Download Benthic use of phytoplankton blooms: Agnes M. L. Karlson

Benthic use of phytoplankton blooms:
Uptake, burial and biodiversity effects in a species-poor system
Agnes M. L. Karlson
Department of Systems Ecology
Stockholm University
Doctoral thesis in Marine Ecology, 2010
Agnes Karlson, [email protected]
Department of Systems Ecology
SE-106 91 Stockholm
Sweden
© Agnes Karlson, Stockholm 2010
ISBN 978-91-7155-991-3
Printed by US-AB, Stockholm, Sweden
Cover illustration by Ilmari Hakala, 2009
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ABSTRACT
Animals living in marine sediments, the second largest habitat on earth, play a major role in
global biogeochemical cycling. By feeding on organic matter from settled phytoplankton
blooms they produce food for higher trophic levels and remineralize nutrients that can fuel
primary production. In the Baltic Sea, anthropogenic stresses, such as eutrophication and
introductions of invasive species, have altered phytoplankton dynamics and benthic
communities. This thesis discusses the effects of different types of phytoplankton on the
deposit-feeding community and the importance of benthic biodiversity for fate of the
phytoplankton bloom-derived organic matter.
Deposit-feeders survived and fed on settled cyanobacterial bloom material and in doing so
accumulated the cyanobacterial toxin nodularin. Their growth after feeding on cyanobacteria
was much slower than on a diet of spring bloom diatoms. The results show that settling
blooms of cyanobacteria are used as food without obvious toxic effects, although they do not
sustain appreciable growth of the fauna. Since all tested species accumulated the cyanotoxin,
negative effects higher up in the food web can not be ruled out. Both species composition and
richness of deposit-feeding macrofauna influenced how much of the phytoplankton bloom
material that was incorporated in fauna or retained in the sediment. The mechanism behind
the positive effect of species richness was mainly niche differentiation among functionally
different species, resulting in a more efficient utilization of resources at greater biodiversity.
This was observed even after addition of an invasive polychaete species. Hence, species loss
can be expected to affect benthic productivity negatively. In conclusion, efficiency in organic
matter processing depends both on pelagic phytoplankton quality and benthic community
composition and species richness.
Key words: biodiversity, ecosystem functioning, benthic-pelagic coupling, niche, resource
partitioning, competition, eutrophication, cyanobacterial blooms, diatoms, invasive species,
Baltic Sea
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Contents
LIST OF PAPERS
5
INTRODUCTION AND AIMS
6
BACKGROUND
Benthic-pelagic coupling – processes fundamental for ecosystem functioning
Links between Biodiversity and Ecosystem functioning
Mechanisms relating biodiversity to ecosystem functioning
Current challenges in research on biodiversity and ecosystem functioning
Importance of food quality in ecosystem functioning
Deposit-feeders and food quality
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7
7
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STUDY SYSTEM: THE BALTIC SEA
Anthropogenic influences
Phytoplankton blooms in the Baltic Sea
Nutritional aspects of blooms
Baltic soft-bottom benthos
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EXPERIMENTAL APPROACH
Isotope tracers in food-web studies
Stable isotopes
Assessing growth and nutritional value to animals
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14
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RESULTS AND DISCUSSION
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Importance of phytoplankton quality for benthic fauna
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Cyanobacteria as a food source
Changes in phytoplankton dynamics affect benthic production?
Biodiversity effects on processing of phytoplankton bloom material
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Mechanisms behind biodiversity effects on measured processes
Long term changes in benthos: implications for ecosystem functioning
Recent changes in benthic biodiversity: implications for ecosystem functioning
Generalizations of biodiversity results to other systems
CONCLUSIONS AND SUGGESTIONS FOR FUTURE RESEARCH
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ACKNOWLEDGEMENTS
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LITERATURE CITED
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LIST OF PAPERS
This thesis is based on the following five papers, referred to in the text by their roman
numerals. Published papers are reprinted with permission of the publishers.
I
Karlson AML, Nascimento FJA, Elmgren R (2008). Incorporation and burial of
carbon from settling cyanobacterial blooms by deposit-feeding macrofauna.
Limnology and Oceanography 53(6): 2754-2758
II
Karlson AML and Mozuraitis R. Deposit-feeders accumulate the cyanobacterial toxin
nodularin. (Manuscript)
III
Nascimento FJA, Karlson AML, Näslund J, Gorokhova E (2009). Settling
cyanobacterial blooms do not improve growth conditions for soft bottom meiofauna.
Journal of Experimental Marine Biology and Ecology 368: 138-146.
IV
Karlson AML, Nascimento FJA, Näslund J, Elmgren R. In press. Higher diversity of
deposit-feeding macrofauna enhances phytodetritus processing. Ecology
V
Karlson AML, Blomgren Rydén S, Näslund J. Effects of a polychaete invader on
ecosystem functioning in a species-poor soft bottom. (Manuscript).
My contributions to the papers: (I, V) –Major part in experimental design and execution,
responsible for all analyses and data processing, writing. (II) – Major part in experimental
design and execution, preparation of samples for mass spectrometry, data processing, writing.
(III) – Participated in experimental design and execution and contributed in writing (IV) –
Participated in experimental design and execution, responsible for all analyses and data
processing, major part in writing.
Additional publications by the author of this thesis:
Karlson AML, Almqvist G, Skora KE, Appelberg M (2007). Indications of competition
between non-indigenous round goby and native flounder in the Baltic Sea. ICES Journal of
Marine Science 64: 479-486
Nascimento FJA, Karlson AML, Elmgren R (2008). Settling blooms of filamentous
cyanobacteria as food for meiofauna assemblages. Limnology and Oceanography 53 (6):
2636-2643
Karlson AML and Viitasalo-Frösen S (2009). Assimilation of
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C-labelled zooplankton
benthic eggs by macrobenthos. Journal of Plankton Research 31 (4): 459-463
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INTRODUCTION AND AIMS
The study of trophic interactions is central to ecology. Determining the factors regulating
trophic transfer of energy and nutrients is essential for understanding ecosystem productivity.
Marine sediment ecosystems cover about 70% of the planet’s surface and sediment-living
organisms play a major role in global biogeochemical cycling and hence are key components
in ecosystem functioning. By feeding on organic matter from settled phytoplankton blooms
they produce food for higher trophic levels, including fish. Faunal feeding activities also
result in burial of bloom material into the sediment, where break-down of organic matter
(mineralization) is slower, so that the bloom material can serve as food for the animals over a
longer period of time. The overall aim of this thesis is to study the role of sediment-living
animals in these two fundamental ecosystem processes connecting the bottom of the sea
(benthos) with the open water (pelagic ecosystem). The simple ecosystem of the Baltic Sea is
a good model system for detailed studies on the role of biotic factors for these processes, also
because it experiences large scale changes in both phytoplankton dynamics and benthic
biodiversity. Little is known of how increased blooms of toxic cyanobacterial blooms and
invasive species affect marine ecosystem productivity. I experimentally studied how
phytoplankton bloom material that reaches the sediment is processed by benthic fauna. More
specifically, I have focused on the importance of phytoplankton quality for growth and
nutrition of deposit-feeding macrofauna (I-V) and how macrofaunal species composition and
species richness affect incorporation and burial of the bloom material (IV and V).
Primary production
PHOTIC ZONE
INO
RG
AN
IC
NU
T
RIE
NT
S
APHOTIC ZONE
Sedimentation
Trophic transfer
Faunal incorporation
Mineralization
Microbial
loop
Burial
Figure 1. Simplified illustration of benthic-pelagic coupling from a food-web perspective. This thesis
discusses mainly incorporation and burial of bloom material whereas mineralization has been measured
only indirectly. Processes in grey are given only to present the larger picture into which the studied
processes fit.
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BACKGROUND
Benthic-pelagic coupling – processes fundamental for ecosystem functioning.
In aquatic ecosystems, a considerable proportion of the primary production from
phytoplankton blooms sink to the sediment (Wetzel 1995; Lignell et al 1993). Most benthic
communities below the photic zone are entirely dependent on such imported organic matter
(Elmgren 1978; Graf 1992). The growth and population dynamics of detritus-feeding animals
living in sediments, so called deposit-feeders, are tightly coupled to sedimentation of organic
material from the pelagic zone (e.g. Elmgren 1978; Graf 1992; Goedkoop and Johnson 1996;
Lehtonen and Andersin 1998).
Deposit-feeders play a key role in deep benthic ecosystems by converting detritus to
secondary production available for higher trophic levels (Snelgrove et al. 1997). Also, the
feeding, respiration and burrowing activities by the animals, collectively called bioturbation,
have a major impact on the biogeochemical cycling of elements that limit primary production
and hence on whole-scale ecosystem productivity (Meysman et al. 2006). The break-down of
the deposited phytodetritus results in regeneration of nutrients in inorganic form
(mineralization) that are subsequently made available for phytoplankton through bioturbation
and mixing of water masses (Nixon 1981; Blackburn 1988; Graf 1992).
The impact by deposit-feeders on mineralization can be both direct, through the metabolism
of the animals and indirect, by stimulating bacterial activity. For instance, bioturbation results
in enhanced transport and mixing of solids and solutes due to the increased area of sedimentwater interface and improved oxygenation of deeper anoxic sediments, which enhance
microbial activity and increase the mineralization rate (Aller and Aller 1998; Kristensen 2000;
Mermillod-Blondin and Rosenberg 2006). Furthermore, bioturbation may result in burial of
the settled phytoplankton into deeper sediment layers, where anoxia slows the rate of
decomposition (Kristensen et al. 1995; Blair et al. 1996; Andersen 1996; van de Bund et al.
2001). In temperate water, the input of phytoplankton bloom material to sediments is a
seasonal phenomenon and buried phytodetritus may therefore fuel the soft bottom
communities for many months (Rudnick and Oviatt 1986; Andersen and Kristensen 1992;
Josefson and Hansen 2003). Finally, bioturbation activities may influence population structure
of the pelagic organisms with inactive benthic life-stages, e.g. resting cells of phytoplankton
or dormant eggs of zooplankton, through facilitating or inhibiting their emergence from the
sediment (Hairston et al. 2000; Ståhl-delBanco and Hansson 2002; Viitasalo et al. 2007).
Links between Biodiversity and Ecosystem functioning
Until recently, the assumption has been that biodiversity is the dependent variable responding
to changes in ecosystem processes or functions (e.g. primary productivity or organic matter
input) (Naeem 2002). However, due to rapid anthropogenically driven extinction rates and
spread of non-indigenous species there are concerns that altered biodiversity will affect the
“ecological services” that ecosystems provide to humanity (Costanza et al. 1997; Chapin et al.
2000; Hooper et al. 2005). The main biodiversity aspect studied in this thesis is species
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richness, however biodiversity in its broadest sense refers to genetic, taxonomic and
ecological diversity over all spatial and temporal scales.
Three main hypotheses that relate the responses of ecosystem processes to reductions in
species richness have been proposed (e.g. Lawton 1994). First, the linear, “rivet” hypothesis
suggests that all species contribute to ecosystem function (e.g. Lawton 1994). Second, the
“redundancy” hypothesis suggests that ecosystems can lose many species with no
consequences for their performance, as long as the major functional groups are still present,
i.e. it is not the number of species per se which is important but the functional traits of the
species (Walker 1992; Lawton 1994). Third, the “idiosyncratic” hypothesis states that species
diversity affects ecosystem processes, but not in a predictable direction, because the roles of
individual species are complex and context-dependent (Lawton 1994; Naeem et al. 1995).
Clearly, the type of relationship observed depends on which measures of biodiversity (e.g.
species richness within one or across several trophic levels) and on which function or
functions are being considered.
Mechanisms relating biodiversity to ecosystem functioning
Accumulating theoretical and empirical evidence suggests a common positive relationship
between biodiversity and ecosystem functioning (e.g. Loreau et al. 2001; Hooper et al. 2005;
Cardinale et al. 2006). However, understanding the mechanisms that underpin this presumed
causal relationship remain an important challenge when trying to predict the environmental
consequences of species loss or addition (Loreau and Hector 2001; Naeem 2002; Fox et al.
2005). Three mechanisms that have been proposed to explain a positive relationship between
species richness and ecosystem functioning are: (i) niche/trait differentiation, (ii) facilitation
and (iii) the selection or dominance effect. The niche is often represented as an n-dimensional
space, consisting of environmental conditions, resource levels and densities of other
organisms, together allowing for the survival, growth and reproduction of species
(Hutchinson 1957 in Leibold 1995). In this thesis, the niche concept is discussed mainly in
relation to food resource partitioning.
(i) Niche differentiation results from reduced interspecific competition through e.g. food
resource partitioning. If species use different resources, more of the total available resources
can be used and if these resources limit growth, then increasing richness should lead to greater
productivity in an ecosystem (e.g. Tilman et al. 1997; Griffin et al. 2008).
(ii) Facilitation occurs when coexisting species positively affect a process through direct
interaction (e.g. Cardinale et al 2002; Bulleri et al. 2008).
(iii) The dominance or selection effect occurs through selective processes, such as
interspecific competition, which cause dominant species to outperform others in multi-species
treatments (e.g. Cardinale et al. 2006; Jiang et al. 2008).
Both niche differentiation and facilitation can increase the performance of communities above
that expected from the performance of individual species, and are collectively referred to as
complementarity. Dominance and complementarity, are both ecologically interesting
mechanisms that can be confused with an experimental artifact called the “sampling effect”
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(Huston 1997), which is the increased probability with increased species richness of including
a species with a particular trait in species-rich treatments.
Analysis and interpretation of biodiversity experiments have progressed from simple
comparisons of i.e. primary production across treatments to examining changes in relative
performance (relative yield) among component species within and between treatments.
Loreau and Hector (2001) used an equation to partition the net diversity effect (the observed
deviation from the value predicted from individual species monoculture performance) into
complementarity and selection components. Positive complementarity occurs when species
function better than expected when combined, independently of their traits and not at the
expense of other species. Dominance is analogous to natural selection in evolution (Price
1970) and occurs when species with particular traits dominate at the expense of other species.
Fox (2005) further refined the equation, to take into account that species may have nested
niches (trait-dependent complementarity), with species with wide niches attaining high
relative yield in multi-species treatments, but not at the expense of species with narrow
niches. See Box 1 for details.
Box 1. Definitions and ecological interpretations (bold style) of diversity components calculated
according to Fox (2005). The outcome for ecosystem functioning are also shown (bold style).
TIC=Trait-independent complementaritry, TDC=trait-dependent complementarity, D=dominance.
Positive value
TIC
TDC
D
Negative value
Species increase their performance /
yield without affecting other species.
Species decrease their performance /
yield at the expense of other species.
Facilitation or niche differentiation
→ Over-yielding
Competition or inhibition
→ Under-yielding
Species with high monoculture yield
increase their performance without
affecting other species
Species with low monoculture yield
increase their performance without
affecting other species
Nested niches → Over-yielding
Nested niches → Under-yielding
Species with high monoculture yield
dominate mixtures at the expense of
other species
Species with low monoculture yield
dominate mixtures at the expense of
other species
No niche differentiation
→ Over-yielding
No niche differentiation
→ Under-yielding
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Current challenges in research on biodiversity and ecosystem functioning
As stated above, a prerequisite for differentiating among the possible mechanisms behind
observed biodiversity-ecosystem functioning relationship is to determine the species-specific
contribution to the measured process in mixed species assemblages. However, this is only
possible when measuring non-cumulative processes (Rafaelli et al. 2003). Another problem
that complicates interpretation of experimental results is that the effects of species loss have
often been simulated by randomly or otherwise artificially reducing the species assemblages
of naturally diverse ecosystems (see review by Loreau et al. 2001). Randomized species
removal may result in the loss of a whole functional group present in the original community,
sometimes leading to highly artificial set-ups with results difficult to translate to natural
ecosystems (Bracken et al. 2008). Also, it is difficult to make inferences about the functioning
of natural systems if only a single process has been measured, since different species can
maximize different processes. Hence an approach measuring multiple processes is
recommended (Gamfeldt et al. 2008). Moreover, integration with food web ecology is
desirable since both bottom-up and top-down processes strongly affect secondary production
and cycling of nutrients (Duffy et al. 2007; Woodward 2009). In other words, an important
current challenge is to understand how trophic structure affects the relationship between
biodiversity and ecosystem functioning.
Importance of food quality in ecosystem functioning
The flux of organic matter and nutrients in a food web is affected not only by the quantity but
also the quality (elemental and biochemical content) of the food (Sterner and Elser 2002).
Rates of ingestion, digestion, absorption and assimilation and resulting growth all depend
critically on food quality. Research on the relationship between food quality and secondary
production has so far concentrated on zooplankton (Brett and Müller-Navarra 1997; Sterner
and Elser 2002; Vrede et al. 2002). Food availability and manageability affect ingestion
efficiency, e.g. filamentous cyanobacteria may clog zooplankton feeding appendages (Holm
et al. 1983). Differences in cell wall structure and in the level of decomposition of ingested
food affects digestibility, and the chemical composition of the food affects the efficiency with
which it is absorbed and assimilated. In particular, nitrogen (N) and phosphorus (P) have been
considered important in this context (Elser and Sterner 2002). Large differences in elemental
composition between the food source and the consumer have implications both for the growth
of the consumer and for nutrient recycling in food webs (Sterner and Hessen 1994; Elser and
Urabe 1999). The elemental limitation approach may, however, rather reflect limitation of one
or more specific organic compounds (Müller-Navarra 1995). In recent years, the importance
of essential long-chain poly-unsaturated fatty acids and sterols for invertebrate growth and
reproduction has been demonstrated (Brett and Müller-Navarra 1997; von Elert et al. 2003). P
content is sometimes a good predictor of the content of polyunsaturated fatty acids in
phytoplankton material (Ahlgren et al. 1997), suggesting that it is important to take both
approaches into account when the evaluating the nutritional quality of food. In addition, other
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factors, such as toxicity, are also important (Lampert 1981). Coping with toxin related stress
may constrain the energy available for growth (Dahl et al. 2006).
Deposit-feeders and food quality
A particular challenge for deposit-feeders arises from the low levels of organic matter
available to them in the sediment, forcing them to ingest large volumes of sediment in order
to meet their nutritional requirements. They are often bulk-feeders, but can also be selective in
terms of the organic-rich fraction of the sediment, feeding depth and particle size (Lopez and
Levinton 1987). Especially nitrogen seems often to be limiting in benthic systems below the
photic zone (Tenore 1988). Organic matter is mineralized at different rates depending on its
chemical composition and on oxygen conditions in the sediment (Kristensen et al. 1995;
Middelburg and Levin 2009). High quality organic matter may be decomposed rapidly in
oxidized sediment, whereas organic matter which is more refractory can function as food for a
longer time, thus contributing to long-term productivity despite its lower quality. Some subsurface feeders show a preference for feeding on old organic matter rather then fresh
phytodetritus (Rudnick and Oviatt 1986; Widbom and Frithsen 1995; Byren et al. 2006).
Goedkoop et al. (2007) found that a sediment-dwelling freshwater midge could synthesize
essential polyunsaturated fatty acids from low levels of shorter homologues, an example of an
adaptation to a poor-quality food source.
Temporary meiofauna and meiobenthos, such as bivalve spat and benthic eggs of
zooplankton, may also serve as supplemental food sources (Elmgren et al. 1986; Karlson and
Viitasalo-Frösen 2009). Bacteria play dual roles as organic matter decomposers by
remineralizing organic carbon (into CO2) and as biomass producers (by incorporating carbon
from the environment). Since they usually constitute a small fraction of the diet of
macrofaunal deposit-feeders (Goedkoop and Johnson 1994), bacteria are still considered
mainly a sink for organic matter in the sediment (van Oevelen et al. 2006). However, bacterial
and meiofaunal conditioning of refractory organic matter may be an indispensable processing
step in transforming organic matter into a form more readily digestible for macrofauna
(Tenore et al. 1977). Bacterial activity can further facilitate trophic transfer through
degradation of harmful natural toxins in organic matter (e.g. Mazur-Marzec et al. 2009). In
conclusion, facilitative interactions among taxa can have a positive effect on trophic transfer
and mineralization efficiency.
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STUDY SYSTEM: THE BALTIC SEA
The Baltic Sea is a large, semi-enclosed, shallow brackish water system. Due to its recent
geologic origin and low salinity, species diversity is low, with very few endemic species.
Inflows of saline water from the North Sea through the Danish straits in combination with
freshwater run-off result in a salinity gradient, ranging from about 20 in the south to 2 in the
northern Bothnian Bay. The saltwater intrusions depend on specific weather conditions over
the North Atlantic (Schinke and Matthäus 1998) and occur irregularly. The saltwater inflows
create a strong permanent halocline at 60-80 m depth in the Baltic proper, which reduces
vertical exchange between surface and bottom water. Under the halocline, oxygen is depleted,
in the deeper parts generally to the point of anoxia.
Anthropogenic influences
More than 85 million people live within the drainage basin of the Baltic Sea and the
ecosystem is under severe anthropogenic stress, through over-fishing, eutrophication and
hazardous chemicals (Elmgren 2001). Increased nutrient load from anthropogenic activities
during the last half century (Larsson et al. 1985) has resulted in increases in phytoplankton
production and subsequent sedimentation of organic material (Jonsson and Carman 1994).
This has resulted in anoxic bottoms becoming more widespread in the Baltic (Karlson et al.
2002). Since most multicellular organisms need oxygen, eutrophication negatively affects
benthic fauna abundance, distribution, and diversity. Anoxic bottoms also influence cycling of
nitrogen and phosphorus, which may result in accelerated eutrophication (Middelburg and
Levin 2009).
Another aspect of the anthropogenic influence is the largely unintentional spread of exotic
species. In the last few decades more than 100 non-indigenous species have been recorded in
the Baltic Sea, and about 70 of these have established reproducing populations (Olenin and
Leppäkoski 1999; Leppäkoski et al 2002). The invasions of exotic species have significantly
changed communities (Zettler et al. 1995; Perus and Bonsdorff 2004) and food web structure
(Gorokhova et al. 2005) in the Baltic Sea.
Phytoplankton blooms in the Baltic Sea
As in other boreal waters, production is strongly pulsed and a succession of phytoplankton
blooms takes place (Andersson et al. 1996; Höglander et al. 2004). The two major bloom
events are the spring bloom, dominated by diatoms, and the summer bloom, dominated by
filamentous, nitrogen-fixing cyanobacteria. The sedimentation of the spring bloom is high
(Elmgren 1978; Lignell et al. 1993), since diatoms sink rapidly and zooplankton abundance at
this time of the year is not high enough to graze down the algal biomass.
Cyanobacterial blooms have been reported to have increased in frequency, biomass and
duration in recent decades, probably due to increased phosphorus concentration as a
consequence of eutrophication (Finni et al. 2001; Poutanen and Nikkilä 2001). The settling of
cyanobacteria to the sediment have previously been considered negligible, but Gustafsson et
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al. (2004) recently showed that sediment trap collections may underestimate true rates of
summer sedimentation several-fold in the Baltic Sea. Presence of pigment, toxin and isotope
signatures specific for cyanobacteria have been demonstrated in Baltic proper sediments
(Bianchi et al. 2000; Mazur-Marzec et al. 2007; Voss et al. 2005), suggesting that the
cyanobacterial input to sediments may previously have been underestimated.
Nutritional aspects of blooms
Diatoms are generally considered to be good food for both zooplankton and benthic depositfeeders due to their high content of lipids and polyunsaturated fatty acids, which are made
available to the benthos due to efficient sedimentation (Andersson et al. 1993; Ahlgren et al.
1997). Sedimentation of spring bloom material results in rapid growth of benthic fauna, both
in the Baltic (Elmgren 1978; Cederwall 1979; Lehtonen and Andersin 1998, Ólafsson and
Elmgren 1997) and in lakes (Johnson and Wiederholm 1992). Cyanobacteria, on the other
hand, have commonly been considered a low quality food source due to their potential
toxicity and low content of polyunsaturated fatty acids (e.g. DeMott and Müller-Navarra
1997; Engström et al. 2000).
Figure 2. Surface accumulations of filamentous, nitrogen-fixing cyanobacteria, dominated by the toxic
species Nodularia spumigena, in the Baltic proper, July 8, 2005 (courtesy of M. Kahru).
In the Baltic Sea, the most common toxin is nodularin, which is produced by the filamentous
nitrogen-fixing cyanobacterium Nodularia spumigena (Sivonen et al. 1989). Nodularin is a
potent hepatotoxin, and surface accumulations of toxic cyanobacteria (Figure 2) have resulted
in deaths of domestic animals and cause health concerns most summers (Edler et al. 1985). N.
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spumigena and nodularin have been shown to have negative effects on survival and
reproduction of pelagic and littoral invertebrates and increased blooms of toxic cyanobacteria
are suspected to have effects at the ecosystem level (Karjalainen et al. 2007). Several field
studies have confirmed that bioaccumulation of nodularin takes place in Baltic zooplankton
(Karjalainen et al. 2006), filter-feeders such as blue mussels and clams, and fish (e.g. Sipiä et
al. 2001; Kankaanpää et al. 2001). Since it is generally assumed that cyanobacterial toxins are
more harmful to vertebrates, including fish, than to other aquatic organisms (Kiviranta et al.
1991), nodularin may pose a health risk via transfer and accumulation in the food web. In
addition, toxins other than nodularin are produced by cyanobacteria, for example the newly
discovered neurotoxin beta-methylamino-L-alanine (Cox et al. 2005), which is suspected to
reach humans through food chain transfer (Jonasson et al. 2008).
Baltic soft-bottom benthos
In the Baltic proper the soft-bottom community below the photic zone is dominated by only
4-7 macrofaunal species (Elmgren 1978) and about 50-60 meiofauna species (Elmgren 1976).
Only three common species of native macrofauna are classified as deposit-feeders: the
amphipods Monoporeia affinis and Pontoporeia femorata and the facultatively suspensionfeeding bivalve Macoma balthica (Figure 3). The amphipods are morphologically similar but
have different origin and ecological characteristics. M. affinis is a freshwater glacial relict
while P. femorata is of marine origin. M. affinis is more active, has higher fecundity
(Cederwall 1979) and is found closer to the sediment surface than P. femorata (Hill and
Elmgren 1987). Both amphipods have a 2-year life cycle at sub-thermocline depths and are
commonly the most abundant species, often occurring in densities of over 2000 ind m-2
(Ankar and Elmgren 1976; Cederwall 1999). They are night-active and mate during October
to December, after which the males die. Females die after releasing juveniles around the time
the spring bloom settles (Sundelin and Eriksson 1998). M. balthica often dominates the
macrobenthic biomass in the Baltic (Ankar and Elmgren 1976, Laine 2003). It has a longer
life cycle, and can live up to 27 years in deep waters (Segerstråle 1960). It switches feeding
mode between suspension- and deposit-feeding, depending on food availability (Ólafsson
1986). Spawning takes place in late spring (Ankar 1980), and the planktonic larvae settle six
to eight weeks later.
All the native deposit-feeding species are important as food for both demersal and pelagic fish
(Aneer 1975; Ehrenberg et al. 2005). They are also prey for three invertebrate predators: the
isopod Saduria entomon, the polychaete Harmothoe sarsi and the priapulid Halicryptus
spinulosus. In recent years, three species in the non-indigenous suspension- and depositfeeding polychaete genus Marenzelleria spp. have invaded the Baltic Sea (Olenin and
Leppäkoski 1999; Blank et al. 2008). Marenzelleria arctia is the dominant Marenzelleria
species in muddy sediment bottoms at somewhat larger depths, sometimes co-existing with
M. neglecta, while M. viridis is commonly found in shallow, sandy habitats (Blank et al.
2008). All species in this genus are probably facultative suspension-deposit-feeders and
14
burrow much deeper in the sediment than the native Baltic species (Dauer et al. 1981; Zettler
et al. 1995).
Meiofauna, defined as benthic animals with a body size between 40 and 1000 µm, are
omnivores and deposit-feeders. Generally, meiofauna have short generation times and often
continuous reproduction, but their modes of feeding is highly specific (Giere 1993). Due to
their high abundance (often over 106 individuals m-2 of sediment surface, corresponding to
about 1 g dw of biomass), they play important roles in the benthic food web and for
mineralization rates of organic matter (Goedkoop and Johnson 1996). In Baltic sediments, the
most important groups are nematodes (constituting about 50% of the total meiofaunal
abundance), followed by ostracods and harpacticoid copepods (Ankar and Elmgren 1976;
Ólafsson and Elmgren 1997).
Gulf of
Bothnia
Bothnian
Sea
Askö
Baltic proper
Figure 3. Map showing the Baltic Sea and its major sub-basins and the gradient in species richness of
common deposit-feeding macrofauna below the summer thermocline depth (from left: Monoporeia
affinis, Pontoporeia femorata, Macoma balthica and Marenzelleria spp.). Dashed lines indicate
addition of the invasive species.
15
EXPERIMENTAL APPROACH
In this thesis the effect of phytoplankton on the growth of benthic fauna and the influence of
the fauna on the fate of the phytodetritus have been studied in controlled laboratory
experiments, where we simulated settling spring or summer blooms in microcosms with
sediment, in which we had full control of the species assemblages. Fauna, sediment and
phytoplankton bloom material were collected from the Askö area in the north-western Baltic
proper and the experiments were carried out at the Askö Laboratory (Figure 3) in the
summers of 2005 and 2006 and in spring 2008.
Isotope tracers in food-web studies
Isotope tracer techniques provide powerful tools for analyses of energy and material flow
pathways and food web structures (Peterson 1999). Natural elements exist as both stable and
unstable (radioactive) isotopes, i.e. atoms with the same number of protons but differing in
the number of neutrons.
The radioactive carbon isotope 14C is commonly used to study breakdown and uptake of
settling organic matter (Lopez and Crenshaw 1982; Andersen and Kristensen 1992;
Goedkoop et al. 1997; Byrén et al. 2002). Radioactive isotopes disintegrate with time, but the
half-life of 14C is long (5570 years) and its specific activity low, making it suitable for
experimental work. When added in carbonate form, 14C can be assimilated by algae or
cyanobacteria during photosynthesis. By isotope labeling of phytoplankton (e.g. van de Bund
et al. 2001; Byrén et al. 2006) it is possible to follow the fate of the added material. Labeled
material taken up by animals and radioactivity in sediment can then be measured with a
scintillation counter. The basic principle of this technique is to dissolve the radioactive sample
in a liquid chemical medium capable of converting the kinetic energy of nuclear emissions
into light energy.
Stable isotopes
Nitrogen and carbon have two stable isotopes each, 14N and 15N, and 12C and 13C, respectively.
The heavy isotopes are less common than the lighter ones in biological material. In naturally
occurring carbon only ~1% is 13C and in natural nitrogen only ~0.4% is 15N. The small
difference in atomic mass between the isotopes can be measured with high accuracy by mass
spectrometry and the ratio (R) between the heavy and the light stable isotopes (15N:14N and
13
C :12C) in a sample is expressed as the deviation in ‰ from an international reference
standard. This deviation is denoted δ and defined by the equation (Peterson and Fry 1987):
δ (‰) =[(Rsample- Rstandard)/Rstandard] × 1000
The standards are VPDB (a limestone) for carbon, and atmospheric nitrogen gas for nitrogen.
Many natural processes affect the relative abundance of stable isotopes in predictable ways
(DeNiro and Epstein 1978). Therefore, natural isotopes are commonly used to determine diet
and origin of animals. The interpretation of data obtained from stable isotope analyses is
16
rather complex, since this technique relies on a set of assumptions. To allow more precise
estimates of the diet and the transfer of organic matter than possible by using stable isotopes
at natural abundance, the isotopic composition of phytoplankton can be modified as for
radiolabelling, e.g. by culturing them in medium where some or all C and N are replaced with
the heavy isotope (e.g. Moodley et al. 2002). To quantify the contribution of different food
sources with clearly different isotope values (e.g. sediment vs isotope enriched bloom
material) to a sample (animal or sediment), we used a simple linear 2-source mixing model
(Fry 2006).
Assessing growth and nutritional value to animals
Methods for determining growth rate often rely on repeated measurements of individuals,
which is time-consuming and difficult, especially in species that are sensitive to handling.
However, biochemical indicators that reflect growth are a promising alternative (Buckley et
al. 1999). The RNA:DNA ratio is a sensitive method for estimating the instantaneous rate of
somatic growth. It is based on the assumption that the amount of deoxyribonucleic acid
(DNA) is quasi-constant, while the amount of ribosomal ribonucleic acid (rRNA) changes in
proportion to protein synthesis, or growth. Several studies have found that RNA:DNA ratios
of e.g. zooplankton respond rapidly to changes in quantity and quality of food (Vrede et al.
2002; Wagner et al. 2001; Gorokhova 2003). RNA and DNA are quantified using a dye that
exhibits fluorescence when binding to nucleic acids. After a first reading, a nuclease, RNAse,
is added to the sample to break down RNA, leaving only DNA, which can be quantified after
a second reading. Hence, RNA content is the difference between the two detections.
The cyanotoxin nodularin was quantified in animals using liquid chromatography followed by
mass spectrometry (Karlsson et al. 2003). Samples were first purified by adding the extract of
the animal to a solid-phase extraction column of such properties that the compound of interest
(nodularin) is retained in the column. Thereafter nodularin is eluted with a solvent to which it
has a higher affinity for than the material in the column. The purified sample can then be
identified and quantified using coupled high pressure liquid chromatography-mass
spectrometry (HPLC-ESI-MS). The principle consists of ionizing chemical compounds to
generate charged molecules or molecule fragments which are measured and quantified by an
electron multiplicator using their mass-to-charge ratios.
17
RESULTS AND DISCUSSION
Importance of phytoplankton quality for benthic fauna
This subsection discusses the results of papers I-III in which different aspects of incorporation
and growth of deposit-feeders fed cyanobacteria were studied. Since there were no previous
studies on the effects of cyanobacteria on deposit-feeders, our first question was whether they
survived and fed on settled cyanobacterial bloom material (I). Thereafter we studied if they
accumulate toxins (II) and how animal growth after feeding on cyanobacteria compares to
growth on a spring bloom of diatoms (III).
Cyanobacteria as a food source
Due to their morphology, nutritional inadequacy and frequent toxic content, cyanobacteria are
generally considered a poor food for invertebrates (Holm 1983; DeMott and Müller-Navarra
1997; Engström et al. 2000). However, most studies so far have used pure laboratory cultures
of cyanobacteria fed to laboratory cultures of zooplankton in short term experiments (de
Bernardi and Giussani 1990). Studies using natural cyanobacterial bloom material have
shown less negative and sometimes even positive effects on pelagic organisms, e.g. by
constituting a supplemental food source, because they are associated with a rich microheterotrophic community (Engström-Öst et al. 2002). In support of this, the results of paper IIII demonstrate that settling natural cyanobacterial bloom material can be utilized as food by
deposit-feeders with no cost in mortality (see also Nascimento et al. 2008). Compared to
spring bloom material (van de Bund et al. 2001, Byrén et al. 2006), incorporation of both nontoxic and toxic species of cyanobacteria was, however, relatively low and did not result in
growth of amphipods (I). In paper II, where the supply of cyanobacteria was higher and
duration of the experiment longer, incorporation was accordingly higher, but still none of the
macrofaunal species increased significantly in biomass. Lack of growth can perhaps be
attributed to an energy demanding process of coping with cyanotoxins (i.e. nodularin), as has
been proposed for zooplankton and fish (Koslowski-Suzuki et al. 2003; Pääkkönen et al.
2008). All macrofaunal species tested accumulated nodularin (II), indicating that the fauna fed
directly on cyanobacteria, rather than on aged material, which had already been detoxified by
the bacterial community (Torunska et al. 2007; Mazur-Marzec et al. 2009). However, the
observed lack of significant growth may also be related to the poor nutritional quality of
cyanobacteria, rather than to their toxicity. Paper III showed that diatoms supported growth of
the meiobenthos but toxic cyanobacteria did not. Even though the cyanobacterial sample had
relatively high concentrations of aminoacids and proportions of polyunsaturated fatty acids,
the amount of bioavailable aminoacids and the proportion of the essential fatty acid
eicosapentaenoic acid, which is believed to determine efficiency in trophic transfer between
primary producers and consumers (Müller-Navarra et al. 2000), were much lower in
cyanobacteria than in diatoms from the spring bloom. In conclusion, settling blooms of
cyanobacteria are not directly harmful to the benthos, but are not a nutritionally fully adequate
food source.
18
Changes in phytoplankton dynamics affect benthic production?
In the Baltic Sea, the spring bloom of diatoms is considered the most important input of high
quality organic matter to the sub-thermocline soft-bottom community (e.g. Elmgren 1978;
Uitto and Sarvala 1991). After the spring bloom has settled to the bottom, the main benthic
growth period of the year ensues (Cederwall 1979; Lehtonen and Andersin 1998, Ólafsson
and Elmgren 1997), as shown experimentally for meiofauna in paper III. Also, while no
significant growth was recorded for any of the macrofaunal species in sediments with
cyanobacterial input, significant growth was recorded when they were fed diatoms (paper V).
Both studied amphipod species (M. affinis and P. femorata) time the release of their young to
coincide with the spring bloom (Sundelin and Eriksson 1998) and the bivalve M. balthica
invests in gonadal growth during this time (Ankar 1980). This suggest that time of the year
strongly influences the species-specific performance regarding incorporation and that the
cyanobacterial input may supply the soft-bottom community with a much needed energy
source at a time when the high quality spring bloom input to the sediment has been exhausted.
There is however still uncertainty concerning the quantity of the cyanobacteria that reaches
the benthos, and detailed studies on this topic are needed.
In recent years, the biomass of the spring bloom in the Baltic proper and Gulf of Finland has
decreased, while the summer bloom of cyanobacteria has increased (Wasmund et al. 1998;
Raateoja et al. 2005). These large scale changes have been related to hydrographic changes
and to eutrophication (Suikkanen et al. 2007). Lehtimäki et al. (1997) suggested that
especially N. spumigena may benefit from a future temperature increase in concert with
increasing phosphorus concentrations. Monitoring data (Swedish National Monitoring
Program) show a decrease of winter concentrations of dissolved inorganic nitrogen (N) since
the early 90s and a recent increase of dissolved inorganic phosphorus (P), resulting in a lower
N:P ratio, which favors cyanobacterial growth (Stal et al. 2003). Since native deposit-feeders
seem to rely on nutrients found mainly in the spring bloom input for growth (III), a shift in
phytoplankton composition towards dominance by cyanobacteria may affect benthic
productivity negatively. In contrast, the invasive polychaete M. arctia grew almost as rapidly
in sediments without diatoms (paper V) and fed on toxic cyanobacteria without cost in
mortality (pers. observation), suggesting that it may gain a competitive advantage over the
native species if the spring bloom input is reduced.
Cyanobacterial blooms have sometimes been described as part of a vicious circle (Vahtera et
al. 2007), since more P as a consequences of eutrophication enhances summer blooms, which
then increase the N content of the Baltic Sea through N fixation (Larsson et al. 2001).
Addition of N to the system further stimulates phytoplankton growth, with increased
sedimentation causing more anoxic, P-leaking sediments as a consequence. The fact that
increased cyanobacterial blooms not only enhance eutrophication but also increase
bioaccumulation of cyanotoxins (that are potentially harmful to humans) adds a further
dimension to the vicious circle (II). There are indications that trophic transfer of nodularin
might be more effective in the benthic than in the pelagic food chain, since higher
19
concentrations have been detected e.g. in flounders and blue mussels than in pelagic fish and
zooplankton (see Karjalainen et al. 2007). Nodularin is considered more toxic to vertebrates
than to invertebrates (Kiviranta et al. 1991), and fish exposed to nodularin, either directly or
by feeding on nodularin-containing prey, have shown evidence of oxidative stress and liver
damage (Persson et al. 2009; Vuorinen et al. 2009) as well as reduction in feeding activity
(Karjalainen et al. 2005). Even though feeding on cyanobacteria seems not to harm the
benthos, it may still lower their value as prey.
In conclusion, the cyanobacterial input may provide maintenance energy during a critical time
of the year, but is inferior to the spring bloom of diatoms in supporting growth of the benthic
fauna. Hence, increased cyanobacterial blooms can not fully compensate for reduced diatom
blooms. In addition, feeding on cyanobacteria could also result in a benthic fauna that is
harmful as food for fish due to bioaccumulation of toxins, with potential for transfer even to
humans.
Biodiversity effects on processing of phytoplankton bloom material
In this subsection I discuss the results of papers IV and V, where the amounts of added
phytoplankton taken up by fauna and remaining in the sediment were compared among
communities of benthic deposit-feeding macrofauna, differing in species composition and
richness. The studies were performed at different times of the year (summer and spring) and
used different types of phytoplankton (cyanobacteria and diatoms). Paper IV focused on the
species composition and richness of native species whereas paper V also included an invasive
species in the experimental design.
These studies benefit from their methodological approach. Direct measurements of
incorporation and burial and indirect calculations of mineralization losses have led to
improved understanding of benthic-pelagic coupling, since these three processes together
determine the fate of settled phytoplankton. An example of the links between the different
measured processes is that burial increases retention of phytodetritus in the sediment, which
supports continued incorporation in the longer term. Incorporation provides information on
species-specific contributions to multi-species treatments, a prerequisite for partitioning of a
diversity effect into diversity components (trait-independent complementarity, trait-dependent
complementarity and dominance; Fox 2005). Furthermore, the ability to relate the result to the
behaviour of the individual species and their distribution in the sediment allows a greater level
of insight into the mechanisms underlying the relationships between biodiversity and
ecosystem functioning than is typical of such studies.
Mechanisms behind biodiversity effects on measured processes
The surface deposit-feeders generally had high incorporation values (IV, V) while the subsurface feeder showed lower values but instead had stronger effects on burial (IV, V) and on
the oxidized layer (V) than the other species. Macoma balthica was the species that showed
the most contrasting effects in the two experiments, with low incorporation of cyanobacteria
20
but high incorporation of diatoms. This difference may either be related to differences in
feeding activity over the year or to a particular sensitivity to cyanobacteria as a food source
(Lehtonen et al. 2003). Of the studied species, Marenzelleria arctia differed from the native
species primarily through its ability for rapid growth, also from sediment without diatom
input.
The species-specific differences in performance resulted in species composition always being
significant for the outcomes of the studied processes. However, species richness had a
significant positive effect on incorporation of cyanobacterial N. In the experiment with
diatoms, only composition was significant for the corresponding treatments, but species
richness had a weak but significant positive effect on N incorporation and burial of N when
the M. arctia treatments were also included in the test. Hence, the addition of the invasive
species enhanced processing of bloom material and therefore both studies suggest that a
reduction in deposit-feeding species richness would decrease the effectiveness of benthic
processing of phytoplankton bloom material.
Reasons for the positive effects of species richness on incorporation and burial could be
differences among the species in feeding depth, resulting in niche differentiation. M. balthica
feeds mainly on the surface of the sediment and on suspended material, Monoporeia affinis in
the upper centimeter and Pontoporeia femorata deeper down. Accordingly, by comparing the
relative yield among component species within and among treatments, it was clear that
positive trait-independent complementarity was the main cause for over-yielding in both
studies. The dominance effect was small or even negative, in the latter case counteracting
positive complementarity components (paper V). Hence, weak net biodiversity effects could
result from contrasting effects of ecologically interesting mechanisms. The results from the
partitioning are strengthened by previous studies on the interactions among these species. The
amphipods M. affinis and P. femorata provide an especially interesting case, since both field
and lab studies show that they segregate by depth and feed on different resources when in
sympatry (Hill and Elmgren 1987; Byrén et al. 2006), providing a clear ecological
explanation to the observed complementarity (IV, V). In contrast, the community composed
of the two native surface-feeding species M. affinis and M. balthica, showed negative
complementarity in spring time (V), indicating competition over the diatom input.
Interestingly, these species seldom co-occur in high abundances on a local scale (Segerstråle
1973).
By partitioning the net diversity effects in paper V it was demonstrated that, on average,
communities including the invasive species showed larger complementarity than communities
composed of only native species. This comparison is however confounded by the fact that in
the substitutive design used, species richness inevitably increases when adding a new species.
Positive complementarity in communities including the invasive species still suggests
facilitation and low niche overlap among the species. According to invasion theory, ”empty
niches” are likely to occur in species-poor ecosystems, since the level of interspecific
21
competition is expected to be lower with fewer species (Elton 1958). However, incorporation
of bloom material only represents one specific component of niche dynamics. Utilization of
old organic matter also influences growth, as shown in paper V, where the sub-surface
feeding P. femorata and the invasive species M. arctia had almost as high biomass increase in
treatments without bloom input to the sediment. Successful invaders are often thought to
possess traits making them functionally different from the native species (Shea and Chesson
2002). The ability of M. arctia to grow rapidly from sediment without spring bloom input (V)
could be an example of such a trait, resulting in positive complementarity through resource
partitioning or, if directly translated into higher fitness and abundance, leading to competitive
suppression of competitors in a longer perspective (Byers 2000).
Long term changes in benthos: implications for ecosystem functioning
Long term monitoring data from both the Askö area (Figure 4) and other parts of the northern
Baltic proper (Perus and Bonsdorff 2004; Laine et al. 2007) show that over the last 20 years,
the bivalve M. balthica has increased in abundance and biomass while the two amphipods M.
affinis and P. femorata, have decreased. M. balthica is more tolerant of low oxygen
concentrations than the amphipods (Modig and Ólafsson 1998) and considering the largescale changes in benthic communities due to eutrophication, this shift in community
composition can be expected to have effects at the ecosystem level. Firstly, M. affinis has a
high per capita uptake and metabolism (Cederwall 1979; van de Bund et al. 2001, IV, V) and
constitutes an important trophic link to pelagic fish, such as the commercially important
herring (Aneer 1975). Secondly, the bioturbation activities of the sub-surface feeding
amphipod P. femorata proved to be especially important for retention of bloom material in the
sediment as a large proportion was buried deeper down in the sediment where mineralization
rates are slow (IV, V). Thirdly, the amphipods incorporated more C relative to N from the
bloom material, while the opposite is true for M. balthica (IV, V). These species-specific
differences in elemental requirements can have consequences for cycling of N. In paper IV,
the M. balthica monoculture showed increased mineralization of both C and N relative to
multi-species treatments, perhaps due to the observed high oxygen penetration depth in the
sediment in this treatment. Hence, increased abundance of M. balthica could result in more
rapid mineralization of bloom material, with less food supplied to sub-surface feeders and
lower resource utilization. A reduction of species richness would lead to lower food web
productivity in the long run, since the most species-rich community was also the most
efficient in both incorporation and retention of cyanobacterial material (IV). Rapid
mineralization in the presence of M. balthica is in accordance with a study in which this
species stimulated mineralization more than M. affinis (Karlson et al. 2005). Furthermore,
Viitasalo-Frösen et al. (2009) demonstrated that M. balthica (and M. cf. arctia) increased
fluxes of ammonium and phosphate out of the sediment while M. affinis had the opposite
effect. Such internal feed-backs on nutrient cycling as consequences of an altered benthic
community may accelerate eutrophication.
22
However, the results from paper V show that, given the right circumstances, M. balthica can
be highly efficient in incorporation of bloom organic matter. Not only did M. balthica show
as high per capita incorporation of diatom C and N as M. affinis, it even managed to grow
when fed sediment without spring-bloom input, whereas M. affinis did not. This demonstrates
that the type or quality of phytoplankton can affect the link between biodiversity and
ecosystem functioning.
Marenzelleria
Monoporeia affinis
Pontoporeia femorata
Macoma balthica
Abundance (individuals m-2)
3500
3000
2500
2000
1500
1000
500
19
71
19
73
19
75
19
77
19
79
19
81
19
83
19
85
19
87
19
89
19
91
19
93
19
95
19
97
19
99
20
01
20
03
20
05
20
07
0
Figure 4. Abundance of macrofaunal deposit-feeders in the Askö region from a 37-year time series
(Swedish National Marine Monitoring Program; Cederwall, pers comm.). Data are averages from 4
stations at 20-40 meters depth. See text for details.
Recent changes in benthic biodiversity: implications for ecosystem functioning
On a regional scale, the biodiversity of deposit-feeders in the Baltic Sea has increased in
recent years due to the invasion of the genus Marenzelleria spp. The first individuals were
found in the Askö area in 2002 but the abundance at the National Marine Environmental
Monitoring stations at 20-40 m depth remained low until 2006, after which it increased
considerably (H. Cederwall, Dept. Systems Ecology, SU, pers. comm.). The Marenzelleria
spp. invasion has in some areas been considered responsible for the decline of M. affinis
(Zettler et al. 2002). This seems unlikely in the Askö area since the abundance of M. affinis
has been decreasing here since the late 1970s (Figure 4). Still, Marenzelleria spp. abundances
can locally reach abundances of 30,000 individuals m-2 (Zettler et al. 2002; pers obs.) and
might therefore hinder a potential recovery of the M. affinis population.
The invasions of the Marenzelleria spp. in the Baltic ecosystem have so far not been studied
from a trophic perspective. This is complicated by the three Marenzelleria spp. potentially
differing in their resource requirements. M. viridis occurs primarily in shallow sandy bottoms
while M. arctia is dominant at larger depths in muddy bottoms, where it sometimes co-occurs
with M. neglecta (Blank et al. 2008). Several studies demonstrating competition for space or
23
resources (Neideman et al. 2002, Kotta and Ólafsson 2003) and studying the effects of
Marenzelleria on contaminant fate (Hedman et al. 2008) and nutrient fluxes (Norling et al.
2007) have used animals collected from a shallow sandy habitat dominated by M. viridis or
M. neglecta in microcosms intended to simulate deeper sediments, where the naturally
dominant Marenzelleria species is M. arctia (for exceptions of studies concerning nutrient
fluxes, see Hietanen et al. 2007 and Viitasalo-Frösen et al. 2009). The results of paper V show
that M. arctia did not have a negative effect on utilization of bloom material by the native
species. Eriksson-Wiklund et al. (2008) likewise found no evidence of negative interactions
between M. cf. arctia and M. affinis and concluded that the reason for a dramatic decrease in
M. affinis abundance in the Bothnian Bay during 1999-2003 was lower food quality (reduced
spring bloom and increased terrestrial runoff), rather than the invasion of M. arctia.
The ability of M. arctia to grow rapidly on sediment without spring bloom input has likely
been important for the successful invasion of this species, but can perhaps increase
competition over old organic matter with the native species during the part of the year when
spring-bloom material is not available. Ehrenberg (2008) found that the sand goby, the main
vertebrate predator on sub-thermocline bottoms in the Baltic proper (Ehrenberg et al. 2005),
feeds on Marenzelleria spp., and so the addition of this species could increase trophic transfer
of both sediment organic matter and freshly deposited bloom material. However, it is still
possible that Marenzelleria spp. escapes predation better than the native species or is a less
preferred food item, which would give the opposite result. Overall, the long-term net effect on
ecosystem functioning, by the addition of Marenzelleria spp. to the benthic community, is
difficult to evaluate. Bioturbation by Marenzelleria spp. can result in high P fluxes from the
sediment (Hietanen et al. 2007; Viitasalo-Frösen et al. 2009) and in release of sequestered
contaminants (Granberg et al. 2008). Increased P-fluxes could lower the N/P ratio, thus
favouring cyanobacterial blooms (Stal et al. 2003), and remobilization of toxins could
potentially slow the decreasing trends of contaminants recorded in Baltic biota (Bignert et al.
1998), both undesirable outcomes.
Generalizations of biodiversity results to other systems
These two studies (IV, V) are the first to test the effects of altered deposit-feeding biodiversity
on incorporation and burial of organic matter from phytoplankton blooms. However, in
addition to exploring relationships between biodiversity and ecosystem functioning in a
poorly studied system, our studies also provide links to food web ecology (through consumerresource interactions), evolutionary ecology (through the discussion on different life history
traits in respect to feeding activity and elemental requirements) and invasion biology (through
discussion on niche differentiation and competition). Bridging research fields is necessary for
deeper insights concerning relationships between biodiversity and ecosystem functioning
(Duffy et al. 2007; Schmitz et al. 2008; Woodward 2009).
The Baltic Sea, with its naturally low biodiversity and clear gradient in species richness,
proved to be a good system for testing hypotheses on the link between biodiversity and
24
ecosystem functioning (Elmgren and Hill 1997). The results can, in a unique way, be
extrapolated to field situations, since the species combinations used in experimental set-ups
represent real species combinations found in the field. Considering the large-scale changes in
benthic biodiversity observed in the study area, and the wider Baltic in general, inferences to
natural systems are both facilitated and strengthened. The results from this species-poor
system are likely widely applicable to other systems where detritivores drive nutrient and
energy cycling, like sediments of lakes and seas, and perhaps even terrestrial soils, and
especially to stressed environments with reduced species richness like sediments subject to
periodic hypoxia and anoxia. On the other hand, it is difficult to make extrapolations to very
species-rich systems, where each functional group is represented by many species. Since the
macrofaunal species studied in this thesis seemed to maximize different processes, they can
not be considered redundant, but must be considered to belong to different functional groups.
The redundancy hypothesis can therefore not be tested in this system. Raffaelli et al. (2003)
found that increased species richness of benthic macrofauna belonging to different functional
groups had a significant effect on nutrient fluxes from shallow sediments while increased
species richness within the same functional group had no effect.
Taken together, the results of papers IV and V tend to support the idiosyncratic hypothesis, as
also found in several other studies of detritivores in soil and soft bottom ecosystems (Mikola
and Setälä 1998; Emmerson et al. 2001; Hiddink et al. 2009), where the effect of species on
ecosystem processes are unpredictable and context-dependent. From a management point of
view it would imply that management should strive to retain all species, since we cannot
predict the outcome of ecosystem processes from the monoculture performances of the
relevant species and since species richness tends to improve ecosystem functioning.
25
CONCLUSIONS AND SUGGESTIONS FOR FUTURE RESEARCH
This thesis shows that both the type of phytoplankton bloom and the species composition and
richness of the benthic community affect the efficiency of resource utilization for settled
phytoplankton bloom material. The native Baltic deposit-feeding macrofauna seem to depend
largely on diatoms for growth even though the summer bloom of cyanobacteria can provide
some additional and perhaps crucial maintenance energy before the winter starvation.
Furthermore, it seems that the spring bloom input supports coexistence between native
species and the invasive polychaete Marenzelleria arctia, since the latter was not a strong
competitor for diatom bloom material. Therefore, reduced spring blooms might favour the
invader. The type of phytoplankton may also affect the nutritional value of the benthic fauna
for their predators - even though feeding on toxic cyanobacteria may have no immediate
negative effect on the benthic invertebrates, their vertebrate predators may be more sensitive.
The nutritional value of benthos as prey for higher trophic levels is an important future study
area.
The species-poor sediment of the Baltic Sea proved to be a good system for studying the link
between biodiversity and ecosystem functioning, and for elucidating the ecological
mechanisms behind the successful invasion of an exotic species, which is now an important
benthic element in many areas of the Baltic Sea. Species-rich communities had higher
incorporation of bloom material than expected, due to complementarity (niche differentiation
and interspecific facilitation) among these functionally different species. The effect of species
composition vs species richness on incorporation depended on the type of phytoplankton and
also season, perhaps due to differences in life-history strategies among the species. However,
incorporation of bloom material represents only one specific component of niche dynamics,
and animal growth depends also on e.g. competition for old organic matter in the sediment.
The invasive species showed resource partitioning with the native species when bloom input
was available, but competition can be expected to be more intense during the rest of the year.
Taken together, the data supports the idiosyncratic model of the relationship between
biodiversity and ecosystem functioning, meaning that species performances and hence
outcomes of ecosystem processes are context-dependent. Future studies should aim at
simultaneously manipulating quality of phytoplankton and species richness over several
trophic levels (i.e. including predators), to study how these factors jointly impact ecosystem
functioning (Cardinale et al. 2009). In conclusion, we have provided evidence that altered
benthic biodiversity leads to demonstrable changes in food web structure and ecosystem
functioning.
26
ACKNOWLEDGEMENTS
Studying deep sediment is a cold and dirty job… But also fascinating since it is a
transdisciplinary research field. I have had the pleasure to work with a number of skilled
people.
First and foremost, I would like to thank my supervisor Ragnar Elmgren, who has always
been ready to give constructive criticism, improve any text in an elegant way and given me a
lot of scientific and financial freedom!
My closest colleagues and good friends, Francisco Nascimento and Johan Näslund: thanks for
all the happy memories of planning and terminating experiments and discussions over small
and big things. Thanks Johan for all the last minute help!
Thanks also to my other coauthors for good collaboration: Elena Gorokhova for always being
“spot on” the weak points in a manuscript, Raimondas Motsuraitis for mastering the HPLCESI-MS and Sara Blomgren Rydén for weighing more tin cups than any other master student.
Askö laboratory staff and the Chemistry lab personnel are acknowledged for good
collaboration. I would like to thank Clare Bradshaw for reading several of my papers and
Jonas Gunnarsson for being so enthusiastic. Several happy assistants have helped sieving
endless amounts of sediment and picking animals: Erland Karlson, Elke Morgner, Hanna
Axemar and Ola Svensson.
Thanks also to all the PhD students at the department and other departments (including former
colleagues - you know who you are!) for all the fun during and after work. Thanks to Antonia
Sandman for help with figures and file formats and Lisa Almesjö for the Baltic Sea map.
Special thanks go to my former and present room mates Sigrid Ehrenberg, Francisco
Nascimento and Peter Sylwander for being patient with my messy desk(s).
I would also like to thank Satu Viitasalo and Sanna Suikkanen for good collaboration at
Tvärminne in 2007, even though that work did not make it into this thesis, and to my mother
Anna-Karin Borg-Karlson and the group at Ecologic Chemistry for help with nodularin
analyses.
Apart from pure science it has been great fun teaching with Mikael Tedengren at Askö and
Tjärnö, and it would of course not have been as fun without all the Bio-geo students!
Mamma och Pappa, tack för alla middagar och för all hjälp med huset!
Finally, I would like to thank Doug Jones for enthusiastically reading my manuscripts and the
summary, and for all the adventures we have had so far and for the ones to come!
The work within this thesis was funded by: Swedish Scientific Research Council and the
Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning
(Formas) (grants to Ragnar Elmgren), and to me from Stockholm Marine Research Center and
Lars Hiertas Minnesfond.
27
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