the end of the
experiment leaves were again dried in 60oC for 48 h and weighed. Leaf weight was adjusted
in term of moisture absorption by using standard leave weight.
3.4 Experimental set-ups
The experiment was conducted in the green house at Biology Department, Linköping
University over four weeks between November and December, 2010. For each lake there
were 10 different treatments. Protocols were: low density single species/ecotype (6
individuals); high density single ecotype/species (18 individuals); combination of both
ecotypes (6 individuals from each); a combination of one ecotype and Gammarus pulex (6
individuals of each.) and three-form combination of both ecotypes and Gammarus pulex (6
individuals of each.) (Table 1). All the treatments were replicated five times for each lake. So,
the experimental set-up was consisted of total 100 aerated plastic experimental aquaria (l x w
x d: 200 x 170 x 100 mm) filled with 2 L of filtered (400 µm mesh) lake water from Tåkern.
Each aquarium accommodated one periphyton covered tile and leaves. The aquariums were
grouped into ten blocks and placed on two tables. Each block contained all the ten treatments.
First table contained 3 blocks from Lake Tåkern and 2 blocks from Lake Fardume and second
table contained 3 blocks from Lake Fardume and 2 blocks from Lake Tåkern.
Table 1. Schematic illustration of the experimental set-up (C = chara ecotype of Asellus
aquaticus (grazer), R = reed ecotype of Asellus aquaticus (detritivore), G = Gamarrus pulex
(grazer- detritivore))
Treatment
C
R
G
C+R
C+G
R+G
C+R+G
3xC
3xR
3xG
No. of individual
6
6
6
6+6
6+6
6+6
6+6+6
6+6+6
6+6+6
6+6+6
In every second day 50ml of fish cue was added in each aquarium to maintain natural
predation environment in the aquarium (Hertonsson 2010). Fish cue was collected from a
water tank containing Perch (Perca fluviatilis) which is a benthivorous fish species noted to
feed on Asellus in both chara and reed habitats of shallow Swedish lakes (Rask & Hiisivuori
1985). The fishes were fed with live Asellus and Gammarus. The day night regime was set to
9
12:12 h. Water temperature was 17 oC to 19 oC. The light intensity above the aquaria was
measured by irradiameter (Kahl scientific instrument corporation, USA, model: 268 WA
310). In the first table, containing the three of the five blocks, the average light intensity was
9057μW whereas, in second table it was 9596μW. The difference in radiation among the
aquaria was anticipated to be minor and randomly distributed among treatments.
3.5 Measurements of periphytic algal biomass, decomposition and animal interactions
3.5.1 Algal biomass
The biomass of the periphytic algae on the tile from each aquarium was measured in
term of amount of Chlorophyll a (chl a)(μg) at the end of the experiment.
3.5.2 Decomposition
At the end of the experiment the remaining leaves from each experimental aquarium was
collected, dried and, weighed. The reduction of leaf mass (mg) was used as a measure of
decomposition. Leaf decomposition was measured for both elm and oak leaves separately.
Decomposition = (Leaf start- Leaf end)…………………. (1)
As macroinvertebrate species differ in size, decomposition was calculated per dry weight
(DW)(mg) consumer.The following length-weight relationships were used to for Asellus
aquaticus to calculate DW of the isopods (Hass et al. 2007).
ln (Weight) = -4.212+ 2.268* ln (Length)……………. (2)
For Gammarus pulex, thirty individuals were photographed and their bend length was
analyzed with ImageJ v. 1.37v. The following regression equation was constructed by BoxCox transformation of the response with specified lambda = 0 in Minitab 16.
ln (Weight) = -1,24998 + 0,239452 Length………… (3)
3.5.3 Species Interactions
As a measure of species interactions mean growth and proportional mortality were
used. All experimental animals were photographed at the start and end of the experiment.
Animal size (body length) was analyzed with ImageJ v. 1.37v (http://rsbweb.nih.gov/ij)
(Franken et al. 2005). Growth and proportional mortality were calculated according to:
Growth= (Length end -Length start)………………..(4)
Proportional mortality = (n start – n end)/ n start ………………..(5)
Where n= number of individuals
3.6 Statistical analysis
First, one-way ANOVA analysis was done to check the general differences among the ten
treatments (listed on Table 1) in the four response variables: periphytic algae biomass,
decomposition, mortality and growth respectively. Then more specific analysis was done by
means of three-way ANOVA to find out the specific effects, and their interactions, of lakes,
ecotypes and three types of competition on the above response variables. More specifically,
the factors were ecotype (chara and reed ecotypes of Asellus), lake of origin (Tåkern and
10
Fardume) and three competition treatments such as, low competition (C, R); intra-specific
competition (3*C, 3*R); inter-specific competition (C+G, R+G). The lower number of
Gammarus (6 indv.) added in the inter-specific treatment compared with Asellus (12 indv.) in
the intra-specific treatment was compensated by a higher individual biomass of Gammarus.
Following issues were examined through three-way ANOVA: functional differences between
two ecotypes from both lakes; whether the ecotypes from both lakes show any competition
effect (or density dependence) on the response variables mentioned above and finally, their
responses to functional role and fitness in presence of an additional competitor, Gammarus
pulex.
Before the analyses were performed, data were tested for normal distribution
(Anderson-Darling goodness-of-fit statistic) and equality of variance (Levenes test). In
ANOVA, data from the treatments C+(R) (for mortality); R+(C+G) and 3*G (for growth)
were not normally distributed but had equal variances (Levenes test). So, data from those
treatments were not log transformed to avoid negative mortality and growth values in the
model. All the statistical analyses were done in Minitab 16.
4 Results
4.1 Periphytic algal biomass
There was no general difference between chara and reed Asellus ecotypes regarding effects on
periphytic algal biomass on the experimental tiles at the end of experiment (Fig. 2; Table 2).
Periphyton biomass was not significantly different among the single species/ecotype
treatments (One-way ANOVA; C vs R, C vs G and R vs G; Fig. 2). The amount of algae
biomass was significantly higher (Fig. 2) in both of the inter-specific treatments than single
ecotype treatments (One-way ANOVA, F1,18=12.52, P=0.002 and F1,18= 7.92, P= 0.011
respectively). So, the presence of Gammarus pulex tended to increase the algae biomass on the
tiles. The same pattern could be seen in the C+R+G treatment in which periphyton biomass
was significantly higher (Fig. 2) than in the intra-specific Asellus treatments (3*C, 3*R) (Oneway ANOVA, F1,18= 4.61, P= 0.046 and F1,18=5.04, P= 0.038 respectively). However,
Gammarus pulex showed no significant difference between inter-specific and intra- specific
treatments (F1,18=0,56 and P= 0,464).
11
A three factor ANOVA showed no significant difference between chara and reed ecotypes in
their effects on periphytic algae. Similar result was observed for the ecotypes from both Lake
Tåkern and Lake Fardume (Table 2, Fig. 3a). However, the amount of chl a was significantly
different among the three selected competition treatments (Table 2). It was highest in the
inter-specific treatment, relatively lower in intra-specific treatment. In contrast, it was
inconsistent in low-competition treatment for two ecotypes (Fig. 3b).
Table 2. Three factors ANOVA on the effect of Asellus ecotypes, lakes from which Asellus
were collected and competition (single ecotype at two densities and along with Gammarus
pulex) on periphytic algal biomass at the end of the experiment.
Source
Ecotype
Lake
Competition
Ecotype*Lake
Ecotype*Competition
Lake*Competition
Ecotype*Lake*Competition
Error
Total
DF
1
1
2
1
2
2
2
48
59
Seq SS
0.0000026
0.0000103
0.0013929
0.0000193
0.0000510
0.0000398
0.0000038
0.0024980
0.0040177
MS
0.0000026
0.0000103
0.0006964
0.0000193
0.0000255
0.0000199
0.0000019
0.0000520
F
0.05
0.20
13.38
0.37
0.49
0.38
0.04
P
0.823
0.658
0.000
0.545
0.616
0.684
0.964
In line with treatment effect (Fig. 2), both chara and reed ecotypes showed a positive impact
on algal biomass when an additional competitor, Gammarus pulex, was added in the interspecific treatment (Fig. 3b). Similar pattern was observed in both lakes (Fig. 3c). Finally, no
interaction effect of selected factors was evident for algal biomass (Table 2).
12
25
20
15
10
5
3*
G
3*
R
3*
C
C
+R
+G
+G
R
+G
C
+R
C
G
R
0
C
Decomposition/DW(mg)
4.2 Leaf decomposition
The experimental animals only fed on elm leaves during the four week of incubation and no
decomposition of oak leaves was found at the end of the experiment. So, leaf decomposition/
DW consumer was measured for elm leaves only. I found no difference between chara and
reed ecotypes in decomposition per DW (dry weight) consumer (Fig. 4 and Table 3). However, combined effect of chara and reed ecotypes on decomposition was significantly lower
(One-way ANOVA, F1,18= 28.59; P<0.001 and F1,18=17.26; P<0.001) than their individual
effect. Decomposition did not differ significantly when the two ecotypes co-existed with
Gammarus pulex (Fig. 4; One-way ANOVA, F1,18= 0,25 and P= 0,623). In the high density
treatments, both chara and reed ecotypes had significantly higher (One-way ANOVA, F1,18=
Treatments
Figure 4. Elm (Ulmus glabra) leaf decomposition/DW consumer at the end of experiment,
after four weeks incubation. Means+sd, n=10 (abbreviations according to Fig. 2).
114.28; P<0.001 and F1,18= 113.59; P< 0.001) leaf decomposition in intra-specific treatment
than inter-specific treatment. Gammarus pulex also had significantly higher leaf
decomposition in intra-specific competition than inter-specific competition (Fig. 4). However,
the individual effect of isopod and amphipod on leaf decomposition in inter-specific treatment
was unknown and decomposition by microbes was not examined in the current study.
Three factors ANOVA analysis also showed no significant difference in leaf
consumption/DW consumer between chara and reed ecotypes irrespective of competition and
lake history (Table 3). Lake of origin also showed no significant effect on leaf decomposition
(Table 3 and Fig. 5a). However, the difference in leaf decomposition among the three selected
competition treatments is highly significant (Fig. 5b and Table 3). In the low-competition
treatment, chara as well as reed ecotype resulted in highest leaf consumption. However, the
leaf decomposition/DW consumer in low-competition was marginally significantly higher for
chara ecotype than reed ecotype (Table 3). But the three factor interaction among lake,
ecotype and competition indicate that actually this tendancy may only relevant for one of the
lakes.
The presence of Gammarus pulex tended to decrease the decomposition process for
both ecotypes. Finally, three-way interaction among the factors showed that both chara and
reed ecotypes from Lake Fardume had high leaf consumption than those from Lake Tåkern
when the ecotypes existed in low density.
13
Table 3. Three factors ANOVA on the effect of Asellus ecotypes, lakes from which Asellus
were collected and competition (single ecotype at two densities and along with Gammarus
pulex) on leaf decomposition/DW consumer.
Source
Ecotype
Lake
Competition
Ecotype*Lake
Ecotype*Competition
Lake*Competition
Ecotype*Lake*Competition
Error
Total
DF
1
1
2
1
2
2
2
48
59
Seq SS
10,73
18,51
1214,86
0,01
42,28
2,39
50,98
360,97
1700,74
MS
10,73
18,51
607,43
0,01
21,14
1,20
25,49
7,52
F
1,43
2,46
80,77
0,00
2,81
0,16
3,39
P
0,238
0,123
0,000
0,971
0,070
0,853
0,042
4.3 Mortality
In general, chara and reed ecotypes did not differ in mortality (Fig. 6; Table 4). One-way
ANOVA results showed that chara and reed ecotypes did not have any impact on the
mortality of each other. Similarly, Gammarus pulex had no significant influence on the
mortality of any of the two ecotypes (Fig. 6) of Asellus.
Three factors ANOVA showed that lake of origin had significant effect (Table 4) on
the mortality of the isopods, but this effect differed between the ecotypes, shown by
significant interaction between ecotype and lake. Mortality tended to be higher in the chara
ecotype than reed ecotype among the isopods from Lake Tåkern, whereas, among the isopods
from Lake Fardume the chara ecotype had lower mortality than reed ecotype (Fig. 7a; Table
4). So, ecotypes from different lakes had different responses to mortality.
14
1
0,8
0,6
0,4
0,2
3*
G
3*
R
G
C+
(R
)
(C
)+
R
C+
(G
)
(C
)+
G
R+
(G
)
(R
)+
C+ G
(R
+G
R+
)
(C
+G
)
G+
(R
+C
)
3*
C
R
0
C
Proportional mortality
The three selected competition treatment also had significant effect on the mortality of
isopods (Table 4). This effect tended to differ in lake of origin which is indicated by
significant interaction between lake and competition treatment but not in ecotype level (Table
Treatments
Figure 6. Proportional mortality of animals at the end of experiment, after four weeks
incubation. Means+sd, n=10. Alphabet without parenthesis indicates the mortality of that
species/ecotype in the combination (abbreviations according to Fig. 2).
4; Fig. 7b & 7c). Mortality was lowest in low-competition (or low density) treatment and
higher in intra-specific competition (or high density) followed by inter-specific competition
(or mixed species) treatment (Fig. 7b). Both ecotypes showed density dependence on
mortality. However, the addition of Gammarus pulex tended to increase the difference on
mortality between two ecotypes. Chara ecotype had higher mortality than reed ecotype when
co-existed with Gammarus pulex. In general, lake of origin tended to influence the mortality
of the isopods.
15
Table 4. Three factors ANOVA on the effect of Asellus ecotypes, lakes from which Asellus
were collected and competition (single ecotype at two densities and along with Gammarus
pulex) on the mortality of the ecotypes.
Source
Ecotype
Lake
Competition
Ecotype*Lake
Ecotype*Competition
Lake*Competition
Ecotype*Lake*Competition
Error
Total
DF
1
1
2
1
2
2
2
48
59
Seq SS
0.02882
1.18363
0.17283
0.29454
0.00899
0.19888
0.03084
1.12018
3.03873
SS
0.02882
1.18363
0.17283
0.29454
0.00899
0.19888
0.03084
1.12018
MS
0.02882
1.18363
0.08642
0.29454
0.00449
0.09944
0.01542
0.02334
F
1.23
50.72
3.70
12.62
0.19
4.26
0.66
P
0.272
0.000
0.032
0.001
0.825
0.020
0.521
4.4 Growth
Chara and reed ecotypes had no significant different in growth (Fig. 8 and Table 5). One-way
ANOVA results showed no difference between chara and reed ecotypes both in low density
(C vs R) and high density (3*C vs 3*R) (Fig. 8). Moreover, Gammarus pulex did not
influence the growth of chara ecotype as well as reed ecotype. Similarly, chara and reed
ecotypes did not influence the growth of one another. Additionally, in high density, intraspecific and inter-specific treatments had no significant impact on the growth of two ecotypes
(Fig. 8).
Growth(mm)
2,5
2
1,5
1
0,5
3G
3R
3C
)
)
+C
R
G
+(
C+
G
)
R
+(
R+
G
)+
G
C
+(
G
)
(R
+(
R
)+
G
G
)
(C
+(
)+
R
C
(C
R)
G
C
+(
R
C
0
Treatments
Figure 8 Growth of animals at the end of experiment, after four weeks incubation. Means+sd,
n=10. Alphabet without parenthesis indicates the growth of that species/ecotype in the
combination (abbreviations according to Fig. 2).
Three factors ANOVA showed significant lake effect (Table 5) on the growth of isopods.
Isopods from Lake Tåkern showed higher growth than those from Lake Fardume (Fig. 9a).
However, mean growth of chara ecotype was higher than reed ecotype among the isopods
from Lake Tåkern whereas, mean growth of reed ecotype was higher than chara ecotype
among the isopods from Lake Fardume (Fig. 9a).
There was no significant effect of different competition treatments on the growth of
both ecotypes (Table 5). However, the presence of Gammarus pulex in inter-specific
competition influenced the growth of two ecotypes in opposite direction.
16
The effects of three selected competition treatments on isopods’ growth tended to differ
between two lakes (Table 5). The growth of isopods was higher in Lake Tåkern for both intraspecific and low-competition treatments compare to Lake Fardume. However, in presence of
Gammarus pulex, isopods from Lake Fardume had higher mean growth than those from Lake
Tåkern. Three form interaction among ecotype-lake-competition showed that both chara and
reed ecotypes from lake Tåkern had significant (Table 5) higher growth than those from lake
Fardume when they existed in low density and high density. So, lakes had different effects on
the growth of isopods.
Table 5. Three factors ANOVA on the effect of Asellus ecotypes, lakes from which Asellus
were collected and competition (single ecotype at two densities and along with Gammarus
pulex) on the growth of the two ecotypes.
Source
Ecotype
Lake
Competition
Ecotype*Lake
Ecotype*Competition
Lake*Competition
Ecotype*Lake*Competition
Error
Total
DF
1
1
2
1
2
2
2
48
59
Seq SS
0.0232
1.5806
0.1375
0.4493
0.5016
1.7292
2.4577
7.4919
14.3710
MS
0.0232
1.5806
0.0687
0.4493
0.2508
0.8646
1.2288
0.1561
F
0.15
10.13
0.44
2.88
1.61
5.54
7.87
P
0.702
0.003
0.646
0.096
0.211
0.007
0.001
5 Discussion
5.1 Preiphytic algal biomass
The main objective of this study was to examine the functional role of two ecotypes of Asellus
aquaticus. In term of feeding on periphytic algae, I found no significant difference between
the two ecotypes in general. In addition, lake history generally had no effect on the feeding of
algae by the two ecotypes. Both ecotypes showed almost similar impact on algal biomass in
17
response to different competition treatments. However, in the low density (low-competition)
treatment, mean algal biomass on the tile was less (although not significant) for chara ecotype
than reed ecotype (Fig 3b). This might have resulted from the observed higher mortality of
chara ecotype than reed ecotype in low density treatment (Fig. 7b) as invertebrates add
nutrient in water through excretion which also stimulate algae growth (Post & Palkovacs
2009). The presence of Gammarus pulex significantly increased the algal biomass in interspecific treatment than intra-specific or low-competition treatment for both ecotypes. This
could be resulted from strong inter-specific interference effect between G. pulex and the two
ecotypes of Asellus that inhibited the invertebrates to graze on the epiphytic algae. In contrast
to my result, Hertonsson et al. 2008 in their experiment found that co-existed snails and
mayflies significantly reduced the periphyton biomass compare to their single species
treatment irrespective of density. However, G. pulex is both efficient detritivore and grazer
and larger than Asellus aquaticus in body size. It may consume more algae and dead leaves
and excrete more, which in turn would influence higher algae growth through nutrient input in
the water. This idea also helps to explain higher algae biomass in inter-specific treatment for
both ecotypes.
5.2 Leaf decomposition
I found no significant difference between chara and reed ecotypes in the second functional
role, in leaf consumption. The two ecotypes did differ neither between the lakes nor among
the selected competition treatments. However, the three competition treatments tended to
differ in impact on leaf decomposition. Leaf consumption per DW consumer was higher in
low-competition treatment, lower in intra-specific competition and lowest in inter-specific
competition when each ecotype co-existed with Gammarus pulex. So, the lower leaf
consumption in high density treatment than low-competition treatment could be resulted from
strong intra-specific interference effect within the individuals of chara and reed ecotypes
respectively (Jonsson and Malmqvist 2000, 2003). The other reason could be higher grazing
on periphytic algae than feeding on leaf in high individual treatment. Moreover, periphyton is
regarded as more nutritious than leaf litter (Hertonsson 2010). So, species can gain more from
grazing on periphyton than leaf consumption. Lowest leaf decomposition for both ecotypes in
inter-specific treatment suggests strong inter-specific interference effect between G. pulex and
A. aquaticus where both species shared the available food resource instead of decreasing the
resource biomass (Hertonsson 2010, Brown et al. 1994) in large extent.
5.3 Mortality
The use of available food resource through grazing or decomposition affects the fitness
components e.g. survival and growth of a species. I checked the mortality as well as growth of
both ecotypes separately and in an interaction with Gammarus pulex. Irrespective of lake and
competition effect, I found no significant difference in mortality between chara and reed
ecotypes. However, different ecotypes from different lakes experienced variable mortality.
For both ecotypes mortality was higher in Lake Tåkern compared to Lake Fardume. The
chara ecotype from Lake Fardume had a lower mortality than reed ecotype from same lake,
where as the chara ecotype from Lake Tåkern had higher mortality than the reed ecotype (Fig.
7a). So, lake origin tended to have a signature not only on the absolute, but also on the
relative mortality of the ecotypes.
A previous study (Eroukhmanoff and Svensson 2009) stated that the emergence of chara
ecotype in two Swedish lakes (Tåkern and Krankesjön) is an example of parallel evolution
where chara ecotypes have independent evolutionary origins. So, chara ecotypes from
different lakes can exhibit different traits of fitness components that lead to differentiation on
18
mortality between two lakes in my experiment. Competition effect can also be translated into
the survival and growth of the interacting species (Hertonsson et al. 2008). Chara and reed
ecotypes showed almost similar pattern of mortality in low density (or low-competition) and
high density (or intra-specific) competition (Fig. 7b). In inter-specific competition the chara
ecotype had higher mortality than the reed ecotype. This can be driven by two interaction
scenarios: observed higher mortality of chara ecotype from Lake Tåkern (Fig. 7a) and higher
mortality for in inter-specific competition for Lake Tåken (Fig. 7c). However, it can’t be
certain that which ecotype from Lake Tåkern had higher mortality in inter-specific
competition. This observed mortality can also be explained by the strength of inter-specific
interactions between chara and Gammarus pulex or reed and Gammarus pulex. Reed ecotype
might strongly compete with the amphipod for shared resources where as chara was out
competed by amphipod as chara ecotype has less endurance than reed ecotype (Eroukhmanoff
and Svensson 2009). Moreover, high genetic variation is observed among the isopods from
reed habitat than those from chara habitat in both Tåkern and Fardume (Eroukhmanoff et al.
2009). So, due to less genetic variation chara ecotype could have less resistance to
environmental or competition stress which might result in higher mortality of chara ecotype in
the laboratory study. In addition, exploratory behaviour study done by Eroukhmanoff and
Svensson 2009 showed that in presence of both food substrates, dead leaves and periphyton,
reed ecotype had higher tendency to forage on alternative substrate than chara ecotype. The
weak exploratory behaviour could also increase the mortality of chara ecotype.
The effects of competition were significantly different between the two lakes. Among Asellus
from Lake Fardume, competition had no influence on mortality; where as, both intra- and
inter-specific competition had a significant influence on mortality among Asellus from Lake
Tåkern. So, lake history has potential to influence the fitness (e.g. mortality, growth) of
species. Lake Tåkern experienced both turbid (dominated by phytoplankton) and clear
(dominated by submerged vegetation) water states in past few decades. This shift also
affected both biotic (e.g trophic web structure, benthic invertebrate, fish and waterfowl
assemblage etc.) as well as abiotic ( e.g total phosphorus, organic nitrogen concentration)
characters of the lake (Hargeby et al 2007, Hargeby et al 1994). This could also affect the
fitness of ecotypes of Asellus aquaticus from Lake Tåkern. However, Lake Fardume did not
experience such alternative shift. Moreover, genetic variation of ecotypes of Asellus is higher
between the two lakes compared to within lakes (Eroukhmanoff et al. 2009). So, different
lake can have different impacts on the fitness of isopods. However, a further result from
several lake studies is needed to generalise this idea.
5.4 Growth
In line with mortality, chara and reed ecotypes of Asellus showed no difference in growth at
ecotype level. Similarly, ecotypes from Lake Tåkern had higher growth than those from Lake
Fardume (Fig. 9a). This could be resulted from higher mortality of isopods in Lake Tåkern.
As there were fewer individuals, the remaining isopods got more food and showed better
growth. Same might happen for Lake Fardume where high survival resulted in reduced
growth of isopods. Similar to mortality, isopods from different lakes have variable growth in
different competition treatments (Fig 9c). So, lake history has potential to influence the
growth of a species .
6 Conclusion
To sum up, present study suggests that there is no general difference between chara and reed
ecotypes in their potential role of leaf decomposition and grazing on periphytic algae.
However, competition itself has potential impact on ecosystem processes. The ecosystem
19
processes (e.g. grazing on algae and leaf decomposition) were decreased due to inter-specific
and intra-specific competitions. In both cases, an interference effect occurred instead of
reducing the available food resources. However, the observed impact of lakes on the mortality
and growth of the isopods in this study indicates the need of further study to investigate
whether lake history can affect the mortality and growth of a species.
7 Acknowledgements
I like to thanks my supervisor Anders Hargeby for his proper guidance and valuable time
during this project and also Biology Department, Linköping University to provide all the
facilities specially permission to use the green house. In end, I want to thanks all my teachers
and classmates who helped and encouraged me during my Master’s Study period at
Linköping University.
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