Download Trophic ecology of meiofauna: Francisco J.A. Nascimento

Trophic ecology of meiofauna:
Response to sedimentation of phytoplankton blooms in the Baltic Sea
Francisco J.A. Nascimento
Department of Systems Ecology
Stockholm University
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Doctoral thesis in Marine Ecology, 2010
Francisco Nascimento, [email protected]
Department of Systems Ecology
SE- 106 91Stockholm
Sweden
© Francisco Nascimento, Stockholm 2010
ISBN 978-91-7447-083-3
Printed by US-AB, Stockholm, Sweden
Cover artwork by Guro Stugu and Fredrik Pettersson
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ABSTRACT
Marine soft sediments are the second largest habitat on Earth. How animal
communities in this habitat are structured and their abundance and diversity regulated
is a central issue in marine ecology. Food is an important limiting factor for many
benthic populations, and since the great majority of aquatic soft bottoms are in waters
below the photic zone, settling organic matter from phytoplankton blooms is of vital
importance to them. The mineralization of this settled organic matter is a basic
benthic ecosystem process, and critical for sustaining aquatic primary production.
This thesis discusses the effects of settling phytoplankton blooms on benthic
meiofaunal populations in the Baltic Sea and how biotic interactions between
meiofauna, macrofauna and microbes affect the fate of settled organic matter.
Eutrophication in the Baltic Sea has altered phytoplankton community dynamics and
thus the quantity and quality of settling of organic matter reaching the benthos, with
indications that toxin-producing cyanobacterial blooms may now reach the benthos in
greater quantity than previously. Paper I found that meiofauna can feed on settled
cyanobacteria at rates similar to what other studies have found for diatoms, yet suffer
no apparent increase in mortality. However, growth of meiofauna is significantly
slower on a diet of cyanobacteria than when fed spring bloom diatoms, indicating that
the studied cyanobacteria are nutritionally poor and, even if assimilated, do not much
improve growth (Paper II). Still, cyanobacteria may provide critical maintenance
energy for some meiofaunal populations during periods of the year when high quality
food is unavailable.
Paper III highlights how biotic interactions between macrofauna and meiofauna can
determine how settled phytoplankton blooms are processed by meiofauna. We found
that the presence of macrofauna reduces the access of meiofauna to settled organic
matter from phytoplankton, presumably through interference competition. Spatial
niche differentiation between macrofauna species is likely to reduce the sediment
volume in which meiofauna can feed undisturbed by larger competitors, suggesting
that interference increases when several macrofauna species are present.
We also found that meiofaunal populations influence the provision of ecosystem
services by benthic microbes. Although the direct meiofaunal contribution to benthic
mineralization and contaminant degradation can be considered small, our results
indicate that microbial activity and species composition is top-down controlled by
meiofauna. Paper IV shows that when meiofauna is abundant, mineralization of
organic matter is positively affected, presumably through facilitation mechanisms. In
contrast, paper V reports that degradation of the contaminant naphtalene decreases
significantly at high meiofauna abundance, due to higher grazing pressure on the
naphthalene-degrading bacteria.
In conclusion, this thesis shows that type and quality of organic matter available, as
well as competition from macrofauna, affect how meiofauna grow and incorporate
nutrients. Furthermore we found meiofauna to be an important functional component
of the benthic ecosystem, with marked effects on ecosystem processes such as
nutrient regeneration and contaminant degradation.
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1. LIST OF PAPERS 5 2. INTRODUCTION 6 2.1. B ENTHIC PELAGIC COUPLING 2.2. B ENTHIC INVERTEBRATES AND M EIOFAUNA 2.3. E UTROPHICATION AND EFFECTS ON SETTLING ORGANIC MATTER 2.4. Q UALITY OF ORGANIC MATTER AND BENTHIC GROWTH 2.5. C OMPETITION IN BENTHOS AND ACCESS TO ORGANIC MATTER 2.6. B ENTHIC ECOSYSTEM PROCESSES 7 8 10 11 12 13 3. EXPERIMENTAL APPROACH 14 3.1. S TUDY SYSTEM : THE B ALTIC S EA 3.2. I SOTOPE TRACERS IN FOOD - WEB STUDIES 3.3. B IOCHEMICAL TOOLS 15 15 16 4. RESULTS AND DISCUSSION 16 4.1 C HANGING PHYTOPLANKTON COMMUNITY DYNAMICS AND EFFECTS ON
MEIOFAUNAL POPULATIONS 17 4.2. I NTERSPECIFIC COMPETITION IN SOFT SEDIMENTS 18 4.3 H OW ARE BENTHIC ECOSYSTEM PROCESSES AFFECTED BY MEIOFAUNA ?
19 5. CONCLUDING REMARKS AND FUTURE STUDIES 20 6. ACKNOWLEDGMENTS 21 7. REFERENCES 24 4
1. LIST OF PAPERS
This thesis is based on the following five papers, referred to in the text by their
Roman numerals.
I
Nascimento FJA., Karlson AML., Elmgren R. (2008) Settling blooms of
filamentous cyanobacteria as food for meiofauna assemblages. Limnology &
Oceanography 53(6): 2636-2643
II
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: 138146.
III
Nascimento FJA., Karlson AML., Näslund J., Elmgren R. Diversity of larger
consumers enhances interference competition effects on smaller competitors.
(Submitted manuscript).
IV
Nascimento FJA, Näslund J, Elmgren R. Meiofauna enhances organic matter
mineralization in soft sediment ecosystems (Manuscript).
V
Näslund J., Nascimento FJA., Gunnarsson JS. (in press) Meiofauna reduces
bacterial mineralization of naphthalene in marine sediment. ISME Journal
My contributions to the papers: (I) –Major part in experimental design and execution,
all meiofauna sorting analyses and data processing, major part in writing. (II) – Major
part in experimental design and execution, all meiofauna sorting, preparation of
samples for RNA/DNA quantification, data processing, major part in writing. (III) –
Major part in experimental design and execution, all meiofauna sorting and
preparation of samples for stable isotope analysis, data processing, writing (IV) –
Major part in experimental design and execution, all meiofauna sorting, analyses and
data processing, major part in writing. (V) – Major part in experimental design and
execution, meiofauna community analysis, participated in data processing,
contributed in writing.
Additional papers by the author of this thesis:
Boyra, A., Nascimento, F.J.A., Tuya, F., Sanchez-Jerez, P., Haroun, R.J., 2004.
Impact of sea-cage fish farms on intertidal macrobenthic assemblages. Journal of the
Marine Biological Association of the U.K. 84, 665-668.
Karlson AML, Nascimento FJA, Elmgren R (2008). Incorporation and burial of
carbon from settling cyanobacterial blooms by deposit-feeding macrofauna.
Limnology & Oceanography 53(6): 2754-2758.
Karlson AML, Nascimento FJA, Näslund J, Elmgren R. In press Higher diversity of
deposit-feeding macrofauna enhances phytodetritus processing. Ecology
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2. INTRODUCTION
One of the fundamental goals of ecology is to understand the processes that determine
the abundance and distribution of species, and hence the composition of biological
communities. As soft bottoms cover 70% of our planet’s surface, regulation of animal
communities in these habitats is a central question for marine ecology. Due to the
complexity of aquatic soft bottoms, the usual generalisations about how communities
are structured are hard to use for benthic assemblages (Wilson 1990). Soft bottoms
have unique characteristics, such as their three-dimensional spatial structure and the
ability of animals to rapidly rework the sediment and change the physical and
chemical conditions of their habitats (Meysman et al. 2006). The community structure
of benthic invertebrates is determined by several interacting factors, one of the most
important being how individuals acquire nutrients. Most of ocean bottoms are
situated below the photic zone, which mean that animals living in these sediments
have to depend on inputs of allochthonous organic matter for food (Graf 1989). A
large part of the organic matter that reaches ocean bottoms comes from settling
phytoplankton blooms. How benthic animals use this vital limiting resource is,
therefore, a determining factor for benthic communities (Graf 1992). This
phytoplankton material is usually either remineralized back to the water column via
microbial decomposition and metazoan grazing and respiration, or permanently
buried in the sediments (Sellner 1997). Thus, animals living in soft sediments have an
important role in global biogeochemical cycles, by influencing how much carbon is
sequestered into the geosphere (Van Cappellen 2003) and how remineralized
nutrients are returned to the water-column, to drive primary production (Webb and
Montagna 1993).
The aim of this thesis was to examine the response of Baltic soft-bottom meiofauna to
phytoplankton sedimentation and the trophic interactions with the other two
components of the benthic system, macrofauna and prokaryotes, mediate the fate of
settled blooms.
Baltic plankton production is strongly pulsed, with a succession of phytoplankton
blooms of different species composition (Andersson et al. 1996; Höglander et al.
2004). The spring bloom has been considered the most important bloom event,
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providing most of the annual new production and input to the benthos (Elmgren 1978;
Lignell et al. 1993). Cyanobacterial summer blooms are considered to have increased
in frequency and biomass in recent decades, likely as a consequence of eutrophication
(Finni et al. 2001; Poutanen and Nikkilä 2001)
The first part of this thesis deals with how cyanobacterial organic matter is processed
by meiofauna in the benthic food web and how it affects the survival and growth of
meiofauna assemblages in the Baltic Sea (Paper I and II). In the second part I studied
how biological interactions such as competition, grazing and facilitation between
meiofauna, macrofauna and microbial communities determine the fate of organic
matter in Baltic Sea soft sediments (Paper III and IV and V).
Fig.1 – Simplified illustration of benthic-pelagic coupling with focus on the processes studied
in this thesis.
2.1. Benthic pelagic coupling
Benthic communities in the aphotic zone are food limited for considerable periods of
the year (Rudnick 1989). Settling organic matter therefore greatly affects the
metabolism and population dynamics of benthic communities (Elmgren 1978; Graf
1992; Gullberg et al. 1997) and many species in benthic assemblages exhibit life-
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history characteristics adapted to seasonal inputs of settling organic matter (Boon
1998; Ólafsson and Elmgren 1997).
The sheer amount of organic matter derived from phytoplankton blooms that reaches
aquatic sediments every year makes them a globally important reservoir of organic
matter. The mineralization of this organic matter in marine sediments is driven mainly
by microbial processes with bacteria as the primary mediators (Gage and Tyler 1991;
Marinelli and Waldbusser 2005). However, meio- and macrofauna have been shown
to influence mineralization, both directly and indirectly. The activity of depositfeeding benthic fauna facilitates the access of the bacterial community to the organic
matter present in the sediment, by enhancing the vertical and horizontal mixing of the
sediment (Boon 1998; Diaz et al. 1994; Osinga et al. 1997; Vanduyl and Kop 1994;
Webb and Montagna 1993; Yingst and Rhoads 1980). In addition, other ecological
processes connected to benthic fauna activity, like bioturbation control important
environmental parameters that promote mineralization of organic matter in sediments,
such as exchange of nutrients, oxygen and other metabolites between the sediment
and the overlying water (Aller and Aller 1992; Boon 1998; Meysman et al. 2006). All
these processes help stimulate bacterial metabolism and organic matter degradation.
In addition, bioturbation may bury a significant fraction of settled phytoplankton
blooms into deeper sediment layers, where rates of decomposition are much slower
(Andersen 1996; Blair et al. 1996; Kristensen et al. 1995; van de Bund et al. 2001).
Such buried phytodetritus have the potential to feed soft bottom communities during
the many months when fresh organic matter is not available (Josefson and Hansen
2003; Rudnick and Oviatt 1986). If not used, this buried organic matter will
eventually be permanently sequestered, and removed from the biosphere, with impact
on the global carbon cycle.
2.2. B enthic invertebrates and Meiofauna Benthic invertebrates have traditionally been grouped by size into macro- and
meiofauna (Schwinghamer 1981; Warwick 1984). The size boundaries of macro- and
meiofauna are based on the methodology used in benthic studies, and correspond to
the size mesh of the sieves used during sorting (Warwick et al. 2006). As a result,
organisms retained on 0.5 or 1 mm mesh are classified as macrofauna, and those
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passing through this mesh, but retained on a 40 µm mesh, as meiofauna (Giere 2009).
As the focus of this thesis is on the trophic ecology of Baltic meiofauna, we followed
the recommendations for meiobenthic studies in the Baltic Sea (Elmgren and
Radziejewska 1989) and used 1000 and 40 µm mesh as the upper and lower limit for
meiofauna.
Fig. 2- Illustration of the heads and bucal cavity of some of the nematode taxa studied in
Paper I a) Paracanthoncus sp. b) Axonulaimus spinosus. c) Desmolaimus sp. d) Sabatiera
pulchra
Meiobenthic metazoans differ from macrofauna not only in size but also in a number
of biological characteristics (Warwick 1984), such as having direct benthic
development with adult dispersion, and often short generation times and continuous
reproductive activity. Regarding feeding adaptations they are motile organisms
seeking food particles in discriminating manner (Giere 2009). They inhabit a wide
variety of aquatic habitats, both freshwater and marine, from the surface to the
greatest depths and are found in all types of sediments (Coull 1988). Meiofauna are
more abundant and species-rich than macrofauna and include phylogenetic
representatives from most animal phyla; 22 of the 33 metazoan phyla have at least
one meiobenthic taxa (Coull 1999). On average one can expect to find numbers in the
order of 106 ind. m-2 of sediment surface and a standing stock of dry weight biomass
of 0.75-2 g m-2 in water above 100 meters depth (Coull 1988; Coull and Bell 1979;
Giere 2009). In soft sediments, nematodes (Fig. 2) are generally the most abundant
group, encompassing 60-90% of the total meiofauna abundance, with harpaticoid
copepods (Fig.3) usually the second most abundant group, at 10-40% (Coull 1999). In
the Baltic Sea the salinity and the temperature gradients are limiting factors for many
meiofauna species, leading to a lower species diversity than in fully marine or
freshwater systems (Elmgren 1978; Elmgren 1984; Rumohr 1996). In 1991, only 67
species had been reported from sediments below the photic zone in the inner Baltic
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proper (Ólafsson and Elmgren 1991). As is the case globally, meiofaunal assemblages
in the Baltic are usually dominated by nematodes, with more than 50% of the total
meiofauna abundance. Other common groups are harpacticoid copepods and
ostracods (Fig. 3), with the latter constituting the major part of meiofauna biomass in
some areas of the Baltic Sea (Ólafsson and Elmgren 1997). Due to its low number of
species and trophic links, the Baltic Sea has been considered particularly suitable for
studies of food webs and ecological couplings (Elmgren and Hill 1997).
2.3. Eutrophication and effects on settling organic matter
Human activities have profoundly changed the delivery of inorganic nutrients to
aquatic ecosystems (Galloway et al. 2003) and eutrophication is today acknowledged
as one of the main environmental problems affecting coastal areas (Rabalais et al.
2002). Today approximately 85 million people live in the Baltic drainage area, with
considerable impact on the quantities of inorganic nutrients released to the Baltic
ecosystem. The most striking ecological effect of excess inputs of nitrogen and
phosphorus to aquatic ecosystems is the stimulation of algal growth and consequent
degradation of water quality (Rabalais et al. 2002). In the Baltic Sea, the
anthropogenic input of nitrogen and phosphorous (Larsson et al. 1985), primary
production and resulting sedimentation of organic matter has increased markedly in
the last half-century (Jonsson and Carman 1994). Furthermore, the phytoplankton
bloom dynamics have changed in recent years, with indications that nitrogen-fixing
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and potentially toxic cyanobacterial blooms (Fig. 4) have increased in size and
frequency (Finni et al. 2001). Initially, it was thought that these cyanobacterial
blooms were almost entirely decomposed and mineralized by bacteria and flagellates
in the water column, causing little sedimentation of organic matter (Hoppe 1981;
Kononen et al. 1992; Sellner 1997). However, a number of studies provide indications
that the sedimentation caused by these cyanobacterial blooms and consequent organic
input to Baltic Sea sediments may be larger than previously believed (Bianchi et al.
2000; Bianchi et al. 2002; Gustafsson et al. 2004; Heiskanen 1998). The effects of the
sedimentation of these blooms on benthic organism are still largely unknown.
Regarding the meiofauna, ostracods can utilize newly settled cyanobacterial
Aphanizomenon sp. blooms, (Limén and Ólafsson 2002), but there is still a lack of
understanding of how and to what extent these organic matter inputs are utilized as
food by meiofauna. Additionally, there is little information on how toxins produced
by cyanobacteria can influence the meiofauna after ingestion. Paper I attempts to
contribute to clarify these issues.
Fig. 4- Summer bloom of the diazotrophic, nitrogen-fixing Nodularia spumigena, in the
Baltic Sea proper.
2.4. Quality of organic matter and benthic growth
How primary consumers use nutrients is related to both quantity and quality of the
food consumed. A number of studies have shown that secondary production can be
largely determined by food quality (Gulati and DeMott 1997; Vargas et al. 2006;
Vrede et al. 2002), with animal growth rates decreasing when the food has too low
concentrations of essential nutrients (Boersma and Kreutzer 2002)
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The low quantity of limiting nutrients, such as organic nitrogen, available in
sediments below the photic zone is a difficult challenge for deposit-feeding animals.
As a result, food quality can be an important structuring factor for communities of
benthic invertebrates. A number of biological parameters such as meiofaunal
community composition and abundance (Ólafsson and Elmgren 1997), macrofaunal
growth (Goedkoop et al. 2007), feeding preferences (Johnson 1987) and lipid contents
(Gardner et al. 1985; Richoux et al. 2004) are influenced by the quantity and
nutritional quality of settling phytoplankton and phytodetritus.
The quality of the OM that reaches aphotic sediments depends largely on seasonal
variations in phytoplankton production and community composition. In the Baltic
Sea, the spring bloom, which is generally dominated by diatoms, has been considered
the most important organic matter input to the benthos, providing the largest part of
the annual new production of both macro –and meiofauna (Lehtonen and Andersin
1998; Ólafsson and Elmgren 1997), likely due to their high content of lipids and polyunsaturated fatty acids (Ahlgren et al. 1992). As mentioned previously, blooms of
nitrogen-fixing bacteria now often dominate the summer phytoplankton community in
much of the Baltic Sea. Cyanobacteria are often seen as unsuitable food for aquatic
invertebrates due to a morphology that restricts ingestion, as well as their toxicity and
nutritional inadequacy (DeMott and Moxter 1991; Engström-Öst et al. 2002). After
finding in Paper I that meiofauna could utilize settled blooms of N. spumigena and
Aphanizomenon sp as food, it was important to asses the quality of freshly settled
cyanobacteria as food for the benthos, when compared to the spring bloom. Paper II
provides relevant information on this subject.
2.5. Competition in benthos and access to organic matter
Most habitats have a limited supply of food and/or space and therefore competition
between species for these resources is likely to be an important structuring factor of
populations (Wilson 1990). In this thesis we use the definition of interspecific
competition in Begon et al. (1990) that states that interspecific competition occurs
when “individuals of one species suffer a reduction in fecundity, survivorship or
growth as a result of resource exploitation or interference by individuals of another
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species”. Competition between species can occur through exploitative competition,
where negative interactions arise from the removal of a shared resource, or through
interference competition, where one species reduces the capacity of other species to
utilize a resource through behavioral mechanisms (Amarasekare 2002; Begon et al.
1990). Of these two, interference competition has received less attention even though
interference competition is likely to have strong impacts on evolution and community
structure of marine animals (Branch 1984 ).
The larger size of macrofaunal species when compared to meiofauna gives
macrofauna the potential to physically modulate several factors that structure
meiofaunal populations (Austen and Widdicombe 1998; Austen et al. 1998;
Schratzberger and Warwick 1999), including access to limiting resources such as
freshly deposited organic matter (Modig et al. 2000; Ólafsson et al. 2005). Therefore,
how interspecific competition from macrofauna regulates the use of fresh organic
matter by meiofaunal deposit-feeders is important for understanding the patterns of
coexistence between these two faunal groups in benthic ecosystems. This is the focus
of Paper III.
2.6. Benthic ecosystem processes
Benthic ecosystems provide several vital ecological services, including the production
of seafood and maintenance of life-supporting processes such as storage and cycling
of materials, nutrients, and degradation of pollutants (Snelgrove 1999). As
anthropogenic activities have altered benthic habitats, anoxic bottoms have become
more widespread globally, sometimes with severe consequences for benthic
biodiversity, abundance and species distributions (Diaz and Rosenberg 2008). Since
the loss of species may hamper certain ecosystem processes, understanding the
sources and mechanisms of variability in ecosystem functioning, and the conditions
under which different species can influence ecosystem processes is a vital focus of
ecological research (Solan et al. 2004).
Some ecosystems processes in benthic marine habitats, such as organic matter
mineralization and biodegradation of anthropogenic contaminants are driven mainly
by the action of prokaryotes (Gage and Tyler 1991; Marinelli and Waldbusser 2005).
However, biological interactions such as facilitation and predation between these
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microorganisms and benthic animals have the potential to play an important role in
these ecosystem processes. Interactions between infauna and the microbial
community in soft sediments are complex. Animals can increase sediment fluxes of
solutes and oxygen and remove toxic metabolites from sediments stimulating
microbial activity (Kristensen and Mikkelsen 2003). In addition, the activity of
infauna can also increase prokaryote metabolism by the disaggregation of particles,
which facilitates microbial access to organic matter (Rice 1986), and through grazing
or gardening that keeps bacterial populations growing at exponential growth rates
(Kemp 1987). On the other hand, the feeding activities of benthic fauna can compete
directly with the microbial community by removing organic matter otherwise
available for decomposition (Kristensen and Mikkelsen 2003; Tenore et al. 1982).
Therefore infauna has the potential to either stimulate or compete with microbial
communities. While interactions between macrofauna and microbial communities in
marine sediments are relatively well studied (Heilskov and Holmer 2001; Herman et
al. 1999; Holmer et al. 1997; Josefson et al. 2002; Kristensen et al. 1992; Kristensen
and Mikkelsen 2003), how meiofauna interacts with the microbial component of the
benthic ecosystem is still poorly understood, despite meiofauna being by far the most
abundant and diverse metazoan group in most benthic habitats. Several studies have,
however, provided evidence that meiofauna can stimulate microbial activity (Findlay
and Tenore 1982; Gerlach 1978; Rieper 1978; Rysgaard et al. 2000; Tenore et al.
1977; Tietjen 1980). Papers IV and V focus on these questions and study the effects
of meiofauna on organic matter mineralization and on biodegradation of an
anthropogenic pollutant.
3. EXPERIMENTAL APPROACH
In this thesis I studied the effect of settling phytoplankton blooms on Baltic
meiofauna and how benthic fauna influences the fate of the phytodetritus. This was
done through a series of controlled experimental studies that used isotopes as tracers
to follow the fate of the added organic matter.
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3.1. Study system: the Baltic Sea
The Baltic Sea is one of the largest brackish water bodies in the world and presents a
number of unique characteristics. Perhaps the most important one is the steady
salinity gradient from North to South, with salinity as high as 15 ppt in the
Southwestern Baltic Sea and as low as 3 ppt in the Northern Baltic Sea. A salinity
stratification is also present vertically, since the denser water that flows in from the
North Sea mixes only partially with the lower salinity water already in the Baltic Sea,
and therefore accumulates in deeper areas (Reid and Orlova 2002). Thus, a halocline
is formed, usually at a depth of 50 to 70 m (Melvasalo et al. 1981), separating the
upper layer from the weakly stratified deep water. This salinity gradient is paralleled
by a temperature gradient. Temperature affects layering during the summer when a
less dense, typically 10-20m thick, warm layer forms on the surface. This thermocline
divides low salinity waters into two layers: a well mixed surface layer down to a
depth of 10–25 m, and a deeper, colder layer extending down to the sea-bed or to the
halocline (Weaver 2003). These gradients in salinity and temperature restrict the
distribution of many species in the Baltic Sea, leading to a biological community with
unique ecological characteristics, with a mixture of marine and freshwater species
able to tolerate brackish conditions and true brackish water-adapted species (Elmgren
and Hill, 1997).
3.2. Isotope tracers in food-web studies
Isotopes are atoms of the same element that have equal numbers of protons but differ
in their number of neutrons in the nucleus. The difference between the various
isotopes in the number of neutrons of an element means that they have the same
charge but different masses (Jardine et al. 2003; Kendall et al. 1995). Isotopes can be
either, stable and non-stable. When the nuclei of the isotope does not decay to other
isotopes, but may themselves be produced by the decay of radioactive isotopes, the
isotope is classified as stable (Schimel 1993).
Isotopes are commonly used as natural tracers in ecological studies (Fry 2006), both
at the single organism level and at the ecosystem level, to trace food webs and
biogeochemical cycles. With the advantages of simple and straightforward collection
techniques and relatively inexpensive analysis costs (eg Michener and Schell 1994),
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isotope tracing is a powerful technique for looking at the processes, connections and
energy flows in aquatic systems (Lajtha and Michener 1994).
3.3. Biochemical tools
Biochemical indicators, such as nucleic acid indices, have been used with some
success as an alternative to the classical methods of evaluating growth rates. One of
the most widely used indices in marine ecology is the RNA:DNA ratio. This index is
based on the assumption that the quantity of deoxyribonucleic acid (DNA) in a
somatic cell is approximately constant, while the amount of ribosomal ribonucleic
acid (RNA), which associated with protein synthesis, is affected by the nutritional
state of the organism (Bremer and Dennis 1996). A number of studies have found
nucleic acid indices to respond to the quantity and quality of available food
(Gorokhova 2003; Wagner et al. 2001), demonstrating that this ratio can be used as a
proxy for assessing individual growth rate and nutritional status of individuals
(Menge 2000; Norkko et al. 2005).
4. RESULTS AND DISCUSSION
How nutrients are incorporated in biological communities play an important role in
regulating community structure and ecological interactions between organisms. In this
thesis I focused on a number of the factors that affect how carbon and nitrogen from
settling phytoplankton blooms are acquired by meiofauna and how meiofauna nutrient
incorporation affects and is affected by the other members of the benthic community,
macrofauna and prokaryotes. Papers I and II study the effects of cyanobacteria, an
increasingly important phytoplankton group in the Baltic Sea, on meiofauna carbon
incorporation and growth. Paper III looks on how competition by macrofauna
regulates meiofauna incorporation of nitrogen and carbon from a settling
phytoplankton bloom, while Paper IV and V focus on how the trophic interaction
between meio- and microfauna determine ecosystem processes performed by benthic
microorganisms.
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4.1 Changing phytoplankton community dynamics and effects
on meiofaunal populations
Organic matter type and quality is especially important for benthic communities
living below the photic zone, which are generally considered to be almost entirely
dependent on sedimenting allochthonous organic matter, mainly from the pelagic
zone (Goedkoop and Johnson 1996; Graf 1992). In the Baltic Sea, the spring bloom,
which is generally dominated by diatoms, has been considered to provide the most
important annual input of organic matter to the benthos (Graf 1992; Ólafsson and
Elmgren 1997). However, the biomass of the spring bloom has been decreasing in
recent years in certain parts of the Baltic Sea (Raateoja et al. 2005; Wasmund et al.
1998), with summer blooms of diazotrophic, toxin-producing cyanobacteria
increasing in intensity and frequency, with possible consequences for the benthic
community. The results of Paper I show that a number of meiofaunal species can
incorporate freshly deposited carbon from cyanobacterial blooms without increased
mortality. Furthermore, we found that some meiofauna groups assimilate carbon
from settling cyanobacterial blooms in considerable quantities. Comparing the results
of Paper I with those of Ólafsson et al. (1999) that studied meiofaunal incorporation
of carbon from a diatom bloom, we find that meiofauna taxa that assimilated carbon
from diatoms showed similar uptake of carbon as from cyanobacteria in our
experiment.
The findings of Paper I suggest that cyanobacteria can be an important food source
for benthic animals. The results in paper II show that meiofauna feeding on
cyanobacteria exhibited comparatively low growth, when compared to meiofauna that
were fed diatoms. This trend was consistent for all species tested in Paper II. The low
meiofaunal growth found in sediments with added cyanobacteria agrees with other
studies that found cyanobacteria to be of low nutritional value for both planktonic
crustaceans (Engström et al. 2000; Engström-Öst et al. 2002; Koski et al. 2002) and
benthic species (Korpinen et al. 2006; Svensen et al. 2005). Paper II found
cyanobacteria to be relatively poor in available aminoacids and polyunsaturated fatty
acids, suggesting that the low growth of meiofauna that fed on cyanobacteria was due
to their poor nutritional quality. In addition, Fewer et al. (2009) recently reported that
N. spumigena produces a cocktail of enzyme inhibitors, including spumigins, that
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have the potential to hinder the growth of crustacean grazers and may explain in part
the ecological success of this cyanobacterium in brackish water bodies worldwide.
Nevertheless, several experimental studies have shown that aquatic crustaceans are
able to survive and grow on a diet of Baltic cyanobacteria (Engström et al. 2000;
Koski et al. 2002). It is possible that the settling of summer blooms of cyanobacteria
provide these sediments with a much-needed food source at a critical time, when the
availability of fresh organic matter is low, after the spring bloom input to the
sediments has been exhausted. Although poor in unsaturated fatty acids they may
contain other elements that are important for the diet of grazers (Ahlgren et al.
1992).Thus, at least for animals with relatively short life cycles and high energy
requirements, such as harpacticoid copepods and to a lower degree the ostracod C.
neglecta, organic matter from cyanobacteria seems to be a useful summer food as
Paper I demonstrates. Nevertheless, Paper II indicates that meiofaunal growth seems
to be critically coupled spring bloom sedimentation, which is supported by the
observation that peaks of abundances of meiofauna in the Baltic Sea are related to the
input of detritus from the spring bloom (Ólafsson and Elmgren 1997).
4.2. Interspecific competition in soft sediments
Paper III found that the rate of incorporation of fresh organic matter by meiofauna
was lower in the presence of macrofauna, presumably because of interference
competition. In fact, the incorporation of labelled carbon and nitrogen was influenced
by both species identity of macrofauna, and the number of macrofauna species present
in the treatment, with meiofauna uptake being lowest in the treatment with all three
native deposit-feeding macrofaunal species (Monoporeia affinis, Macoma balthica
and Pontoporeia femorata). This increased interference at higher macrofaunal species
richness is probably related to the different bioturbation activities of the three
macrofaunal species hindering ostracod feeding on freshly deposited nitrogen and
carbon in complementary ways. The amphipods M. affinis and P. femorata, for
example, demonstrate spatial niche segregation with P. femorata feeding at deeper
layers of the sediment when in sympatry with M. affinis (Byrén et al. 2006; Hill and
Elmgren 1987). Through this spatial segregation macrofauna reduces the sediment
volume in which meiofauna can avoid the disturbance caused by macrofaunal
18
activity. The addition of the sediment reworking activities of M. balthica to the
disturbance caused by the amphipods will further increase the physical disruption of
the sediment and explain why the lowest incorporation of labelled nitrogen and
carbon by meiofauna is found at the highest macrofauna diversity. The results in
Paper III suggest that macrofaunal interference can force meiofauna to reduce their
foraging activity when faced with high frequency of amphipod and bivalve
disturbance both at and below the surface. The more time meiofauna individuals
spend on avoiding contact with macrofauna, the less time it will have available for
feeding, thus, reducing the access of meiofauna to freshly deposited organic matter.
This interaction could play an important role in soft sediment community dynamics.
A consistent pattern in benthic ecosystems is the faster decrease with water depth of
abundance and biomass of macrofaunal species, when compared to meiofauna (Rex et
al. 2006; Thiel 1975). This transition to a meiofauna-dominated system is related to a
number of factors including to lower food availability (Rex et al. 2006; Thiel 1975).
Such a meiofauna-dominated, low energy ecosystem is also seen in the northern
Baltic Sea where meiofaunal biomass exceeds that of macrofauna in the Bothnian Bay
(Elmgren et al. 1984). As meiofauna in general have lower energy requirements and
higher feeding efficiency than macrofauna (Elmgren 1978; Thiel 1975; Warwick
1984), their biomass and abundance decreases at a slower rate with depth, as they are
less affected by the low food availability. Our results suggest that meiofauna also
benefit from the release from interspecific competition by macrofauna in such low
energy ecosystems. With lower abundance and diversity of macrofauna, meiofauna
will have better access to the food available, and this will partly counterbalance the
lower food availability in deeper ecosystems.
4.3 How are benthic ecosystem processes affected by
meiofauna?
Papers IV and V clearly show that meiofauna are important for ecosystem processes
in benthic systems. Through interactions with the microbial community meiofauna
have an impact on the mineralization of phytoplankton material, as well as on the
degradation of an anthropogenic pollutant. The direction of this impact was, however,
different for the two studied processes. Paper IV shows that meiofauna grazing
19
pressure had a clear positive effect on the rate of mineralization of organic matter,
presumably by stimulating the bacterial populations to maintain high growth rates.
Furthermore, bioturbation by meiofauna increases nutrient and oxygen fluxes and thus
stimulates aerobic degradation of organic matter. Additionally we found that
mineralization in sediments with high meiofauna abundance did not increase further
when macrofauna was present. This suggests that the meiofauna community can drive
organic matter mineralization in sediments with reduced macrofauna abundance, thus
increasing resilience of benthic systems regarding the recycling of nutrients. On the
other hand, in Paper V we found that the presence of high numbers of meiofauna
significantly decreased the degradation of PAH, probably by feeding on PAHdegrading bacteria, thus explaining their reduced numbers in out test sediments. These
results improve our understanding of the fate of contaminants in aquatic ecosystems
and should be taken into account in bioremediation measures. Paper IV and V taken
together highlight the multi-faceted impact of meiofauna on benthic ecosystem
processes. Interestingly, we found grazing pressure on microbes to have positive
effects on a broad ecosystem function such as degradation of organic matter, which
can be performed by a large number of bacterial species. Conversely, this same
grazing pressure may be detrimental to ecological processes mediated by fewer, more
specialized bacteria, as found in Paper V. 5. CONCLUDING REMARKS AND FUTURE STUDIES
This thesis shows that both the type and quality of organic matter that reaches the
sediments affect the efficiency of resource utilization by meiofaunal populations. The
native Baltic deposit-feeding meiofauna seems to be critically dependent on spring
bloom input for growth, even though the amounts of cyanobacterial carbon
assimilated by meiofauna suggest that summer bloom of cyanobacteria can provide
some additional and perhaps important energy at times of low food availability. As
meiofauna also are food for benthic predators (Aarnio 2000; Aarnio et al. 1996), an
interesting future research questions is whether the type and quality of settling organic
matter has an impact on the nutritional value of meiofauna as prey. A logical
continuation of our experimental work in this area would be to confirm with field data
the importance of cyanobacteria as a food source for the different meiobenthic groups
20
and to test if meiofauna accumulate cyanotoxins and are transfer vector to higher
trophic levels. However, the detection limits of a variety of biochemical techniques
constitute an obstacle that will need good equipment and planning to overcome.
Biological interactions are extremely important in mediating the fate of organic matter
in aquatic sediments. In this thesis we show that interference competition from
macrofauna greatly reduces the incorporation of nutrients by meiofauna. In addition,
increased macrofaunal species richness also reduced incorporation of bloom material
by meiofauna, possibly due to the complementarity in spatial niche use between
macrofaunal species that reduce the availability of food for meiofauna. This
interaction may help explain how the relation between macrofauna and meiofauna is
regulated in soft sediment habitats. Since not all benthic species seem to depend on
fresh organic matter for food, an interesting future study area would be to determine
how interspecific competition can affect the use of older organic matter present in
sediments. It is possible that some meiofauna groups can switch to a higher reliance
on older organic matter when faced with strong interference competition by
macrofauna.
Meiofauna interactions with the microbial community in sediments clearly influence
the benthic ecosystem processes studied in my thesis. Meiofauna has a crucial role in
benthic ecosystems mediated both through facilitation processes and grazing pressure.
These results show that meiofauna has to be taken into account when studying benthic
ecosystem processes. It would be interesting to test how these biological interactions
depend on the type and quality of settling organic matter. In addition, since top-down
effects are a pervasive force in marine systems it would relevant to test how the
presence of benthic predators affect the dynamics of use of settling blooms by benthic
macro-, meio- and microfauna.
6. ACKNOWLEDGMENTS
During the past five years I had the luck and pleasure to work with a number of
people which contribution and support made this thesis possible. Foremost, I would
like to thank my supervisor Ragnar Elmgren for taking a chance on an unknown
student from Madeira. Ragnar is an invaluable source of wisdom and scientific
21
knowledge that spurred many inspiring discussions, not always only about science.
His guidance has allowed me to develop greatly as person and given me what I feel is
a great foundation for a career within science.
Thanks also to Agnes Karlson, my closest partner in this rollercoaster! Agnes’s
alertness, constant problem anticipation and readiness to press the panic button have
been an excellent complement to my southern European approach to life. Thank you
Agnes for being my sister in arms! The “mud gang” was never complete before Johan
Näslund joined us. Thanks Johan for all the good food, music and humor that have
brightened these past five years. Your (sometimes annoying) ability to always be
right, and talent to quickly solve any problem have been a great help! But most of all,
thank you both for all the laughs and friendship!
I gratefully acknowledge the financial support provided by the Fundação de Ciência e
Tecnologia. I am also very grateful to my assistant supervisor Clare Bradshaw and my
coauthors Elena Gorokhova and Jonas Gunnarsson for a great collaboration and all
the insightful comments that have helped shape my work. Thank you Jonas for your
contagious enthusiasm for ecotoxicology!
I am thankful to Emil Ólafsson for all the support at the start of this adventure. I
would like to also acknowledge the many people that have assisted me in my
experiments: Julia Stempa Tocca, Agnes Simon, Erland Karlson, Elke Mogner and
Hanna Axemar. Thank you Satu Viitasalo and Sanna Suikannen for good
collaboration in Finland.
Thanks to all the PhD students at the department for the joyful environment and the
camaraderie. Many thanks to the football gang for good fun every Friday and for their
attempt to disguise their disappointment for my painful lack of talent despite my
Portuguese genes.
Thank you to Katta and Julia for listening (most of the times) patiently to all my
moaning and to all my Swedish friends for warming cold Sweden for me. A big
“obrigado” to my friends in Portugal that never stopped caring and supporting me
despite the distance. I am very grateful Carlos Andrade and Natacha Nogueira (there
is no space for your full name!) for your infectious passion for marine science that
inspired me to get here. Thank you Tava for all the laughs and for carrying me
through my frequent downswings.
A special thank you to Lena for being our “family away from home” and proving that
quality is more important than quantity. Thank you for being a great aunt, sister and
22
friend! Thanks to Anita, Annika and Lars for welcoming with open arms into their life
and making me one of them.
Não tenho espaco para mencionar tudo o que devo aos meus pais. Principalmente
quero agradecer-lhes a coragem que me deram para perseguir a minha felecidade.
Obrigado também pelo infinito apoio que nem a um continente de distância deixou de
ser sentido. Obrigado tambem Carolina e Pedro por todo o incentivo.
And finally thanks to the two most important people in my life: Åsa and Sofia. Sofia
meu amor. Obrigado pela alegria e orgulho que sinto cada vez que olho para ti. Åsa
you were the spark that started this journey and the fire that kept it going. None of this
would have been possible without your love and constant support. It is an undying
privilege to walk this life by your side!
23
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