To Ena
List of Papers
This thesis is based on the following papers, which are referred to in the text
by their Roman numerals.
I
II
III
IV
Bartels, P., Cucherousset, J., Steger, K., Eklöv, P., Tranvik,
L.J., Hillebrand, H. Reciprocal subsidies between freshwater
and terrestrial ecosystems structure consumer-resource dynamics. In revision
Bartels, P., Cucherousset, J., Gudasz, C., Jansson, M., Karlsson,
J., Persson, L., Premke, K., Rubach, A., Steger, K., Tranvik,
L.J., Eklöv, P. Terrestrial subsidies to lake food webs: An experimental approach. Accepted in Oecologia
Bartels, P., Hirsch, P.E., Svanbäck, R., Eklöv, P. Water transparency drives intra-population divergence in Eurasian perch
(Perca fluviatilis). Manuscript
Bartels, P., Hirsch, P.E., Svanbäck, R., Eklöv, P. Intrapopulation niche separation mediated by water transparency
limits habitat coupling. Manuscript
Paper II was reprinted with kind permission of Springer Science and Business Media.
Cover illustration by Verena Rohde
Contents
Prologue ........................................................................................................ 11
Introduction ................................................................................................... 13
Ecological boundaries .............................................................................. 13
Food webs among ecosystems ................................................................. 14
Differences between aquatic and terrestrial ecosystems ...................... 15
Effects of subsidies on food webs ....................................................... 15
Food webs within ecosystems .................................................................. 16
Intra-population divergence ................................................................. 16
The role of intra-population divergence for habitat coupling .............. 18
Aims of the thesis ..................................................................................... 19
Methods ........................................................................................................ 20
Literature study ........................................................................................ 20
Mesocosm study ....................................................................................... 20
Field survey .............................................................................................. 21
Statistical analyses.................................................................................... 23
Results and Discussion ................................................................................. 24
Linkages between water and land ............................................................ 24
Subsidies in freshwater and terrestrial ecosystems .............................. 24
POC - a neglected subsidy to lake food webs ...................................... 26
Boundaries within lakes ........................................................................... 27
Water transparency affects intra-population divergence ..................... 27
Intra-population divergence limits habitat coupling ............................ 29
Conclusions ................................................................................................... 32
Future perspectives ....................................................................................... 33
Propagating effects of subsidies ............................................................... 33
The detritus link ....................................................................................... 33
Spatial dynamics ...................................................................................... 34
Feedback effects ....................................................................................... 34
Intra-specific trait variation ...................................................................... 35
Epilogue ........................................................................................................ 36
Sammanfattning på svenska .......................................................................... 37
Acknowledgements ....................................................................................... 40
References ..................................................................................................... 43
Glossary
allochthonous
autochthonous
bottom-up control
detritivore
detritus
DOC
functional response
lentic
lotic
omnivore
PLS
POC
riparian
subsidy
top-down control
trophic cascade
trophic level
produced outside a focal ecosystem
produced inside a focal ecosystem
control of community dynamics by resources, i.e., from lower levels of the food
web
organism feeding on detritus
dead organic matter
dissolved organic carbon
change of resource consumption rate as a
function of resource density
standing waters
running waters
organism feeding on more than one trophic
level
partial least squares regression analysis
particulate organic carbon; here: dead particulate organic carbon
land that is adjacent to freshwaters
resources produced outside a focal system
control of community dynamics by predators,
i.e., from top levels of the food web
here: effects of top consumers that influence
lower non-adjacent trophic levels in the food
web
position of an organism in the food web
10
Prologue
The question “who eats whom” is one that has long accompanied mankind.
Whereas our early ancestors likely adopted a “do lunch or be lunch” attitude
towards this question, contemporaries including myself are merging into the
fascinating intricacy of this seemingly basic question. To emphasize that this
question is not at all basic, let us dig into a simple example. “Foxes eat rabbits”. A naïve questioner might ask why foxes eat rabbits. They might taste
good or they might be easy to catch or easily digested or really abundant or
else. However, there is likely an endless repertoire of questions that might
follow the statement “foxes eat rabbits”. For instance, when do they eat
them? And where? Do they only eat rabbits? And if not, when and why do
they eat other prey? What other prey do they eat? Also, “foxes eat rabbits” is
clearly not the whole picture. Rabbits eat plants. Thus, we have expanded the
game by one more player to “foxes eat rabbits that eat plants”. If the fox eats
the rabbits, does that affect the plants? Likely, if the fox eats many rabbits,
plants might thrive since there are not so many rabbits around. However,
since rabbits are no longer easy to find, the fox might start eating mice to
survive. Because foxes switched to mice, rabbits can in turn increase again
since they are no longer eaten by foxes. You see where this is going. Even
such an apparently simple example can generate an endless complexity (if
you just think long enough).
In ecology, this wide complexity of interactions is integrated in food webs.
Food webs describe “who eats whom” and “who interacts with whom”.
More scientifically, they describe the pathways by which material is transferred and along which energy flows. They are essential for understanding
ecological interactions and are therefore fundamental for describing how
natural communities are organized or how species interact.
11
12
Introduction
Ecological boundaries
The dictionary of contemporary English states (among others) that a boundary is “something such as a wall or fence that is intended to keep people or
things separate”. In ecology, boundaries, although often furnished with a
similar meaning, are not clearly defined (Strayer et al. 2003). Cadenasso et
al. (2003) suggested that a boundary is the transition zone between two compositionally, structurally, or functionally different patches at a given scale.
The definition of a patch is thereby largely dependent on the research question, and might span from a macro-scale such as different geographic regions
or climate zones to a micro-scale such as different moss patches on rocks. In
many cases, the boundaries between such patches are apparent and correspond with boundaries in the landscape such as the interface between a
stream and its riparian or the edge of a forest, whereas in other cases, boundaries might be fuzzy such as the transition zone between a bog and land or
near-shore and off-shore marine habitats.
Several major principles in food web theory have been developed by focusing on single patches within pre-defined boundaries such as a lake ecosystem
or the pelagic zone within a lake. Such “simplified” studies have accumulated highly valuable insights into understanding natural ecosystems. However, boundaries are often permeable and focal patches are connected
through physical, chemical, and biotic linkages to adjacent patches (Polis et
al. 1997, Schindler and Scheuerell 2002). For instance, the dominant source
of iron in the photic zone in the world´s oceans originates from continents
(Duce and Tindale 1991). The input of such allochthonous matter (i.e., matter that is produced outside of the focal ecosystem) can substantially affect
community and food web dynamics within a focal ecosystem (e.g. Holt
2002; Leroux and Loreau 2008). A figurative example was reported by Polis
and Hurd (1995). They observed “extraordinarily high spider densities on
islands” that were characterized by very low internal (autochthonous) primary production. This high secondary production could not be explained by
local autochthonous production alone. Instead, the ocean provided allochthonous detritus such as marine wrack and carcasses that were washed
ashore. This input supplied a food source for coast-dwelling detritivores and
scavangers. In turn these detritivores and scavengers supported high spider
13
densities, much higher than predicted from autochthonous island production
alone (Polis and Hurd 1995). Such and similar processes might be common
in natural ecosystems (Polis 1999). Boundaries that seem apparent to us may
be frequently crossed by energy or material with subsequent effects on the
focal system. Incorporating cross-boundary movements into the study of
food webs is therefore often necessary.
Food webs among ecosystems
Cross-ecosystem movements of material and energy are ubiquitous. In particular, freshwater and adjacent riparian ecosystems are linked through several pathways (reviewed in Richardson et al. 2010; Figure 1). Freshwater
ecosystems receive nutrients and organic matter in form of dissolved organic
carbon (DOC) and particulate organic carbon (POC), and organisms from
terrestrial ecosystems. In lake ecosystems, many studies have demonstrated
that DOC can stimulate heterotrophic production because bacteria can utilize
allochthonous DOC as a carbon source (Tranvik 1988), whereas stream
ecologists have generally focused on the importance of POC in form of detritus (Vannote et al. 1980). The importance of prey subsidies (i.e., allochthonous prey) to aquatic consumers has been acknowledged in lentic and
lotic ecosystems (Nakano and Murakami 2001, Francis and Schindler 2009).
For instance, fish, salamander larvae, and predatory invertebrates such as
odonates frequently consume terrestrial prey. Less is known about the incorporation of POC by aquatic consumers in particular in lake ecosystems. Bacteria and fungi may decompose allochthonous POC and other consumers
such as detritivores may consume allochthonous POC directly, but there is a
lack of estimates of its contribution to consumers (but see Pace et al. 2004,
Carpenter et al. 2005, Cole et al. 2006).
Reciprocal fluxes from freshwater to terrestrial ecosystems have primarily
been studied as prey subsidies to terrestrial consumers (Nakano and Murakami 2001, Baxter et al. 2005, Gratton and Vander Zanden 2009). Emerging
insects can be consumed by a variety of animals such as birds, lizards, spiders, and other predatory arthropods. Terrestrial predators can themselves
cross the water-land boundary to forage on aquatic prey (a.k.a. crossboundary foragers). Annually returning salmon are a major food source for
many mammals and birds (Willson and Halupka 1995) that actively forage
on salmon in the stream channel. The carcasses are then consumed in the
stream or carried into the riparian. In addition, physical processes such as
floods can transport fine and coarse organic matter to the riparian zone
(Jones and Smock 1991), however little is known about the contribution of
aquatic detritus to terrestrial consumers.
14
Figure 1. Fluxes of organic matter across the freshwater-land boundary. Freshwater
ecosystems receive dissolved organic carbon (DOC), fine and coarse organic matter,
and terrestrial organisms from adjacent terrestrial ecosystems. Riparian ecosystems
receive emerging organisms such as insects and detritus that might be deposited by
cross-boundary foragers or during floods.
Differences between aquatic and terrestrial ecosystems
Cross-ecosystem fluxes might be perceived as a phenomenon that could
increase the similarity between terrestrial and aquatic ecosystems by erosion
of their boundaries. However, as early as in the 1940s, Lindeman (1942)
proposed that ecosystems that lie low in the landscape such as aquatic ecosystems receive more organic and inorganic allochthonous matter than ecosystems in high positions such as terrestrial ecosystems. This difference in
subsidy input might lead to systematic differences in aquatic and terrestrial
ecosystems such as the suggested higher secondary production in aquatic
ecosystems (Shurin et al. 2006). Surprisingly, quantifications of subsidy
inputs to aquatic and terrestrial ecosystems, and their potential effects on
recipient consumers are lacking.
Effects of subsidies on food webs
The input of allochthonous resources to recipient ecosystems might affect
consumers directly by subsidizing the diet (Richardson et al. 2010) resulting
in e.g. increased numbers of consumers. Importantly, several indirect effects,
15
i.e., effects that proceed beyond the recipient consumer level, might result
from the utilization of allochthonous resources by recipients (McCann et al.
1998). The impact of allochthonous input on food webs is largely determined by the amount that enters, the preference of the consumer for allochthonous resources, and if low or high trophic levels receive the input (Leroux
and Loreau 2008). If low levels receive subsidies, bottom-up effects should
dominate, whereas top-down effects should dominate if top-consumers receive subsidies (Polis and Strong 1996). Several studies demonstrate that
bottom-up effects result from the input of allochthonous resources. For instance, lotic ecosystems are maintained by inputs of terrestrial organic matter
(Wallace et al. 1997) and coastal ecosystems profit from the input of marine
wrack and carcasses (such as the previously described spider example; Polis
and Hurd 1995).
The input of subsidies can have several effects on top-down control. It has
been suggested that subsidies can strengthen or dilute top-down effects and
trophic cascades (Leroux and Loreau 2008). An increase in reproductive or
behavioral response of the recipient predator due to the consumption of allochthonous prey can result in enhanced consumption of autochthonous prey
(i.e., apparent competition; Holt 1977), thus resulting in stronger top-down
effects on autochthonous prey and potentially strong trophic cascades. In
contrast, top-down control on autochthonous prey is likely weakened if the
predator´s preference for the allochthonous resource is high or when allochthonous resources are abundant enough to saturate the predator´s functional
response. High input of allochthonous resources or high preference for allochthonous resources of the predator can then cause a switch in the predator
to consuming allochthonous resources and thus attenuate top-down control
on autochthonous resources due to decreased predation pressure. Freshwater
and terrestrial ecosystems are linked through several pathways however
whether freshwater ecosystems generally receive subsidies at different trophic levels than terrestrial ecosystems is currently not known.
Food webs within ecosystems
Intra-population divergence
Differences in habitat and resource use have long been viewed as major determinants of phenotypic divergence within and between species. Different
environments may require different environment-specific adaptations of
behavioral, morphological, or life history traits (McPhail 1984, Schluter and
McPhail 1992) which increase the individual´s fitness and ultimately lead to
ecological speciation (Schluter 1996). For instance, structural differences in
habitat result in diverging phenotypes in Anolis lizards (Losos et al. 2000).
Lizards using narrow surfaces such as twigs have short hind limbs, whereas
16
lizards using broad surfaces such as tree trunks or the ground tend to have
long limbs (Losos 1990). In particular, the utilization of different resources
is thought to drive population divergence (a.k.a. resource polymorphism;
Smith and Skulason 1996), where different resources require different trophic traits to increase feeding efficiency. Resource polymorphism is common
(Smith and Skulason 1996), as for example the adaptive variation in beak
morphology in Darwin finches (Schluter and Grant 1984) or in feeding morphology in some African cichlids (Meyer 1989).
Resource polymorphism is notably prevalent in fish. In lake ecosystems,
fish often inhabit either the near-shore littoral or the open-water pelagic zone
resulting in the development of habitat-specific traits such as different body
morphologies (Smith and Skulason 1996). Pelagic individuals are usually
more streamlined to increase long distance swimming performance and to
facilitate feeding on widely dispersed prey whereas littoral individuals are
more deep bodied optimally adjusted to maneuver in structural complex
environments (Ehlinger and Wilson 1988). The development of such habitatspecific traits increases feeding efficiency on habitat-specific resources
(Svanbäck and Eklöv 2003). However, feeding efficiency and/or resource
acquisition might be affected by environmental features. Many fish depend
on vision to detect their prey therefore environmental features that influence
vision might affect foraging efficiency in fish. Ljunggren and Sandström
(2007) showed that foraging efficiency on pelagic prey decreased in low
water transparency in a visual consumer (Perca fluviatilis), whereas low
water transparency did not affect foraging efficiency in a consumer (Sander
lucioperca) that used other senses than vision to detect prey. In contrast to
pelagic foraging, benthic foraging might generally be less vision-dependent
(Uiblein 1992). Bottom-living prey organisms are often cryptic or inhabit the
sediment. Alternative foraging mechanisms such as undirected sampling
might be more important for benthic foraging, thus benthic foraging efficiency is likely less affected by decreased water transparency than pelagic
foraging. Furthermore, constraints in water visibility might alter resource
utilization (Carter et al. 2010) because some prey types might be more visible than others (Jönsson et al. 2011). Differences in foraging efficiency or
alterations in resource use due to decreased water transparency might therefore affect intra-population divergence, i.e., the divergence between individuals within a population, if the divergence is driven by resource acquisition.
It is however not foraging alone that affects resource acquisition. The abundance and/or availability of different resources might also play an important role. For instance, Hendry et al. (2006) suggested that a change in resource availability likely caused by human activity resulted in decreased
population divergence in a Darwin finch (Geospiza fortis) due to altered use
of resources. In lake ecosystems, multiple factors may influence the availability of benthic and pelagic resources. Physical features of the environment
such as lake shape and depth affect the relative availability of benthic re17
sources (Dolson et al. 2009). Furthermore, benthic primary production is
light limited. Thus, environmental factors that decrease light penetration
through the water column can reduce benthic primary production, and might
in turn decrease the availability of benthic resources to fish. An increase in
water color due to an elevated input of terrestrial organic matter can hamper
benthic productivity and the use of benthic resources by fish (Karlsson et al.
2009). Similarly, eutrophication can impede benthic pathways through enhanced pelagic productivity (Vadeboncoeur et al. 2003). This suggests that a
decrease in water transparency independent of its cause might generally affect benthic resource availability to consumers.
The impact of water transparency on population divergence has primarily
been studied by investigating its effect on mating systems. For instance,
Seehausen et al. (1997) showed that fewer and duller color morphs of African cichlids were found in areas of high turbidity. Similarly, mating success
of sand gobies (Pomatoschistus minutus) was more evenly distributed among
large and small males in turbid than in clear water (Järvenpää and Lindström
2004). Although several studies show that water transparency can affect
aquatic ecosystems by changing the foraging of consumers or by altering the
relative availability of resources, its effects on population divergence due to
potential differences in resource acquisition are currently unknown.
The role of intra-population divergence for habitat coupling
Previous studies on lake ecosystems have mainly focused on single habitats,
with a substantial bias on the pelagic habitat (Vadeboncoeur et al. 2002),
thereby neglecting that benthic/littoral habitats may play an important role in
whole lake productivity (Karlsson et al. 2009) and further that benthic/littoral and pelagic habitats are often coupled (a.k.a. habitat coupling;
reviewed in Schindler and Scheuerell 2002). In particular fish can integrate
littoral and pelagic habitats (Vander Zanden and Vadeboncoeur 2002). There
are two potential mechanisms for habitat coupling through fish. First, fish
can move between pelagic and littoral habitats. If resources in one habitat are
few, fish might switch to the other habitat where resources are more abundant. This switch to alternative resources might prevent strong depletion of
habitat-specific resources and enable recovery of the resources during periods when fish feed on alternate resources. Second, fish can excrete nutrients derived from benthic resources to the water column. Fish excretion is
an important source of nutrients for phytoplankton (Braband et al. 1990). If
fish consume pelagic resources and excrete nutrients from pelagic-derived
resources into the water column, this process is referred to as nutrient recycling (Vanni 2002) since nutrients are excreted in the same habitat as where
the resources were derived from. In contrast, if fish consume benthic resources and excrete nutrients from benthic-derived resources into the water
column, it is referred to as nutrient translocation (Vanni 2002), since excre18
tion and consumption take place in two different habitats. Fish might therefore act as “nutrient converters” that can mobilize nutrients that were formerly bound in the benthos and make them available to biota in the water column.
Previous studies on habitat coupling have treated consumer populations as
homogeneous units, thereby neglecting that top consumers may occupy different habitats and forging niches (Power et al. 2005). Intra-population divergence such as the divergence between pelagic and littoral fish might limit
an individual´s use of multiple habitats (Quevedo et al. 2009). For instance,
streamlined pelagic individuals that use littoral habitats to forage might have
a disadvantage since they do not match the habitat-specific requirements.
Such disadvantage can be expressed as e.g. decreased feeding efficiency
(Knudsen et al. 2010). Studies investigating habitat coupling by top consumers have generally assumed “rapid switching behavior” of top consumers as
a key factor for the ability to move between habitats and feed on different
resources (Rooney et al. 2006). That is if resources are low in one habitat,
they can easily switch to the alternative habitat where resources might be
more abundant. However, if consumers express habitat-specific traits, they
might not be able to switch to the alternative habitat since e.g. feeding efficiency in the alternative habitat might be strongly decreased. Thus, the development of habitat-specific traits, such as the intra-population divergence
between more streamlined individuals in the pelagic and more deep bodied
individuals in the littoral habitat, might limit habitat coupling through the
movement of fish because “rapid switching” may be hampered or even unfeasible.
Aims of the thesis
The aims of my thesis were to evaluate the importance and limitations of
food web coupling on two different scales: among and within ecosystems. In
the first part of my thesis, I investigated cross-ecosystem movement of organic matter across the freshwater-land boundary. In particular, I focused on:
• Differences in allochthonous input and responses in recipient consumers between freshwater and terrestrial ecosystems (Paper I)
• The relevance of allochthonous POC as a subsidy to lake food
webs (Paper II)
In the second part, the major emphasis was on food webs within lake ecosystems. In particular, I focused on:
• The role of water transparency as a potential determinant of intrapopulation divergence (Paper III)
• Consequences of intra-population divergence for habitat coupling
through the movement of a mobile consumer (Paper IV)
19
Methods
Literature study
To evaluate the importance of resource subsidies and identify general patterns of subsidy inputs and responses in recipient consumers in freshwater
and terrestrial ecosystems (Paper I), we performed a meta-analysis of 763
entries from 63 papers. Obtained data were divided into different datasets
and included information on subsidy input fluxes (mg m-2 day-1) and standing stocks in recipient ecosystems (mg m-2) and contribution of subsidies to
recipient consumers (% as inferred from stable isotope analyses). Furthermore, log-ratios were used to compare consumer responses at high and
no/low subsidy locations. Across all databases, we categorized each observation by the direction of subsidy input (aquatic to terrestrial or terrestrial to
aquatic), subsidy category (salmon, detritus or prey organism), and trophic
level of recipient consumer (primary consumer, omnivore or predator).
Mesocosm study
To study the importance of POC as a subsidy to a lake food web (Paper II),
we conducted a mesocosm experiment. Mesocosm studies offer the possibility to conduct studies under semi-natural conditions while still being readily susceptible to manipulation and easily replicable. In our study, we set up
16 mesocosms (1.5 m in diameter, 1.9 m depth) that extended from the water
surface into the bottom sediment in a clear-water lake in Abisko
(68°19´91´´N, 19°09´22´´E). We manipulated POC input and light conditions in order to determine whether POC can subsidize lake food webs. To
distinguish between the effects of decreased light penetration and the carbon
input, a full 2 x 2 factorial design was applied with the following treatments:
no carbon and no shade, carbon and no shade, no carbon and shade, carbon
and shade.
Light manipulations were conducted by wrapping and covering the mesocosms with shading cloth, resulting in a 50% light reduction on the bottom
of the mesocosms. As a POC source we used corn starch (hereafter referred
to as starch carbon). We were particularly interested in the effects of POC on
the benthic food web, therefore our use of starch carbon was motivated by
two major requirements: the organic carbon source needed to be 1) insoluble
20
and deposited rapidly so that it was only available to the benthos and 2) easy
to distinguish from naturally available carbon sources using stable isotope
analyses in order to trace it in different food web compartments. We added
high amounts of starch carbon to maximize the isotopic signal and the stimulation of heterotrophic production. The bioavailability of starch carbon is
likely high compared to terrestrial-derived organic carbon which is generally
recalcitrant and which might represent a poor quality resource for consumers
(Brett et al. 2009). However, the objective of our study was to outline potential pathways of POC uptake in lake food webs and thus was similar to previous experiments that used glucose (e.g. Ducklow et al. 1986, Blomqvist et
al. 2001), where the concentration and recalcitrance of the organic carbon
added was not crucial.
Field survey
Comparative field studies are useful for finding patterns in natural ecosystems along gradients of environmental factors. Therefore, to investigate the
effect of water transparency on intra-population divergence (Paper III) and
potential subsequent effects on habitat coupling (Paper IV) we conducted a
field survey of seven lakes along a gradient of low to high water transparency (Figure 2). As a study organism, we used Eurasian perch (Perca fluviatilis). Perch is an omnivorous predator that generally feeds on zooplankton,
macroinvertebrates, and fish, and that can exert strong impacts on its resources and on whole lake food web dynamics. Perch display a continuous
phenotypic variation in relation to habitat and resource use where deeper
bodied individuals that utilize littoral resources are found in the littoral zone
(Figure 3b) and more streamlined individuals that feed mainly on pelagic
resources are found in the pelagic zone (Figure 3c; Svanbäck and Eklöv
2002, 2003), and thus represented an ideal model organism for our study.
21
Figure 2. Map of the locations of the seven lakes included in the comparative field
survey. The small star represents the location of Uppsala. Copyright Lantmäteriet
Gävle (2010): Permisson I 2010/0058.
We used body morphology as a proxy for intra-population divergence in
perch (Paper III, IV). Morphology was analyzed using landmark-based
thin-plate spine (TPS) analysis, a geometric morphometric technique (Zelditch et al. 2004). We used the freeware TPS-dig2, TPS-relw, and TPS-regr
for all morphological analyses. Perch were photographed on the left side,
and 16 landmarks (Figure 3) were digitized for each image using TPS-dig2.
Digitized landmarks were used to evaluate the relative position of each
landmark and variation in body shape by calculating partial warps and uniform scores for each individual using TPS-relw. TPS-relw transforms all
specimens to a centroid size to avoid differences in landmarks caused by size
differences. The uniform shape components parameterize all shape variation
that is uniform throughout the whole geometry such as the bending of the
body. The partial warps measure non-uniform shape variation that is localized to particular regions of the geometry such as the position of a fin. Deformations of body morphology were visualized using TPS-regr. Partial
warps and uniform scores were analyzed with a discriminant function analysis (DFA) where the classification was based on the origin of the fish (e.g.
habitat). The DFA combines all partial warps and uniform scores for each
22
fish into n-1 functions (morphological index) that maximally discriminates
between the groups where n is the number of classification levels. Morphological divergence was calculated as the difference between mean littoral
and mean pelagic morphological index for each lake.
Figure 3. Morphological variation in perch. a) The 16 landmarks that were used for
morphological analyses. Contour of b) a littoral and c) a pelagic individual from
Långsjön.
Resource utilization of perch was estimated with stomach content analyses
(Paper III) and stable isotope analyses of muscle tissue (Paper IV). Stomach analyses are “snap-shots” of a consumer´s diet and might not accurately reflect long-term diet use. However, they provide high resolution on the
utilization of particular resource items. In contrast, stable isotope analyses
integrate resource use over longer time periods and are therefore a good estimate of the utilization of different energy pathways by a consumer.
Statistical analyses
Several statistical tools were used to evaluate the data in this thesis. In Paper I, meta-analysis and randomized ANOVAs were used to analyze the
different datasets from the literature survey. In Paper II, we used circular
statistics (Zar 1996). Circular statistics allow a quantitative understanding of
complex isotopic changes at the community and food web level in time
and/or space (Schmidt et al. 2007). In Paper III, PLS (partial least squares
regression analysis; Eriksson et al. 2006) was applied. In Paper IV, we used
the package Stable Isotope Analysis in R (SIAR, Jackson et al. 2011) to evaluate morphological and trophic niche overlap between littoral and pelagic
perch populations.
23
Results and Discussion
Linkages between water and land
Subsidies in freshwater and terrestrial ecosystems
Already in the 1940s, Lindeman (1942) proposed that aquatic ecosystems
receive higher amounts of subsidies than terrestrial ecosystems due to their
low position in the landscape. However, this has never been tested empirically. Compiling a large dataset of quantitative estimates of subsidies and responses in recipient consumers, we aimed to quantify reciprocal fluxes between freshwater and terrestrial ecosystems, and further to evaluate consumer responses in the recipient ecosystems to these subsidy fluxes.
We found that freshwater ecosystems generally received higher amounts
of subsidies than terrestrial ecosystems (Paper I). This higher input was
primarily driven by the movement of terrestrial detritus, although the input
of terrestrial prey to freshwater ecosystems was also higher than the input of
aquatic prey to terrestrial ecosystems. Salmon carcasses likely presented an
exception to this general pattern. Large amounts of salmon may be transported via cross-boundary foragers and physical processes such as floods to
riparian ecosystems (Ben-David et al. 1998), potentially exceeding other
water to land pathways by several magnitudes.
Despite the large discrepancy in subsidy inputs, responses in consumers,
estimated as either contribution inferred from stable isotope analyses or logratios, were similar in aquatic and terrestrial consumers (Paper I). The stoichiometry of detritus and living organisms differs potentially by several orders of magnitude (Cross et al. 2005). Terrestrial consumers receive primarily high quality resources such as prey organisms derived from freshwater,
whereas aquatic consumers mainly receive low quality resources through
detrital inputs. Aquatic organisms have been shown to selectively feed on
high quality resources (Marcarelli et al. 2011). The difference in quality
between detritus and prey organisms might thus explain the low aquatic consumer response despite high allochthonous inputs. In contrast, terrestrial
consumers receive low amounts of high quality resources. Therefore, responses in recipient consumers independent of the ecosystem are likely governed by the quality of the allochthonous resources.
24
Importantly, the impact of allochthonous input on food web dynamics is
largely determined by the trophic levels receiving the input. If primary consumers receive subsidies, bottom-up effects should dominate, whereas topdown effects dominate if top consumers receive subsidies (Polis and Strong
1996). We found that terrestrial ecosystems generally receive subsidies primarily on one trophic level, i.e., the predator level, whereas freshwater ecosystems receive subsidies on multiple trophic levels including primary consumers and predators (Paper I). Thus, top-down effects should generally be
affected in terrestrial ecosystems following the subsidy to predators, while
both, bottom-up and top-down forces should be affected in aquatic ecosystems. Several studies demonstrated that the input of subsidies caused strong
bottom-up effects in freshwater ecosystems (Wallace et al. 1997). We identified a large bias against studies investigating detrital fluxes from freshwater
to adjacent terrestrial ecosystems, although aquatic detritus can be deposited
via cross-boundary foragers and physical processes such as floods (Jones
and Smock 1991, Ben-David et al. 1998). Whether these fluxes are important for terrestrial consumers needs to be further investigated.
Both terrestrial and freshwater ecosystems receive prey subsidies at the
predator level (Paper I), suggesting that top-down effects should be affected
in both ecosystems. Whether subsidies change the top-down control or cause
trophic cascades remains controversial since the input of subsidies to topconsumers has been suggested to both dilute and strengthen top-down effects
(Leroux and Loreau 2008). Few studies have specifically addressed the impact of allochthonous resources on the strength of top-down effects and results are inconsistent (Nakano et al. 1999, Murakami and Nakano 2002, Sabo and Power 2002a, b). Several studies have confirmed that the input of
subsidies to top consumers increased the strength of top-down effects and
trophic cascades. Henschel et al. (2001) demonstrated that subsidized spiders
exerted higher predation pressure on herbivores, resulting in reduced herbivory. Birds subsidized by emerging insects affected terrestrial herbivorous
insect populations to a higher extent than birds that were not subsidized
(Murakami and Nakano 2002).
The alternative scenario that the input of subsidies to predators can dilute
top-down control and trophic cascades has also been demonstrated repeatedly. The reduction of allochthonous resources to a forest stream resulted in
increased fish predation on stream arthropods and subsequent increase in
periphyton biomass (Nakano et al. 1999). Similarly, Baxter el al. (2004)
reported that the introduction of a non-native fish resulted in strong competition for allochthonous resources with a native fish species, forcing the native
fish species to feed on autochthonous resources. The modification in resource utilization in turn resulted in a strong trophic cascade on stream benthos caused by the native fish. In both studies the results suggest that prior to
the disturbance the input of allochthonous resources impeded strong trophic
cascades. Likewise, a reduction in predation pressure of lizards on terrestrial
25
arthropods occurred when emerging aquatic insects were available (Sabo and
Power 2002b). Whether the input of allochthonous resources alters the
strength of top-down control and trophic cascade differently in aquatic and
terrestrial ecosystems is not known but it is certainly an exciting question for
future studies.
POC - a neglected subsidy to lake food webs
Lake ecosystems were highly under-represented in our literature study (Paper I). Most studies have focused on the importance of DOC to lake ecosystems (those studies were excluded from our study, see Paper I), whereas the
relevance of other allochthonous organic carbon sources has largely been
neglected. In particular, the contribution of POC to lentic consumers is largely unknown (but see Pace et al. 2004, Carpenter et al. 2005; Cole et al.
2006). In addition, major attention has been given to pelagic habitats, whereas less is known about benthic habitats although they might play an important role in whole lake productivity (Vadeboncoeur et al. 2002).
By using an isotopically distinct POC source (starch carbon), we showed
that POC can subsidize lake food webs (Paper II). We traced the starch
carbon in most benthic primary consumers and in a predatory invertebrate.
There are two major entry routes for starch carbon into benthic consumers.
First, benthic consumers fed directly on the starch carbon, which was likely
the case for many detritivorous taxa. Secondly, macroinvertebrates consumed benthic bacteria that were supported by starch carbon. Bacteria discriminate strongly against 15N (Hoch et al. 1994, McGoldrick et al. 2008)
and have low δ15N values compared to benthic algae (Karlsson and
Säwström 2009). We found that the nitrogen isotopic signature of macroinvertebrates was slightly depleted in the carbon and no shade treatment, i.e.,
the isotopic signature was lower in the treatment where carbon was added,
suggesting that starch carbon was at least partly incorporated via bacteria.
Total consumption of primary consumers was likely a combination of direct
consumption and consumption of starch-supported bacteria. We further
traced the starch carbon signal in a predatory invertebrate, indicating that the
starch carbon was further transferred up the benthic food web.
Surprisingly, although we introduced the starch carbon exclusively to the
sediment, we found strong effects of the carbon addition on pelagic biota.
Zooplankton showed equally strong or stronger reliance on starch carbon
than macroinvertebrates (Paper II). This can be explained by three mechanisms. First, the starch carbon was re-suspended from the sediment and subsequently consumed by zooplankton. We suggest that this mechanism was
very unlikely since our mesocosms were rather narrow and comparably
deep. Water movement should be minimized in such mesocosms, and thus
re-suspension was likely absent. Secondly, zooplankton consumed the starch
carbon by directly grazing it from the sediment. Thirdly, zooplankton con26
sumed the starch carbon through pelagic bacteria that were supported by
starch-labeled organic carbon from sediment biota. An increased release of
starch-labeled organic carbon from the sediment and the subsequent incorporation by pelagic bacteria was evident through the decreased chlorophyll a
concentrations in the water column in the mesocosms with carbon addition.
Previous studies have found that the increased input of DOC to the pelagic
habitat decreased primary production and/or chlorophyll a concentrations in
the water (Klug 2005, Stets and Cotner 2008) because algae are inferior in
nutrient allocation compared to bacteria. The uptake of starch-labeled pelagic bacteria was in turn evident through the depleted nitrogen signature in
zooplankton, similar to what we found in benthic macroinvertebrates. Although the uptake of allochthonous DOC by zooplankton through bacteria
has been suggested to contribute only a minor fraction to the reliance of
zooplankton on allochthonous organic carbon (Cole et al. 2006), it likely
contributed to the reliance on starch carbon of zooplankton in our study.
Many studies have demonstrated the importance of allochthonous DOC to
lake food webs, whereas the importance of allochthonous POC has largely
been neglected. The availability of allochthonous POC in sediments is likely
high since allochthonous particulate organic matter can substantially contribute to lake sediments (Kortelainen et al. 2004), and flocculation of DOC
can further increase the POC pools in lake ecosystems (von Wachenfeldt and
Tranvik 2008). Our study showed that allochthonous POC can considerably
subsidize benthic and pelagic food webs in lake ecosystems. We suggest that
the outlined pathways of POC incorporation may play a considerable role in
lentic food webs by subsidizing benthic and pelagic consumers in particular
in lakes that are characterized by low primary production.
Boundaries within lakes
Water transparency affects intra-population divergence
Habitat structure and resources use are important factors governing phenotypic divergence. In particular, resource use can drive intra-population divergence, i.e., trophic polymorphism in many animals (Smith and Skulason
1996). Resource polymorphism is exceptionally common in fish. Surprisingly, although several studies show that decreasing water transparency can
affect resource acquisition in fish by reducing foraging efficiency or altering
resource utilization, its effects on population divergence are currently not
known. Our study indicates that water transparency considerably affects
intra-population divergence in perch (Paper III, IV). We found that perch
strongly diverged into more deep bodied littoral and more streamlined pelagic populations in lakes with high water transparency, whereas littoral and
pelagic populations were morphologically more similar when water transpa27
rency was low. Water transparency mediates several processes in aquatic
ecosystems that likely resulted in the observed patterns. Below I elaborate on
the potential mechanisms responsible for the population divergence.
Differences in habitat and resource use are major determinants of population divergence. Thus, a homogenization of the environment, i.e., an increase
in the similarity between different habitats, might result in decreased population divergence. Freedman et al. (2010) showed that deforestation resulting
in the loss of the transition zone between savanna and rainforest habitats
weakened population divergence in a rainforest bird (Andropadus virens). In
aquatic ecosystems, decreasing water transparency can lead to decreased
macrophyte coverage in littoral habitats (Estlander et al. 2009) resulting in a
less structurally complex environment. In our study, perch from littoral and
pelagic habitats were morphologically more similar (Paper III, IV), and
overall more streamlined in lakes with low water transparency (Paper III),
indicating that structural complexity was likely similar between littoral and
pelagic habitats. Furthermore, previous studies reported that decreasing water transparency due to eutrophication or increasing input of terrestrial organic matter can limit benthic pathways as a result of light limitation, resulting in a higher relative importance of pelagic pathways (Vadeboncoeur et al.
2003, Karlsson et al. 2009). Biomass and composition of littoral and pelagic
resources did not differ between lakes with high and low water transparency
in our study lakes and littoral resource utilization of perch from lakes with
low and high water transparency did not differ when assessed from stomach
content analysis (Paper III). However, littoral resource utilization was lower
in lakes with low water transparency compared to lakes with high water
transparency when inferred from stable isotope analysis (Paper IV). Two
potential mechanisms might explain this apparently inconsistent result. First,
we investigated resource abundance only at one occasion during summer.
Resource abundance might be lower in lakes with low water transparency
during other times of the year, resulting in lower reliance of perch on littoral
resources on long-term. Second, resource abundance per se might not be
determining for resource utilization but that it is rather the availability of
resources to fish that determines their utilization. Although we showed that
benthic foraging is not affected by low water transparency (Paper III) littoral resources might be less available to consumers in lakes with low water
transparency due to structural differences in the environment (e.g. sediment
structure, low macrophyte coverage).
We propose that water transparency also affected intra-population divergence through its effect on foraging. Resource acquisition differed considerably between lakes with low and high water transparency and we found distinct differences between littoral and pelagic populations. Littoral reliance
was generally low to moderate for pelagic populations (range: 10.9 ± 3.6%
to 54.2 ± 13.0%) and did not differ between lakes with low and high water
transparency (Paper IV). However, the utilization of different pelagic prey
28
organisms differed for pelagic populations. In lakes with high water transparency, pelagic perch mainly consumed cladocerans, whereas they consumed
copepods in lakes with low water transparency (Paper III), although zooplankton biomass and community composition did not differ. Cladocerans are
generally the preferred resource (Persson 1986). Several studies have shown
that perch foraging on pelagic prey decreased substantially in poor visual
conditions (e.g. Ljunggren and Sandström 2007). In particular, selectivity for
daphnids decreased in colored water (Estlander et al. 2010). Under impaired
visual conditions, prey motion might be more important than size or visibility. Cladocerans generally move slowly whereas copepods are capable of
evasive movements. The fast and irregular movements of copepods might
make them better detectable when water visibility is low and thus more susceptible to perch predation. A previous study reported that bluegill (Lepomis
macrochirus) preferred faster swimming clones of Daphnia (O´Keefe et al.
1998), supporting that prey motion may increase conspicuousness to fish and
thus the effectiveness of prey detection. The difference in movement ability
between cladocerans and copepods might not only affect the susceptibility to
perch predation but also the quality as a resource for perch. Energy gain is
higher and handling cost is lower for cladocerans (Johansson and Persson
1986), and therefore cladocerans represent a better resource for perch than
copepods. Simultaneous with the change in feeding on cladocerans vs. copepods in high and low water transparency, the condition factor of perch increased with increasing water transparency (Paper III). The condition factor
can be used as a proxy for excess energy which might be used for the development of different morphologies through phenotypic plasticity (Olsson et
al. 2007). Phenotypic divergence through phenotypic plasticity was likely
facilitated when food conditions were more favorable, i.e., when the consumption of cladocerans was high.
Aquatic ecosystems are highly susceptible to environmental change and
in particular human activities can strongly affect aquatic ecosystems. Many
lakes and coastal ecosystems worldwide are eutrophic (Carpenter et al. 1998)
and eutrophication is predicted to become more frequent in the future (Tilman et al. 2001). We can therefore expect increasing changes in water transparency in many aquatic ecosystems worldwide with subsequent effects on
aquatic communities. Independent of which mechanism dominated in the
resulting higher similarity of littoral and pelagic populations in low water
transparency, we suggest that decreasing water transparency will likely impede intra-population divergence in aquatic consumers through its effects on
resource acquisition and foraging.
Intra-population divergence limits habitat coupling
Several pathways can couple littoral and pelagic habitats in lake ecosystems
(reviewed in Schindler and Scheuerell 2002). In particular, fish have been
29
suggested to play a major role in habitat coupling (Vander Zanden and Vadeboncoeur 2002) since they can freely move between habitats. Previous
studies on habitat coupling have used reliance on littoral resources as a
proxy for littoral-pelagic coupling by mobile consumers (e.g. Vander Zanden
and Vadeboncoeur 2002, Dolson et al. 2009). However, these studies treated
consumer populations as homogenous units, neglecting that individuals
might diverge within one population. We demonstrated that the overall contribution of littoral resources tended to increase with increasing water transparency. However this trend was driven by an increasing reliance on littoral
resources of littoral perch, whereas the reliance of pelagic perch was not
affected by water transparency (Paper IV). In lakes with high water transparency, we found strong niche separation, both in morphological traits and in
trophic niche space, whereas we found high morphological and trophic niche
overlap in lakes with low water transparency (Paper IV). This suggests that
the movement between habitats was presumably not restricted in lakes with
low water transparency due to little differences in morphology between littoral and pelagic individuals.
In contrast, strong morphological divergence between littoral and pelagic
populations likely impeded the movement between littoral and pelagic habitats in lakes with high water transparency. Individuals that develop habitatspecific traits such as different body morphologies have a disadvantage in
alternate habitats if they do not match the habitat-specific requirements, resulting in e.g. decreased foraging efficiency (Knudsen et al. 2010). Thus,
switching to alternate habitats might be hampered or unfeasible. However,
other mechanisms of habitat coupling such as nutrient translocation of benthic-derived nutrients to pelagic biota might be promoted. Littoral populations showed strong reliance on littoral resources indicating that nutrient
translocation was likely enhanced although we did not assess that in our
study.
Individuals within populations can differ in several traits such as e.g. resource use (Bolnick et al. 2003), anti-predator defenses (Duffy 2010), and
parasite resistance (Ganz and Ebert 2010) and a recent study of Bolnick et al.
(2011) emphasized that “ecologist cannot ignore [such] intra-specific variation, owing to its large effects on community dynamics”. Previous studies
investigating habitat coupling have however large neglected individual variation within a population (but see Quevedo et al. 2009, Matich et al. 2011,
Rosenblatt and Heithaus 2011). Theoretical studies on food web coupling
generally assumed “rapid switching behavior” as a prerequisite condition of
consumers to be able to shift between different habitats or resources (Rooney
et al. 2006). We argue that switching ability is constrained by the development of habitat/resource-specific traits. Trait adaptations to specific habitats
or resources such as the here observed variation in body morphology are
common (Smith and Skulasson 1996), suggesting that the impediment of
switching to alternative habitats or resources might be hampered in other
30
organisms. For instance, Darwin’s ground finches (Geospiza fortis) show
high variation in beak morphology corresponding to their preferred resource
(Schluter and Grant 1984). Large birds with large beaks usually feed on
large and hard-shelled seeds, whereas small birds with smaller beaks feed on
small and softer seeds. After a severe drought on Daphne Major Island,
small birds died out since they could not find enough small seeds and were
not able to feed on large-sized seeds (Boag and Grant 1981). Although this is
clearly not an example of habitat coupling nor an example of a top consumer, it emphasizes that switching to alternative resources was strongly limited
by the development of resource-specific traits. The study of habitat coupling
is a rather young research field but we suggest that the assumption of “rapid
switching behavior” as a prerequisite for habitat coupling should be considered with great caution due to the frequent occurrence of trait adaptations
within populations. Intra-specific trait variation does matter since it can affect food web dynamics in natural ecosystems.
31
Conclusions
The major findings from my thesis can be summarized as follows:
•
•
•
•
•
•
32
Subsidies are important and contribute substantially to recipient consumers (Paper I, II).
Freshwater ecosystems receive higher amounts of subsidies than terrestrial ecosystems, but the contribution to recipient consumers is similar
(Paper I).
Freshwater ecosystems receive subsidies at multiple trophic levels, whereas terrestrial ecosystems generally receive subsidies at high trophic levels (Paper I).
Allochthonous POC can substantially subsidize benthic and pelagic food
webs in lake ecosystems (Paper II).
Water transparency plays a major role in driving intra-population divergence in perch (Paper III, IV).
Habitat coupling in lake ecosystems through the movement of mobile
consumers is limited by intra-population divergence (Paper IV).
Future perspectives
One of the major challenges in science is not (only) to find answers, but
particularly to raise new questions. I feel that my thesis work has produced
more questions than answers (at least for me). In the following paragraphs I
briefly outline some ideas and perspectives for future studies.
Propagating effects of subsidies
Ample studies investigated the effects of subsidies on recipient consumers
however our knowledge on propagating effects on adjacent and non-adjacent
consumers is still very limited. Although several theoretical studies on the
impact of subsidies on top-down and bottom-up effects are available, the
empiricists lack behind. The very few available studies investigating subsidy
effects on top-down control demonstrate every possible outcome but there is
some evidence that top-down effects in aquatic ecosystems tend to be diluted
by the input of allochthonous resources (Nakano et al. 1999, Baxter et al.
2004) whereas in terrestrial ecosystem there is no such trend (Henschel et al.
2001, Murakami and Nakano 2002, Sabo and Power 2002a, b). Clearly,
there are too few studies to draw any general conclusions however investigating subsidy effects beyond recipient consumers in aquatic and terrestrial
ecosystems represents an exciting research field for the future.
The detritus link
In Paper I, we identified a major bias against the linkage from freshwater to
terrestrial ecosystems through detritus. The input of marine detritus to coastal and island ecosystems is well studied (Polis et al. 2004), however, equivalent studies in riparian ecosystems are lacking. Floods may transport autochthonus or return allochthonous detritus from freshwater ecosystems to the
riparian (Jones and Smock 1991, Ben-David et al. 1998). In addition, aquatic
insects may be deposited in terrestrial ecosystems after mass emergence
(Hoekman et al. 2011). Little is known about the quantity of such fluxes and
their importance to terrestrial consumers and future research should investigate this neglected pathway.
33
Spatial dynamics
Predators have recently been identified as important players in nutrient dynamics (Schmitz et al. 2010). In aquatic and terrestrial ecosystems, predators
are important recipients of subsidies, however, little is known about their
role as “vectors of subsidy-derived nutrients”. Fish can contribute to the
nutrient pool in lakes by excreting terrestrial-derived nutrients (Mehner et al.
2005) and large mammals such as bears can excrete large amounts of marine-derived nutrients in terrestrial ecosystems (Hilderbrand et al. 1999). In
aquatic ecosystems, water currents and mixing might distribute excreted
allochthonous-derived nutrients within the water body, thereby potentially
supporting whole ecosystem production. In contrast, the effects of allochthonous-derived nutrients on terrestrial ecosystems might be locally restricted and might depend strongly on the mobility of the recipient consumer. Subsidies couple spatial matter and energy fluxes to the dispersal and
spatial movement of the recipient organisms, and thus promise an exciting
future in examining the linkages between (meta-) community and (meta-)
ecosystem ecology.
Feedback effects
Trophic interactions involving subsidies are often considered as donorcontrolled (Polis and Strong 1996) where the recipient consumer cannot
influence supply rates, i.e., feedbacks are assumed to be absent. However,
feedback effects might occur at the ecosystem level (Massol et al. 2011).
Sufficient inputs of subsidies to low trophic levels might increase the productivity in the recipient ecosystem to a level where it becomes a donor for
another subsidy type (Loreau et al. 2003). These feedbacks are time-lagged.
Furthermore, the recipient of the “feedback subsidy” likely differs from the
original donor. For instance, leaf litter can enhance aquatic detritivore production, and subsequently increase emergence of insects. Since receivers of
emerging insects are at higher trophic levels, the effects do not directly feedback to the original donor. Yet, the existence of such feedbacks might
change our view of donor-controlled interactions involving subsidies. The
importance of feedback loops across ecosystems remains underappreciated.
34
Intra-specific trait variation
Populations are not homogenous entities. Individuals within a population can
vary substantially in traits such as resource use (Bolnick et al. 2003), antipredator defense (Duffy 2010) or parasite resistance (Ganz and Ebert 2010).
Such individual variation might largely influence community and food web
dynamics (Bolnick et al. 2011). In particular, the coupling of spatially separated food webs might be governed by intra-specific trait variation. A few
recent studies indicated that intra-specific trait variation can affect the
movement between spatially separated food webs (Quevedo et al. 2009, Matich et al. 2011, Rosenblatt and Heithaus 2011). We highlight that trophic
polymorphism a phenomenon that is common in many animals can strongly
limit the coupling of spatially separated habitats. It is likely that other individual trait differences such as variation in growth (Moya-Laraño 2011) or
differences in individual behavior can greatly influence trophic interactions.
The study of food web dynamics would greatly benefit from a higher resolution of consumer populations.
35
Epilogue
“Multichannel subsidies produce more consumers than can be supported by
current and local resource productivity. These consumers then depress their
resources. I suggest that such processes likely underlie most (all?) strong
consumer-resource interactions in natural systems.”
Polis 1999
Before I even started thinking about studying biology, Gary A. Polis suggested that the coupling of adjacent ecosystems and habitats plays a pivotal
role in natural ecosystems. Unfortunately, I will no longer have the opportunity to meet him. What would I tell him if I could? In a nutshell, how could I
convince him of the relevance of my thesis? Well, first, this thesis provides
empirical evidence for a long-standing paradigm. Raymond L. Lindeman
was right. Secondly, this thesis highlights that the neglect of allochthonous
particulate organic carbon as a subsidy for lake ecosystems is unjustified.
Allochthonous particulate organic carbon can support lake foods webs and
we propose several mechanisms that demand further investigation. Thirdly,
this thesis adverts to potential limitations that might challenge our view on
habitat coupling through mobile organisms.
But most importantly, this thesis emphasizes that defining boundaries in an
ecological context is a challenge. Boundaries that might be apparent to us
since they seem distinct at first sight might not at all “keep […] things separate” and I imagine that Gary Polis would definitely agree. However, some
boundaries despite of lacking apparent “borderlines” do obey their classical
definition and separate things that seem contiguous.
36
Sammanfattning på svenska
Vid första anblicken verkar det som de miljöer vi kallar ekosystem är väl
definierade med tydliga gränser. Exempel på sådana ekosystemgränser kan
vara i vattenbrynet där vatten möter land eller i skogsbrynet. Inom vetenskapen har denna uppdelning länge bestått när forskare har fokuserat på enskilda ekosystem. Men ekosystemen skall för den sakens skull inte ses som slutna system utan har kopplingar mellan varandra i till exempel utbytet av organiskt material. Ett sådant utbyte sker när insekter blir uppätna på land efter
att haft sin tillväxtfas som larver i vatten. Ett motsatt utbyte sker när löv eller
landlevande djur faller ned i ett vattendrag och blir till ny näring. Eftersom
en del av näringen kommer utifrån men konsumeras inom systemet kan det
ses som ett externt näringsbidrag.
Ekosystem i sig själva är inte likformiga enheter utan är komplext uppbyggda av mer eller mindre distinkta levnadsmiljöer (även kallade habitat).
Sjöar är bland annat uppdelade i strandzonen och det öppna vattnet. På grund
av växtligheten i strandzonen är den mer komplext uppbyggd än det öppna
vattnet. Fiskarna i sjön kan förflytta sig mellan de olika habitaten för att söka
föda (även kallade resurser) och på så sätt kopplar de samman det strandnära
och det öppna vattnet. Men trots det tenderar fiskar att utveckla karaktärer
som speglar det habitat de lever mest i. Abborrar som lever i vassruggar nära
strandzonen är ofta korta och högryggade eftersom de måste manövrera i tät
vegetation. De fiskar som däremot lever i det öppna vattnet jagar byten
spridda över en större vattenmassa och är därmed mer strömlinjeformade för
att göra det mindre energikrävande att simma längre sträckor. I teorin borde
fiskar som är bättre anpassade till öppna vatten vara sämre anpassade till
vatten nära strandzonen, och tvärtom. Denna uppdelning eller divergens
mellan fiskpopulationerna som lever i det öppna och strandnära vattnet bör
begränsa kopplingen mellan habitaten, men man vet mycket lite om hur generell denna divergens är och mer exakt vilka faktorer det är som styr den.
Miljöfaktorer, som till exempel vattnets klarhet har visat sig kunna förändra abborrarnas födosöksbeteende. Eftersom abborren är ett rovdjur, som
identifierar sina byten i första hand med synen, leder ökad grumlighet av det
öppna vattnet ofta till en nedsatt förmåga till bytesfångst. Alternativt söker
då abborren sina byten på sjöbotten, vilket kräver mindre av synförmågan. I
ett laboratorieförsök kunde jag visa att abborrar som gör sina födosök på
bottenlevande djur inte alls var begränsade av vattnets grumlighet. Sådana
skillnader i fångststrategier som grundar sig på vattnets klarhet, skulle kunna
37
påverka divergensen och därmed hur ofta abborren besöker de olika habitaten.
I min avhandling har jag intriktat mig på att koppla ihop ekosystem i två
rumsliga skalor: i) kopplingen mellan sötvatten- och landekosystem via flöden av organiskt material, och ii) kopplingen inom sötvattensystemet mellan
strandzonen och det öppna vattnet, via fiskarnas förflyttning mellan habitaten. I den första delen undersöker jag näringsutbytet mellan sjö- och landmiljöer och effekterna på de djur som är mottagare av extern näring. I den andra
delen undersöker jag om vattnets klarhet kan påverka divergensen mellan de
två populationerna av abborre i det strandnära och det öppna vattnet och om
dessa skillnader har potential att påverka kopplingen mellan habitaten.
Jag gjorde en litteraturgenomgång på publicerade data om kopplingarna
mellan land- och vattenmiljöer. Jag fann att sötvattensekosystem erhöll dött
organiskt material och bytesorganismer från intilliggande landmiljöer medan
landmiljöer i huvudsak erhöll bytesdjur från sötvattensystemen. Inflödet av
organiskt material från land till sjö är således betydligt större än det motsatta
flödet. Mottagande djurliv gynnas betydligt av detta resursflöde, i medeltal
har 42% av deras biomassa sitt ursprung från angränsande ekosystem. Det
som är förvånande är att material som producerats utifrån det egna systemet
hade samma effekt på djurs biomassatillväxt i både sötvatten och land oavsett mängden inflödande material. En förklaring kan vara den låga kvaliteten
på det organiska materialet som kommer från land.
Jag utförde en fältundersökning i mellersta Sverige som inkluderade tre
sjöar med hög och fyra sjöar med låg vattenklarhet. Jag provtog abborrar
från både det öppna och strandnära vattnet och undersökte maginnehållet
och fiskarnas kroppsform. Sjöarna skiljde inte alltid i sin resurssammansättning och biomassa mellan det strandnära och öppna vattnet. Jag fann att vid
hög vattenklarhet hade abborrarna utvecklat en starkare divergens och habitatspecifik kroppsform för respektive habitat. Abborrarna i det starandnära
habitatet var högryggade medan de var strömlinjeformade i det öppna vattnet. Båda formerna utnyttjade resurser från sitt egna habitat. Fyndet av olika
kroppsformer mellan habitaten tyder på att det inte rör sig om något övergående utan snarare ett permanent fenomen. Jag drog slutsatsen att kopplingen
mellan habitaten genom abborrars förflyttning, troligen är begränsad i klarvattensjöar. I grumliga sjöar var abborrarna mera strömlinjeformade och
skillnaden i kroppsform mellan de olika habitaten var mindre uttalad. Detta
tyder på att det strandnära och det öppna vattnet är starkare kopplat om vattnet är grumligt. Utnyttjandet av resurser från det öppna vattnet var generellt
högt i både det strandnära och det öppna vattnets populationer. Resursbiomassan var lika stor i samtliga sjöar och abborrarnas bytesfångst av bottenlevande djur påverkades inte av sjöarnas klarhet. Detta antyder att tillgången
på byten nära strandzonen var mindre när vattnet var grumligt. Medan
kroppsformen är mindre begränsande för abborrarnas förflyttningar mellan
38
habitaten i grumliga vatten är istället minskad tillgång av resurser en förklaring till minskat utnyttjande av strandnära resurser.
Sammanfattningsvis kan man säga att gränserna mellan land och sjö är
mindre tydliga än man trott. Jag har kunnat visa att det finns en koppling
mellan land och sötvatten genom ett resursflöde mellan de båda ekosystemen
och att det mottagande djurlivet drar stor nytta av detta resursflöde. Även
fast det inom sjöar inte uppvisas några tydliga förflyttningshinder kan abborrarna vara ovilliga att lämna habitat som de är tydligt anpassade till.
Acknowledgments
I would like to thank Philipp Hirsch and Mikael Jönnson for valuable comments on this part of the thesis. I would further like to thank Mattias Vass for
translating the Swedish Summary into sammanfattning på svenska, and especially for letting me pretend to my supervisors until now that I did it. I also
thank Jovanna Kokic, Konrad Karlsson and Göran Kläppe Sundblad for
further improving the Swedish summary.
39
Acknowledgements
Now, this is almost the hardest part – if you can be sure of one chapter of
your thesis that will be read by everyone and I mean EVERYONE, well,
that’s where we are now. In the past 4.5 years, I met a bunch of people, and
many of them have contributed in one or another way to this thesis and I
would like to thank all of them!
But first of all I want to thank my supervisors: Peter, you have been all I
could have hoped for – you have always let me pursue my own ideas, even
supported them; you were always there when I needed you. Your endless
and sometimes unreasonable optimism always made me laugh. Thank you so
much for everything! Lars, although you have not been involved too much
in my work (at least scientifically), you have always been there – thank you
for supporting me, for solving problems, for commenting from a non-fish
perspective, and especially for your peculiar humor.
Hannes – without you it just wouldn’t have been the same. You always
were my rock and I couldn’t thank you enough for taking all the crap from
me. Thank you for all the laughs (and tears). It’s been an unforgettable journey! Philipp, my officemate in crime, where would I be without you? Thank
you for so many inspiring ideas, discussions, advice, and support inside (and
outside) the office. You were always good for a surprise – I never really told
you how much I appreciated that. Cristian, I will never forget Abisko. Although we could “barely lift our arms” it was one of the best times. Thank
you for being such good company – in the field and elsewhere. Göran, you
have been missed! The office was just not the same without you – conditions
were perfect.
I want to thank all the other current and former limnos. My fellow PhD
students, Lorena for 3.5 unforgettable bottles of red wine, Anne for being
such a caring person, Mercè for being such a lovely person, Hannah for
shifting our office to a female bias, Frida, Sara, Inga, Valerie, Blaize, Monica, Torsten, Roger, thank you for all the fun. Kristin and Katrin, you
have been wonderful – thank you for your support and advice (in many
ways). Janne J., the man in the background – thank you for all the emergency counts of zooplankton - without your help I might have even had to do it
myself. Richard, thanks for fun fish meetings and for always being so critical. Anna B. and Eva, thanks for all the organization around my teaching
activities. Anna S., thanks for taking care of Ren and Stimpy and the other
pests every time I was gone. Silke, Sebastian, Gesa, Jerôme, Charles, Ste40
fan, Ina, Eddie, Jürg, Preetam, Dolly, Omneya, Birgit, Alex, thank you
all for making the limno department such as nice, interesting, and friendly
place.
I also want to thank the other former and current people at EBC: Björn
for providing me with Passiflora spp. over the years, Jossan and Mirjam
for organizing EBC pubs, Amber for an awesome Iceland trip, Richard B.
for being such a good listener, Göran A. for always answering statistical
questions, and Kasia, Sandra, Mårten, Matt, Fernando, Holger, Arild,
Leanne, Lisa, and all the other people I forgot for making my life inside and
outside EBC so much more fun.
Thanks also to my collaborators: Julien, it’s been great working with you.
Thank you, Janne K. for the time in Abisko, and Mats for always giving
valuable comments on the manuscript. Also a big thank you to the rest of the
LEREC group! Helmut, I guess I can - at least partly – blame you for ending
up where I am. Thank you for that and for jumping on the meta-analysis.
I want to thank all the people that helped me in the field and in the lab without you my PhD would have not been possible in 4.5 years. Thank you
Jana, Cathrine, Angelica, Anna G., Amélie, Maria, Cyrille, Krijn, Michi, Markus Möscht, and Johnny for devoting your time to fish stomachs
and endless hours of watching perch do nothing.
Although I spent a lot of time at work, there was also a life outside Norbyvägen (although some of the following people might have occasionally
been seen there). Paolo, you are my hero – your genius mind helped me in
endless work and not so much work-related situations. Thank you for your
honesty and directness – although sometimes cruel, it was always appreciated! The girls, Lauren, Katja, Lára, Reelika, Andrea – thank you for all
the girls´ nights and talks (especially lately). Thanks for always having an
open ear and constructive advice! Brian, you have been such a wonderful
friend for almost the entire time. I enjoyed every minute. Erik, Uppsala has
not been the same without you! Thank you for a memorable stay in Abisko,
MTB, and for listening to my gossip (I know you enjoyed it!). Margo, your
stay was way too short – I hope we will meet again soon. Mattias, you are
one of the most tolerant people I know - thank you for being there. Kathie,
thank you for so many lovely coffees and dinners.
My friends back home – I miss you all so much! Although I was gone for
such a long time (and the future predicts no improvement) I know you will
always be there for me. Jennifer, thank you for giving me a “second
chance” (after my first impression on you ;)). Maybe we’ll find a place
where flagellates and fish are equally appreciated… Sarah and Susa, thank
you for naming a room after me and for being such wonderful friends. Jule,
people always accuse me of being such a globetrotter – I wish they had met
you. Thank you for including me in the “Osenauer Silvester” – before that
New Year’s was really not that special. JüJü, although I still call you my
former boss sometimes, you have always been more than that – thank you
41
for being there, always. Thank you Bine for introducing me to the world of
Bayer and for making me realize that the economy is a monster that I will
never ever have anything to do with. Vanessa, thank you so much for taking
over my “precious” - leaving him behind was one of the toughest decisions
of my life but I know you take such good care of him. And thank you Barbara for being such a wonderful friend, a good listener, and an even better
advisor.
My family – I am still convinced that you have no idea what I have actually been doing the last 4.5 years – never the less that makes me even more
thankful for always supporting me. Mutter – Du bist die Grösste! Pa und
Karin – Danke! Pa, Du bist offiziell mein häufigster Besucher. Danke für
alles! Onkel Peter – Immer für mich da! Danke! Bruderherz, every time
someone asked me whom I missed most – well, you were at least always
number two. Thank you so much for being a role model, a friend, and the
best brother ever!
Finally, I want to thank my best friend – Ena, I am so grateful for our
friendship. Next year we’ll make the 20! You have been so far away physically (especially during the last two years), but so close otherwise. You pursued your dream – and look where you are now – I am so proud of you!!!
Maybe, one day, we’ll find a place that we both enjoy… Thank you for everything - always!
42
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