WALTER AND ANDRÉE DE NOTTBECK FOUNDATION
SCIENTIFIC REPORTS
No. 38
The effect of turbidity
on the ecology of pike larvae
MAIJU SALONEN
Academic dissertation in Aqauatic Sciences,
to be presented, with permission of
the Faculty of Biological and Environmental Sciences
of the University of Helsinki,
for public criticism in the Auditorium XII,
University Main Building, Fabianinkatu 33, Helsinki,
on November 9th 2012, at 12 noon.
HELSINKI 2012
This thesis is based on the following papers, which are referred to by their Roman numerals:
I.
Salonen, M., Urho, L. & Engström-Öst, J. 2009: Effects of turbidity and zooplankton availability on
the condition and prey selection of pike larvae. – Boreal Environmental Research 14: 981-989.
II.
Salonen, M. & Engström-Öst, J 2010: Prey capture of pike Esox lucius larvae in turbid water. –
Journal of Fish Biology 76: 2591-2596.
III. Salonen, M. & Engström-Öst, J.: Growth of pike larvae: effects of food quality and turbidity. –
Submitted manuscript.
IV.
Kallasvuo, M., Salonen, M. & Lappalainen, A. 2010: Does the zooplankton prey availability limit
the larval habitats of pike in the Baltic Sea? – Estuarine, Coastal and Shelf Science 86: 148-156.
The printed research articles included in this thesis are reproduced with the kind permission of Boreal
Environment Research Publishing Board (I), John Wiley and Sons Inc. (II) and Elsevier (IV).
CONTRIBUTION OF THE AUTHORS
I
Original idea
MS, JE-Ö
Study design
MS, JE-Ö
Data collection
MS, LU
Laboratory work
MS
Data analysis
JE-Ö, MS
Manuscript
MS
Providing comments
JE-Ö, LU
II
MS
MS
MS, JE-Ö
MS
MS, JE-Ö
MS
JE-Ö
III
MS
MS, JE-Ö
MS
MS
MS, JE-Ö
MS
JE-Ö
IV
MK, AL, MS
MK, AL, MS
MK
MS, MK
MK
MK
MS, AL
AL – Antti Lappalainen, JE-Ö – Jonna Engström-Öst, LU – Lauri Urho, MK – Meri Kallasvuo,
MS – Maiju Salonen.
Supervised by
Dr. Jonna Engström-Öst
ARONIA Coastal Zone Research Team
Novia University of Applied Sciences & Åbo Akademi University
Finland
Reviewed by
Prof. Hannu Lehtonen
Prof. Juha Karjalainen
University of Helsinki
University of Jyväskylä
FinlandFinland
Examined by
Dr. Anne-Christine Utne-Palm
University of Bergen
Norway
Custos
Prof. Jorma Kuparinen
University of Helsinki
Finland
The effect of turbidity on the ecology of pike larvae
MAIJU SALONEN
Salonen, M. 2012: – The effect of turbidity on the ecology of pike larvae – W. & A. de Nottbeck Foundation
Sci. Rep. 38: 1-38. ISBN 978-952-67851-0-3 (paperback), ISBN 978-952-67851-1-0 (PDF).
Organisms have environmental requirements in order to grow and reproduce. These restrictions concerning
environmental requirements lead to the overall distribution of organisms. Alterations in the environment
lead to acclimatisation, changes in distribution or even extinction of a species in the specific environment.
Eutrophication, increase of nutrients and consequently the general productivity level, is a global phenomenon
in the aquatic environment. In the Baltic Sea, the progress of eutrophication has been observed since the 1960s.
The central issue in my thesis is the shift in an environmental condition, i.e. the increase of water turbidity
due to increased primary production and the effects of turbidity on predatory fish, i.e. larval pike. In general,
phytoplankton-induced turbidity deteriorates the visual environment by absorbing visible light. Depending on
the fish species in question, this can have positive, negative or neutral effects on predator-prey interactions.
In addition to effects of water turbidity, my thesis focuses on the ramifications of the quality and quantity
of prey on first-feeding larval pike in the nursery grounds of the northern Baltic Sea archipelago areas. The
amount of suitable prey is important for effective growth. Rapid growth is essential for larvae, as growing
larvae becomes more aware of their surroundings, and are more able to avoid contact with predators and escape
attacks. The quality of zooplankton as prey is affected by community species composition, phytoplankton
community composition, temperature and eutrophication for example. The quality, in turn, has a direct impact
on the growth and development of planktivorous fish.
Pike populations have diminished in some coastal areas of the Baltic Sea since the 1970s, and the catches
have collapsed in areas where environmental changes have been considerable. My thesis included two field
studies, where environmental factors (salinity, turbidity, temperature, oxygen concentration, wave exposure)
and important resources (zooplankton quantity and community structure) are related to the distribution and
condition of pike larvae. I also conducted two sets of experiments that focused on the effects of turbidity and
food quality on prey capture and larval growth.
According to my results, phytoplankton-induced turbidity has a negative effect on larval pike condition
and growth. Turbidity also impacts prey capture negatively by diminishing the number of copepods captured.
In my experiment the quality of prey, measured as fatty acids, was higher in the outer site than in the inner
site. Both increased water turbidity and food quality affected the growth of larval pike when food quantity
was kept constant. However, more sites from both inner and outer archipelago zones should be surveyed in
the future to find out whether this is a trend or an outcome of this experiment. There were also other factors
that affected the larval pike populations in the two areas; the density of zooplankton is higher in the inner
archipelago sites compared with the outer archipelago sites while the density and condition of larval pike
were decreasing towards the outer archipelago sites simultaneously with increasing exposition to pelagic
circumstances. The occurrence and density of important prey species help explain the distribution of larval
pike in the archipelago areas, but as larval pike do not disperse much from the spawning grounds; this is
also related to adult pike spawning behaviour. The countries surrounding the Baltic Sea have made actions
to diminish the amount of allochtonous nutrients entering the sea. Even though many projects have led to a
4
decrease of these substances, the nutrient load is still quite high as the internal loading of nutrients sustains
the eutrophicated and turbid conditions of the sea for a long period of time.
Author’s contact information
Maiju Salonen, University of Helsinki, Department of Biological and Environmental Sciences, Aquatic
Sciences, P.O. Box 56 (Viikinkaari 9), FI-00014 University of Helsinki, Finland, Present e-mail address:
[email protected], [email protected]
5
Contents
1.INTRODUCTION...................................................................................................... 7
1.1. Environmental requirements of an organism..................................................... 7
1.2. Eutrophication and turbidity.............................................................................. 7
1.3. The Baltic Sea.................................................................................................... 9
1.4. Effects of turbidity on predator-prey interactions............................................ 10
1.5. Effects of food quality on fish.......................................................................... 12
1.6. Pike larvae........................................................................................................ 12
2. AIMS OF THE STUDY........................................................................................... 15
3. MATERIAL AND METHODS................................................................................ 16
3.1. Study areas....................................................................................................... 16
3.2. Field studies..................................................................................................... 17
3.3. Experimental set-ups........................................................................................ 18
4. RESULTS AND DISCUSSION............................................................................... 19
4.1.Turbidity.......................................................................................................... 19
4.1.1 Body condition...................................................................................... 20
4.1.2 Prey capture.......................................................................................... 21
4.1.3Growth.................................................................................................. 22
4.2. Prey quantity and quality................................................................................. 22
4.2.1 Zooplankton density and selection....................................................... 23
4.2.2 Differences in prey quality between inner and
outer archipelago sites......................................................................... 23
4.3. Larval habitats.................................................................................................. 25
4.3.1 Degradation of the nursery grounds.................................................... 25
4.3.2 Interactions with other fish species...................................................... 26
5. CONCLUSIONS AND FUTURE PROSPECTS..................................................... 27
6.ACKNOWLEDGEMENTS..................................................................................... 29
7.REFERENCES......................................................................................................... 31
6
7
1.
INTRODUCTION
1.1. Environmental requirements of
an organism
“At the heart of ecology lies the relationship
between organisms and their environments”
(Begon et al. 2006). A condition is an
abiotic environmental factor (e.g. salinity,
temperature, turbidity) that influences the
functioning of living organisms, but unlike
resources, conditions are not consumed
by organisms (Begon et al. 2006). For
environmental conditions, there is an optimal
concentration, which allows the organism
to perform at its best, and a wide range
of conditions and tolerances that allow
them to grow and reproduce in a certain
habitat. The required conditions may alter
throughout the life span of an organism. For
example, a larval fish may require different
environmental conditions than adult fish. A
summary of an organism’s tolerances and
requirements in its living habitat is called a
niche (Begon et al. 2006). Human activities
(e.g. acid rain, eutrophication and climate
change) change these conditions in many
ways. These processes change the conditions
in a habitat resulting in poorer conditions for
species, especially those living at the edge
of tolerance for some condition(s), despite
the amount of resources that the habitat has
to offer. This, in turn, has a strong effect on
the survival and distribution of a species
inhabiting the environment.
This thesis focuses on a specific human
induced change in the Baltic Sea resulting
in altered environmental conditions and
resource availability. Eutrophication
increases the amount of primary production
resulting in increased turbidity in the aquatic
environment. Eutrophication also changes
the production rates and community structure
in different trophic levels. These changes in
the visual environment and trophic levels
affect the entire food web, depending on the
species ability to acclimate to the prevailing
circumstances. In a food web, the visual
environment is an important factor for
visually oriented top-predator such as pike
(Esox lucius L.).
1.2. Eutrophication and turbidity
Eutrophication is a global problem in aquatic
ecosystems. This environmental change is
mainly caused by anthropogenic activities,
such as agricultural and industrial runoff, and
poor wastewater treatment. Eutrophication
can be defined as a complex of processes
leading to an increase in biological
productivity due to excessive addition of
particulate and dissolved inorganic and
organic materials to aquatic systems (Cooke
et al. 1993). Evidence of eutrophication in
the sea is also abundant, especially in coastal
areas (Bonsdorff et al. 1997, Lundberg
2005). Even though eutrophication in
coastal areas has been clearly detected, it
is difficult to assess the degree to which
coastal environments are affected, since these
they are usually quite nutrient-rich naturally
(Valiela 2006). This increase of supply or
production of organic matter leads to many
ecological and biogeochemical consequences
for the water biota.
The central problem in eutrophication
is the excessive inputs of phosphorus and
nitrogen to the water. This increase in nutrient
content has an effect on the whole food web
from primary producers to top predators, but
above all it increases the primary production.
Potential effects of eutrophication in lakes,
rivers and coastal zones include: increase of
biomass of phytoplankton and macrophyte
vegetation, shift to bloom-forming algal
species that might be toxic or inedible,
8
increase of biomass of benthic and epiphytic
algae, change in species composition of
macrophyte vegetation, increase of biomass
of consumer species, increase of incidence
of fish kills, reduction in species diversity,
changes in harvestable fish biomass, decrease
in water transparency, oxygen depletion in
the water body, taste, odour and drinking
water treatment problems, and decrease in
perceived aesthetic value of the water body
(Dokulil & Teubner 2011). The effects of
eutrophication can range from small shifts
in production and species composition to
elimination of most organisms (Valiela
2006). Eutrophication can also cause shifts
in the species structure of the phytoplankton
community. This shift can lead to a dominance
of fast growing, poor nutritional quality or
even toxic phytoplankton, which can decrease
the fitness and survival of other organisms
(Ikawa 2004, Suikkanen et al. 2007).
Through processes that change the habitats
of the fauna, eutrophication may favour,
have no effect, or impair feeding, growth
and survival of consumers from different
levels (Valiela 2006). However, as a result
of eutrophication, the secondary production
by zooplankton and benthos may increase
(Elmgren 1989) and this can be reflected
as an increase in fish fitness and production
(Valiela 2006). Planktivorous fish production
can also be indirectly affected in negative
ways via phytoplankton as a low quality
food resource necessary for zooplankton
growth (Lappalainen 2002, Schiewer 2008c).
The amount of macrovegetation can also
decrease due to eutrophication, resulting
in a decline of potential nursery habitats in
coastal areas, which, in turn, can decrease the
fish populations. In addition, the increased
amount of phytoplankton increases the
turbidity and light attenuation of the water
(Nielsen et al. 2002). Increased turbidity
affects predator-prey interactions in the
community (Utne-Palm 2002).
Turbidity is a visual property of water
and implies a reduction or lack of clarity
that results from the presence of suspended
particles (Wetzel 2001). Inorganic turbidity
is usually created by particles that originate
from the erosion of soil in catchment areas
and from resuspension of bottom sediments,
resulting in brownish-red coloration (Wetzel
2001). Organic turbidity is usually associated
with large concentrations of phytoplankton
or humic substances, and less frequently
pigmented bacteria or microcrustacea in the
water. This usually results in blue-green or
yellowish-brown coloration (Wetzel 2001).
In coastal areas, turbidity is caused by both
increased phytoplankton growth and river
run-off of seston. Turbulence and river
run-off, caused by rainfall washing organic
matter, soil and sand particles into the water,
increase the amount of clay suspended in the
water column. Comparing phytoplanktoninduced turbidity with inorganic turbidity
can be difficult as they have different
light absorbing and scattering properties.
Chlorophyll-a and other phytoplankton
pigments absorb visible light, leading to
light attenuation, whereas inorganic minerals
scatter large amounts of light that lead to high
turbidity values, despite low concentration
of suspended particles (Radke & Gaupisch
2005). The scattering of light interferes
mainly with the background light level and
reduces the contrast between the prey and its
background. In addition to affecting the light
conditions of the water, suspended clay can
hamper gaseous exchange, clog fish gills,
and even result in death (Ardjosoediro &
Ramnarine 2002). The primary production of
planktonic algae, on the other hand, favours
zooplankton growth, by increasing oxygen
concentrations via primary production, and
9
by removing toxic nitrogen compounds from
water (Boyd 1982).
1.3. The Baltic Sea
The Baltic Sea is the world’s second largest
brackish water basin. It is also one of the
most eutrophicated sea areas in the world
due to its unique features. The sea is shallow,
fairly young, and has had altering marine and
freshwater periods in its history. Salinity is
one of the most important factors regulating
the flora and fauna in the Baltic Sea. The
surface salinity varies from 1 psu in the
northernmost areas and inner archipelago
areas to approximately 20 psu in the Danish
straits. Fluctuations in salinity are related
to irregular saltwater inflows from the
Danish straits and freshwater inflow from
the surrounding rivers. There is a permanent
halocline in the Baltic Sea, which constantly
separates the less saline surface water from
the more saline water below 60 m. This layer
prevents complete mixing of the Baltic Sea
and thus, cuts the deeper basins off from the
supply of atmospheric oxygen (Schiewer
2008a, b). The replacement of oxygen is only
possible through heavy saltwater inflows
from the North Sea. This results in a constant
danger of the formation of anoxic regions
and regions containing H2S below the depth
of 130 m (Schiewer 2008a, b).
The flora and fauna consist mainly of
euryhaline species that have extended their
natural range from the North Atlantic, relicts
from previous periods of sea history, brackish
and freshwater species, as well as introduced
species (Segerstråle 1957). In general, the
biological structure of the Baltic Sea is
clearly reduced in its biodiversity, due to
the relatively young age of the sea and the
unfavourable salinity of 5-8 psu in the Baltic
proper (Schiewer 2008a, b).
The catchment area of the Baltic Sea
(1 745 100 km2) comprises in total 14
countries. Assuming the ratio between the
catchment area and surface area of the
Baltic Sea of 4:1, a moderate load is to be
expected (Schiewer 2008a, b). There are
over 85 million people inhabiting the area
with industrial and agricultural activities,
resulting in heavy pollution and nutrient load.
Eutrophication, resulting from direct and
indirect nutrient input, is considered to be a
major problem in the Baltic Sea (Schiewer
2008a, b).
The eutrophication process has continued
since the 1960s, and from the mid 1990s
onwards, rather than having external loads
of nutrients, the general development of
eutrophication is caused by internal loading
(Pitkänen et al. 2008). Simultaneously, as
an indication of ongoing eutrophication,
summertime chlorophyll-a concentrations
of the surface water have significantly
increased (Raateoja et al. 2005). The increase
in phytoplankton biomass is mainly caused
by an increase in cyanobacteria, chlorophytes
and other flagellates (Suikkanen et al. 2007).
A cyanobacteria-green algae dominated
community is generally poor quality food
for grazers (Officer & Ryther 1980, Brett
& Müller-Navarra 1997). During the last
20 years, the zooplankton species number
has been reduced in some areas (Schiewer
2008c). These changes have especially
affected the coastal areas, which are
important nursery areas for pike and other
fish. In the coastal waters, eutrophication
and its associated consequences have shifted
the biomass dominance of fish communities
from percids towards cyprinids (Ådjers et al.
2006, Pitkänen et al. 2008).
The area where my studies were conducted,
the Gulf of Finland, has the largest catchment
area and the highest freshwater inflow of all
areas in the Baltic Sea, and consequently the
10
largest external loading from the surrounding
areas (Pitkänen et al. 2008). The Gulf of
Finland is a shallow, estuarine sea area and
thus sensitive to external perturbations caused
by nutrient loading from its catchment, the
Baltic proper, the atmosphere, as well as to
changes in climatic conditions affecting its
physical regime (Pitkänen et al. 2008). The
south-western coastal habitats of the Gulf of
Finland consists of extensive and shallow
archipelagos, where the coastline is indented
and long, the sea is covered with ice in the
winter months, and tides and strong currents
are essentially absent (Segerstråle 1957). The
coastal zone can be divided into the inner,
middle and outer archipelago zones with
strong environmental gradients (i.e., salinity,
temperature and turbidity). Both marine and
freshwater fish species occur in the area, but
freshwater fish species form a substantial
part of the fish communities in the brackish
coastal areas (Ådjers et al. 2006).
In the future, the salinity of the Baltic
Sea is predicted to decrease due to increased
precipitation and river run-off. This is a
consequence of climate change (Meier 2006,
Meier et al. 2006), and due to a reduction in
the amount and frequency of saline water
inflows from the Atlantic Ocean (Suikkanen
et al. 2007). Furthermore, increased primary
production due to eutrophication and the
increased amount of suspended matter
due to river run-offs are likely to increase
water turbidity. A transition from more
saline summer conditions with higher Si
concentrations in winter towards higher
summer temperatures and higher N and P
concentrations was observed between 1979
and 2003 (Rönkkönen et al. 2004, Suikkanen
et al. 2007). Decreasing salinity also causes
decreases in some of the large zooplankton
in the Baltic Sea (Vuorinen et al. 1998).
There have been significant variations in
the abundances of mesozooplankton species
since the 1970s. The most abundant calanoid
copepod species (Temora longicornis,
Centropages hamatus, Pseudocalanus
minutus elongatus) have decreased,
whereas Eurytemora affinis and Pleopsis
polyphemoides (Cladocera) have increased
(Rönkkönen et al. 2004).
1.4. Effects of turbidity on predatorprey interactions
Predation is simply a consumption of one
organism by another organism, in which
the prey is alive when the predator attacks it
(Begon et al. 2006). Animals need a certain
amount of food for maintenance and when
this threshold is exceeded, the animal is
able to grow and reproduce. Increase in
the amount of prey increases the amount of
growth and reproduction to a certain plateau
(Begon et al. 2006). The amounts of these
food resources vary spatially and temporally,
creating differences between different years
and habitats. Predators can be divided in
generalists that can feed on variety of prey,
and specialists that feed on only one or a
few prey species. Amongst carnivores the
captured prey can often be classified to be
most valuable amongst those available or for
prey that provide an integral part of a mixed
and balanced diets (Begon et al. 2006). Our
species of interest, the pike is a predator that
captures prey ranging in size based in relation
to the mouth gape size, from the beginning
of exogenous feeding.
Turbidity has multiple effects on different
aquatic species. Many of the Earth’s
productive aquatic habitats are usually turbid
due to suspended sediments, algal blooms
and wind-driven suspension of sediments in
shallow water. Water turbidity changes the
environment mainly through diminishing
the amount of sheltering macrovegetation
11
and reducing the visual habitat. Many of
the fish species living in these habitats rely
on vision when catching prey (Abrahams &
Kattenfield 1997). Studies using larval stages
indicate that high turbidity has a negative
effect on visually preying fish (Vinyard &
O’Brien 1976, Confer et al. 1978, Gregory &
Northcote 1993, I, II, III, IV). On the other
hand, some studies show that intermediate
turbidity leads to higher feeding rates
(Boehlert & Morgan 1985, Miner & Stein
1993, Bristow et al. 1996, Utne-Palm 1999).
These differences stem from a difference
in feeding strategies and physiological
adaptations of fish species. Some fish
species use non-visual means in predation,
such as the lateral line, olfactory organ,
electro sensors or tactile stimuli to detect
prey and predators (Vincent & Thomas 2011,
Rodríquez & Lewis 1997), or they have good
sensory adaptation to low light, i.e., rod-cell
dominance in the retina (Rodríquez & Lewis
1997, Temple 2011). The ability to forage in
turbid environments is related to a species
ability to adjust to the new environmental
conditions. Common behavioural effects
of turbidity that have been detected are
decreased reactive distance to prey (Berg
& Northcote 1985, Quesenberry et al.
2007), reduced visual range, i.e., reducing
the volume of water searched (Aksnes &
Giske 1993), changes in the type of prey
(Rowe 1984, Gregory & Northcote 1993,
II), changes in amount of prey consumed
(Sweka & Hartman 2001, II) and decreased
growth (Vøllestad et al. 1986, III). Turbidity
may also enable some species to engage
in foraging activities that would be risky
under clearer conditions (Utne-Palm 2002,
De Robertis et al. 2003). This includes
increased foraging (Gregory & Northcote
1993), migration activities (reviewed by
Utne-Palm 2002), decreased anti-predator
behaviour (Gregory 1993, Snickars et al.
2004, Lehtiniemi et al. 2005), and increased
use of open water areas (Miner & Stein 1996,
Engström-Öst & Mattila 2008).
In many aquatic ecosystems, the ability
of prey and predator to detect each other
is impaired by turbidity (Abrahams &
Kattenfield 1997). Suspended particles
between predator and prey scatter light and
interfere with the detection of each other,
especially at long distances (Utne-Palm
2002). Larger piscivores, in particular, are
found to avoid turbid areas, because of the
lowered foraging abilities (Ruiz et al. 1993).
Young fish and crustaceans are also known
to use turbidity as shelter against predators
(Maes et al. 1998). This may reflect in the
community structure (Blaber & Blaber 1980,
Levy & Northcote 1982). Rodríquez & Lewis
(1997) found that fish with good adaptation
to low light were dominant in turbid lakes,
whereas visually oriented fish dominated the
clear lakes. Turbidity may enhance feeding
by increasing the contrast between prey and
its background (physical effects hypothesis)
(Hinshaw 1985), or by increasing feeding
motivation caused by the lowered risk of
predation (motivation hypothesis) (Gregory
& Northcote 1993).
In turbid conditions, light intensity is
important for fish. Increased light intensity
has positive effects on the visual range of
the predator up to a certain saturation level
(Vinyard & O’Brien 1976, Confer et al.
1978, Utne 1997). Turbidity is considered
to have positive effects on visual feeding if
the light intensity is medium or high (UtnePalm 2002). Low amount of light can reduce
foraging (Diehl 1988, Lehtiniemi et al. 2005)
and in combination with turbidity, feeding
can be reduced by diminishing prey contrast
and visibility (Miner & Stein 1993).
12
1.5. Effects of food quality on fish
High food quality, in terms of polyunsaturated
fatty acids (PUFA), and especially highly
polyunsaturated fatty acids (HUFA) are
important for fish larval development
(Sargent et al. 1999, Ahlgren et al. 2005). Of
these HUFAs, usually DHA (22:6ω3), EPA
(20:5ω3) and ARA (20:4ω6) are considered
essential (Sargent et al. 1999), but there are
also other important PUFAs, which belong
to ω3 and ω6 series (e.g., α-linolenic acid,
18:3ω3 and linoleic acid, 18:2ω6) that can be
metabolised to essential fatty acids in some
fish species (Tocher et al. 2003). PUFAs
are mainly important for cell membrane
functions (Brett & Müller-Navarra 1997).
HUFAs are critical in maintaining high
growth, survival, reproductive rates and food
conversion efficiencies for a wide variety of
marine and freshwater organisms (Brett &
Müller-Navarra 1997) and are also important
for fish larval behaviour and development
(Sargent et al. 1995). Eutrophication can
change phytoplankton composition towards
communities dominated by species of low
fatty acid quality (Raateoja et al. 2005;
Suikkanen et al. 2007), which again may
be reflected in the fatty acid composition of
prey used by fish larvae. Zooplankton fatty
acid composition is also affected by other
factors, such as water temperature (Farkas
1979) and zooplankton developmental stage
(Kattner & Krause 1987).
Without the effect of eutrophication on
the quality of food, there are differences
in the quality among invertebrate prey;
thus, equal amounts in weights of different
zooplankton species do not provide an equal
amount of energy for fish (Desvillettes et
al. 1997b). The general difference between
calanoids and cladocerans is that calanoid
copepods contain a higher amount of DHA
with a smaller fraction of EPA, whereas
cladocerans are rich in EPA, but poor in
DHA (Persson & Vrede 2006, and references
therein). Therefore zooplankton communities
dominated by cladocerans may provide a suboptimal food source for many fish species,
which contain and therefore presumably
require larger amounts of DHA (Ballantyne
et al. 2003, Kainz et al. 2004). On the other
hand, cladocerans are an important food
for planktivorous fish especially in lakes
(e.g. Tolonen et al. 2000). In addition, the
rule in aquaculture is that most organisms
grow better on mixed diets rather than on
any single food source, independent of any
measurable components of food quality
(Brett & Müller-Navarra 1997).
In general, larval organisms may be
more dependent on dietary HUFAs than
adults, because their high somatic growth
rates cannot be satisfied by their fatty acid
conversation capacities (Brett & MüllerNavarra 1997). After hatching, the essential
fatty acid (EFA) composition of food affected
the ability to feed (Bell et al. 1995), as
well as growth rates in larval and juvenile
fish (Watanabe 1993). In general, lack of
PUFA results in poor growth, high mortality
and malformations of cultured animals
(Shamsudin 1998). Animals vary in their
dependence on dietary fatty acids and their
abilities to synthesize these compounds from
precursors (Brett & Müller-Navarra 1997).
Pike larvae growth is known to be sensitive
to different fatty acids in zooplankton diets
(Desvillettes et al. 1997a). The ability of
pike larvae to synthesize essential fatty acids
from precursors is unknown (Desvillettes et
al. 1997a, 1997b).
1.6. Pike larvae
Pike is an important freshwater fish in the
northern hemisphere (Craig 1996), inhabiting
13
Fig. 1. Larval pike (Esox lucius L.)
many northern lakes and brackish waters
(Casselman 1996). Pike is also an important
catch for recreational fisheries. In northern
latitudes, pike spawns between April and
June (Urho et al. 1989, Billard 1996) in
shallow, vegetated, and sheltered areas
(Bry 1996). After hatching, larvae remain
attached to vegetation for 5-12 days, after
which, at a length of approximately 12-15
mm, they swim to the surface and fill their
swim bladder (reviewed by Billard 1996).
The mouth opens at 2-4 days post-hatch
and at 150-160 degree days (i.e., days on
which the mean daily temperature is above
the minimum temperature required for
development) the fry start to feed slightly
before completing the yolk-sac resorption at
approximately 160-180 degree days (Billard
1996). Larvae (Fig. 1) feed voraciously on
living prey, such as zooplankton, insect
larvae and afterwards, other fish larvae. The
size of the prey increases simultaneously
with mouth gape size.
Throughout its life cycle, aquatic
vegetation plays an important role for the
success and survival of pike (Bry 1996).
Larval pike is a visual ambush-predator.
For larval pike, vegetation provides shelter
from predators, more abundant prey, and a
suitable habitat for feeding and lurking for
suitable prey (Raat 1988, Bry 1996). Pike
are considered to be able to adjust to a broad
14
range of environmental factors but vegetation,
temperature, oxygen concentration, water
transparency, light intensity and water depth
are important for pike survival (Casselman
1996). Pike are primarily active during the
day, but feed usually in the crepuscular
hour and their predatory behaviour is more
effective from the cover.
In general, strong year classes of pike
are associated with high water levels
and flooded terrestrial vegetation during
spawning (Beckman & Elrod 1971).
Flooding increases spawning grounds and
offers an abundant supply of abundant
invertebrates. The optimum temperature
for growing young-of-year (YOY) pike is
22-23 °C, and around 19 °C for juveniles
and sub-adults (Casselman 1996). Pike are
also tolerant to low oxygen concentrations
(Casselman 1978), but in low oxygen levels
(<4 mg l-1), they move to better areas and
feeding ceases at <2mg l-1 (Casselman 1996,
Engström-Öst & Isaksson 2006). Adult pike
are dominant top-predators of the food web,
although they compete with other piscivores:
pikeperch Sander lucioperca, yellow perch
Perca flavescens and burbot Lota lota (Craig
1996). However, pikeperch may be more
successful than pike in turbid conditions
(Winkler 1991, Craig 1996), possibly due
to pikeperch’s good visual adaptations to
dim environments and to the deterioration of
macrovegetation important for pike (Craig
1996, Sandström & Karås 2002).
Pike populations have diminished in
some coastal areas of the Baltic Sea since
the 1970s (Lehtonen 1986, Lehtonen et al.
2009, Ljunggren et al. 2010). However,
despite its high ability to adapt to changes
in environmental conditions (Casselman
1996), catches have collapsed in areas
where environmental changes have been
considerable (Lehtonen 1986, Nilsson et al.
2004, Nilsson 2006). The decrease in pike
abundance seems spatial, and the species
has mainly diminished in areas that are
influenced by harsh pelagic circumstances,
such as the effects of upwelling and currents
from the open sea (Lappalainen et al. 2008).
The amount of stabilising reed (Phragmites
australis) beds has increased especially in
the outer archipelago areas. Most of the outer
archipelago reed beds are usually small and
narrow, and therefore have little effect on
stabilising the pelagic conditions; in spring
time some of these reed beds may even dry
out due to low water levels (Lappalainen et
al. 2008). Reed beds in the inner archipelago
with low salinity, high water temperature and
dense vegetation are considered especially
productive for fish reproduction (Kallasvuo
et al. 2011, IV). Furthermore, the average
weight of caught pike has increased with
decreased catches in the outer archipelago
(Lehtonen 1986, Lehtonen et al. 2009).
Recruitment failure is suggested to be the
main reason for this phenomenon (Lehtonen
1986, Nilsson et al. 2004, Ljunggren et al.
2010). Decrease in pike catches is suggested
to be related to low zooplankton abundances
(Ljunggren et al. 2005), declining habitat
quality and quantity and eutrophication
(Winkler 2002), predation of larvae and
eggs (Nilsson 2006) and toxic substances
(Breitzholtz et al. 2001).
Most piscivorous fish have planktivorous
larval stages. Often when studying fish
species biology, the impacts on the larval
stages concerning recruitment and survival
are ignored. For pike, information on the
impact of water transparency on 0+ year
pike behaviour and habitat use is generally
sparse (Skov & Koed 2004). Many of the
studies involving pike are conducted with
juveniles or adults (Craig & Babaluk, 1989,
Casselman & Lewis 1996, Beaudoin et al.
1999, Jepsen et al. 2001, Andersen et al.
2008). Further, most of the sparse information
15
on larval or YOY pike is conducted with
larger individuals than in my studies (Bry
et al. 1992, Skov & Berg 1999, Jacobsen
et al. 2007, Skov et al. 2002, Jönsson et
al. 2011). I used pike larvae in the range
12 to 19 mm in length, in which case they
are truly first-feeding planktivorous larvae
with ongoing physical development. Larger
pike are known to forage also in lower light
intensities due to well-developed vision and
lateral line (Volkova 1973). Development of
lateral line occurs when pike are between
22 and 56 mm (Raat 1988). Pike larvae
become piscivorous at the size of 15-30 mm
(Samardina 1957, Ivanova & Lopatko 1983,
Hudd et al. 1984). In my studies, only a few
of the largest larvae, collected from the field
had a small fish in their stomachs.
2.
AIMS OF THE STUDY
There are two main forces causing major
changes in the Baltic Sea: eutrophication
and climate change. Both of these two forces
are interrelated and seem to deteriorate
pike larvae habitats. In my thesis I studied
effects on fish larvae caused mainly by
eutrophication. My focus was the effects of
phytoplankton-induced turbidity and food
quality and quantity on the success of firstfeeding pike larvae in the Gulf of Finland.
My aim was to study and gather
information on first-feeding larval pike that
are mainly in a zooplankton phase. The
first fieldwork conducted concentrated on
finding out which environmental factors
and resources are affecting larval condition
in different areas of the archipelago (I).
As a result, turbidity, food quality and
quantity became the main interests in this
thesis. Turbidity deteriorates the visual
environment of the water. Depending on
species, turbidity has a negative or positive
effect on predator-prey relationships. I focus
on the effect of turbidity on prey capture of
larval pike, hypothesising that water turbidity
has a negative effect on the prey capture and
foraging success of pike larvae (II).
For larval pike, successful prey capture,
i.e. energy needed for growth, is important,
since growth is essential for successful
recruitment to the adult population.
Differences in prey capture may affect the
food quality of larval pike, since different
zooplankton species differ in their nutritional
value. Eutrophication is also affecting the
nutritional value of a zooplankton species.
I wanted to find out if quality differences in
zooplankton communities existed between
the two archipelago sites (inner and outer),
and whether this would affect the growth
of larval pike (III). In addition to quality
differences between research sites, I tested
whether water turbidity would further
negatively affect the growth of larval pike
(III).
In the fourth article the aim was to
evaluate whether the availability of suitable
zooplankton limits the distribution of the
coastal larval areas. In addition to this I
compared the availability of zooplankton
prey between different types of coastal
littoral habitats and evaluating the suitability
of different habitats as larval pike nursery
areas (IV). Since the focus of my studies is
quite narrow considering the general status
of larval pike in the Baltic Sea, I evaluate
my results by combining them with some
studies from different points of view and
also raise some questions for future concerns
in order to understand the future threats for
pike populations.
16
Fig. 2. Map of the study areas (Modified from article IV, © Elsevier Ltd. 2009). The areas are divided
into inner (A), intermediate (B) and outer (C) archipelago. Detailed information on the additional sites
and area division in the field survey conducted in Ekenäs, Pojo and Tvärminne archipelago, are shown in
article I. Dragsviksfjärden and Joskär are food sampling sites in article III.
3.
MATERIAL AND METHODS
3.1. Study areas
Coastal areas of the brackish northern Baltic
Sea archipelago areas can be divided into
inner, middle and outer archipelago areas
due to the varying environmental conditions
and gradients. Towards the outer archipelago
areas the water : land ratio increases, the
average size of islands decreases, exposure
increases and the environmental conditions
become harsher compared with the sheltered
inner archipelago (Granö et al. 1999,
Tolvanen et al. 2004). Due to freshwater
inflow from rivers and the complexity of
the archipelago, there are large gradients
especially in salinity, temperature and
turbidity from the inner archipelago towards
the outer archipelago. The study area was
located in the south-western coast of Finland
in the Archipelago Sea (60ºN, 21ºE) and in
Ekenäs, Pojo and Tvärminne archipelago
(60ºN, 23ºE) (Fig. 2). The areas were divided
into inner (A), intermediate (B) and outer
(C) archipelago by given features of the
environmental parameters, and previous
studies in the area (Lappalainen et al. 2008).
17
Table 1. Summary of methods for data collection in the field studies.
Variable
Method / Equipment
Article
Salinity
Measured with Thermo Fischer Scientific portable
temperature and conductivity meter or calculated from
conductivity (Hanna Instruments 9835)
Measured with YSI model 95 or Thermo Fischer
Scientific portable temperature and conductivity meter
I, IV
Surface water loggers
IV
Measured with YSI model 95
Measured with Hach 2100P Turbidimeter
Measured with a white Secchi plate, ø 25 cm
Estimated using an effective wave exposure (fetch) index
with a 25 m resolution (Isæus 2004)
3 parallel samples collected by mixing 3 Limnos samples
and taking a 100 ml subsample, or by collecting 15
litres of water with a 2 l scoop and filtering zooplankton
through a 50 µm (I) or 90 µm (IV) sieve, preserved with
acid Lugol’s solution
Filtered through a 43 µm mesh to remove detritus,
10-25% of sample counted under a microscope with a
cuvette using 6× objective (Wild 40)
Fish weighted to the nearest 0.0001 g (Mettler Toledo
AX205). Fish length measured with a graph paper under
a binocular microscope (Leica)
Stomachs emptied and content identified and counted
under a microscope (Wild M40, Leica)
I, IV
I,
IV
IV
Water temperature
Water temperature changes
in time
Oxygen concentration
Water turbidity
Secchi depth
Wave exposure
Zooplankton sampling
Handling of zooplankton
samples
Measuring the fish
Stomach contents
Strong environmental gradients existed from
the inner bays to the outer archipelago areas,
as well as between sites within the different
areas (I, IV, Lappalainen et al. 2008). For
example water turbidities measured in article
I varied between 14.6 NFU in the most turbid
inner archipelago site to 3.16 NFU in the
outer archipelago. Shores covered with reed
beds are considerable part of the shoreline
in the study areas especially in the inner
archipelago areas (Härmä et al. 2008).
I, IV
I, IV
I, IV
I, IV
I
3.2. Field studies
Articles I and IV concentrated on the
effect of environmental variables on the
distribution and condition of larval pike. In
article I, the Ekenäs, Pojo and Tvärminne
archipelago was surveyed in order to find
out which environmental factors affected
the condition of larval pike the most (Fig.
2). Article IV concentrated on finding
out the distribution of larval pike in the
archipelago areas, finding out the suitable
18
reproduction habitats, and whether the
amount of zooplankton prey affected the
distribution (Fig. 2). The data collecting was
conducted in May and June in 2005 (I), and
2006-2007 (IV). Data on the environmental
variables (salinity, turbidity, Secchi depth,
temperature, oxygen concentration, wave
exposure) were collected in addition to
zooplankton samples and pike larvae (Table
1). From the sampling site, approximately
100 m of the shoreline was checked with a
criss-cross pattern, with a sampling duration
of 30 min per study site using two samplers.
In the inner archipelago areas, the spawning
starts earlier and continues longer due to
earlier increase in water temperature. The
sites were visited several times during the
whole spawning period to ensure that all the
possible larval sites were found. Pike larvae
were located using a white plate, and then
caught rapidly with a scoop and preserved
for further analysis. Further details about the
capture method of the fish larvae can be found
in Lappalainen (2008). The samples were
mainly collected from the reed bed shores,
but to find out the suitable reproduction areas
of the larval pike, other shores (i.e., bladder
wrack (Fucus vesiculosus,) shores and shores
without vegetation) were included in article
IV. The condition of larval pike for article
I was estimated from residuals from logtransformed linear relationship of weights
and lengths of larval pike (Ormerod &
Tyler 1990). Values >0 were treated as good
condition, and values <0 as poor condition.
3.3. Experimental set-ups
Articles II and III consists of experimental
studies conducted in the laboratory of
Tvärminne Zoological Station (University
of Helsinki). Fish for the experiments were
obtained from a hatchery in Raseborg
(Trollböle fish hatchery). Parental fish were
of freshwater origin. The fish were obtained
approximately 4 days post-hatch at yolk-sac
phase. They were transported to the station
in a plastic bag containing oxygen-enriched
river water and gradually acclimated to
prevailing seawater temperature. The fish
were reared in 628 l container with brackish
seawater flow-through in a roofed outdoor
facility. The container was aerated to ensure
oxygen levels. The light regime was natural,
varying between 17 : 7 h and 19 : 5 h light :
dark hours during the study period. Before
the experiments, the larvae were reared until
the yolk-sac was fully absorbed and external
feeding had started. Larvae were fed three
times a day with a mixture of zooplankton
community (Table 2), consisting mainly
of copepods (Acartia bifilosa, Cyclops sp.,
Eurytemora affinis and cladocerans (Bosmina
sp., Chydorus sp.).
The experiment was designed to find out
whether phytoplankton-induced turbidity
has an effect on the predation and more
specifically on the capture success of different
prey species (II). The zooplankton species
were chosen due to the clear differences
in behaviour and due to their common
occurrence in the reproduction sites. In the
experiment, larvae were allowed to feed
on zooplankton for 2 h in turbid or clear
water in a 1.5 liter tank. The larvae were fed
with in total 100 prey individuals, of which
50 individuals were cladocerans Daphnia
longispina and 50 individuals were copepods.
The experiment was conducted in two parts,
with two types of copepods together with D.
longispina. In the first part of the experiment,
the larvae were fed with calanoid copepods
(Eurytemora affinis) and in the second part of
the experiment they were fed with cyclopoid
copepods (Cyclops sp.). After the experiment
the fish were preserved and the stomach
content was analysed in order to find out if
19
Table 2. Summary of methods for data collection in the laboratory experiments.
Variable
Method / Equipment
Article
Water turbidity
Zooplankton collection
Measured with Hach 2100P Turbidimeter
Collected with a 90 µm plankton net in open water or
reed bed shores
Fish weighted to the nearest 0.0001 g (Mettler Toledo
AX205). Fish length measured with a graph paper
under a binocular microscope (Leica)
Stomachs emptied and content identified and counted
under a microscope (Wild M40, Leica)
Folch method by Hamilton et al. (1993) was used
Seawater was aerated and filtered through a 10 µm
plankton net in a temperature controlled room (15 °C)
Created with cultured chlorophyte Brachiomonas
submarina (strain TV15) from the collection at
Tvärminne Zoological Station, grown in TV2
medium (Hällfors & Hällfors 1992)
II, III
II, III
Measuring the fish
Stomach contents
Fatty acid analysis
Experiment water
Experiment turbidity
there was a difference in capture rate between
turbid and clear water treatments.
The second experiment was carried out to
reveal, firstly, how turbidity affects growth
of larvae in different sites of the archipelago,
and secondly, if there is a difference in prey
quality between more or less eutrophicated
areas, i.e. inner and outer archipelago (III).
Zooplankton was collected from inner and
outer archipelago sites (Table 2; Fig. 2).
Individual fish were reared for 13 days in
1.5 l plastic tank with turbid or clear water,
provided with inner or outer zooplankton
assemblages as food. Larvae were fed twice
a day with a specific amount of zooplankton
prey and the containers were cleaned
regularly. The larvae were weighed six times
during the experiments to follow growth.
The prey quality was analysed by measuring
the fatty acid content from zooplankton
community (Table 2).
4.
III
II
III
II, III
II, III
RESULTS AND DISCUSSION
4.1. Turbidity
In general, increased turbidity had a negative
affect on pike larvae resulting in decreased
body condition and growth (I, III), and
fewer prey capture of copepods in turbid
water (II). In general, these results agree
with earlier studies that turbidity affects pike
behaviour. The results on the mechanism,
however, vary in the different studies with
different developmental phase and size of
fish. Turbidity was an important factor even
though turbidity in the experiments was not
as high as the highest turbidities measured
in the field (I). For instance, Vøllestad et al.
(1986) found that pike grew more slowly
in a turbid river system than in a less turbid
lake, even though the prey quantity was
higher in the turbid river system. Nilsson
20
et al. (2009) implied that impaired visual
conditions can improve foraging success
for pike. Even though the visual range
decreased with increased turbidity, Nilsson
et al. (2009) suggested that habitat-choice
overlap and probabilities of prey encounter
for pike could actually increase in higher
turbidities. In turbid conditions 0+ pike (9-17
cm) were spread more evenly also outside
the vegetation cover (Skov et al. 2002), and
they foraged also in lower light intensities
due to well-developed vision and lateral line
(Volkova 1973). Craig & Babaluk (1989)
showed that individual pike weight was
related to water Secchi depth. With every
increase in Secchi depth of 1 m over the
1-3 m range, body weight increased by 6 %.
The authors concluded that high turbidity
could inhibit feeding of pike in Canadian
prairie lakes during open-water period. As
stated earlier, in my study the pike larvae
were small first feeding and still physically
developing larvae, of which few studies are
available.
4.1.1 Body condition
In my field study, the condition of pike
larvae worsened significantly with increasing
water turbidity (I), though there was a large
variation in turbidity and body condition
of pike larvae between areas in the inner
archipelago (I). The correlation between
water turbidity and body condition was based
on a few key observations in the most turbid
areas and the trend was reinforced by the
lack of larvae in good condition in the most
turbid areas (I). Poor predation success leads
to poor condition, growth and survival. Most
of the larvae in the outer archipelago had an
empty stomach (I). The body condition and
stomach content observations in the clear
water and outer archipelago areas indicate
that water turbidity is not the only factor
determining the condition of larval pike, but
it was a factor that indicated further research
is necessary.
In the inner archipelago zooplankton
density was found to be high (I, IV), but
of poorer quality (III) and zooplankton
in general may even be smaller in size in
eutrophicated areas (Uye 1994). For pike
larvae in the inner archipelago, changed
selection towards secondary food (II), and
possibly poor quality and smaller size of
prey (III) (Uye 1994), can lead to poor
larval condition. In general, eutrophication
increases the amount of zooplankton in the
Baltic Sea, but the zooplankton community
structure is changing towards smaller and
less preferred food species (Rönkkönen et al.
2004, Schiewer 2008c). Uye (1994) found that
copepod size can decrease in eutrophicated
areas. In addition, eutrophication affects the
quality of zooplankton as food when fast
growing and poor quality phytoplankton
increase (Officer & Ryther 1980, Brett &
Müller-Navarra 1997).
My results showed that pike larval
condition was the best in the intermediate
archipelago areas, moderate in the inner
archipelago areas, and the worst in the outer
archipelago areas (I). In addition to turbidity,
there were many other factors that could
have influenced larval condition in the outer
archipelago. The archipelago zone in the
western Gulf of Finland is defined by strong
environmental gradients in e.g., temperature,
and salinity and turbidity. Shores covered
with reed beds constitute a considerable part
of the shoreline in the study area, especially
in the inner archipelago bays and other
sheltered sites, where coverage can be as
high as 58 % in the innermost areas (Härmä
et al. 2008, IV). In the outer areas, the reed
beds are smaller and narrower, which could
indicate that environmental conditions for a
21
larval pike are more unstable and exposed
in terms of e.g., currents, mixing and
temperature. The intermediate archipelago
area consisted of shallow and sheltered
bay areas (I), where turbidity was lower,
potentially due to stabilizing effects of the
vegetation (Munsterhjelm 2005). In this area,
the salinity was high enough to prevent roach
(Rutilus rutilus) reproduction (Härmä et al.
2008), thereby diminishing the possible
competition for zooplankton between these
species. The fullness of the stomach was the
highest in this area, which indicates good
food conditions as well (I).
4.1.2 Prey capture
According to the results of this study, turbidity
had a strong effect on the composition of prey
found in the stomachs of pike larvae. Our
laboratory studies also showed, the larvae
consumed fewer copepods Eurytemora
affinis in turbid water, compared with clear
water, but no such effect could be detected
when larvae were fed with cladocerans
Daphnia longispina (II). The results of the
second experiment with copepods Cyclops
sp. and D. longispina gave similar results
(II): feeding on Cyclops sp. decreased,
but feeding on D. longispina remained the
same. Predation activity can be divided
into different stages: search, encounter,
active choice, attack, capture, ingestion and
digestion. In this study, turbidity affected the
capture success (II). Since turbidity degrades
the visual environment, the ability to see
more than one prey at a time may deteriorate,
making the selection process or active choice
more difficult. It has also been shown that
turbid water affects the visibility of prey
species differently. Copepods adjust their
pigmentation as a response to UV light.
Carotenoid-pigmented copepods in algal
turbid water caused a relative increase in
foraged prey of juvenile pike (Jönsson et al.
2011). With young pike larvae, the selection
of prey can be affected by undeveloped prey
detection skills (Wanzenböck & Schiemer
1989), which during non-optimal conditions
may direct the attention to more conspicuous
and less evasive prey.
This turbidity effect in prey capture may
be negative for larval pike. In general, large
and evasive copepods are preferred prey
by pike larvae (I, Lehtiniemi et al. 2007).
Copepods quickly fulfil the larval pike
energy demand, enabling them to grow
rapidly (Peterson & Wroblenski 1984,
Urho 2002). Pike larvae select larger prey
and avoid small prey, such as the juvenile
stages of rotifers and copepod, i.e., nauplii
(I, Lehtiniemi et al. 2007). Differences in
capture and escape abilities can be attributed
to the differences in prey capture between
clear and turbid water. Different prey
species exhibit different escape, motion and
swimming abilities (O´Keefe et al. 1998).
In general, prey with ‘active and irregular’
motion patterns can be more attractive for
planktivorous fish than prey with smooth
swimming behaviour (Buskey 1994). There
are variations in swimming behaviour
between the studied prey species (Viitasalo
et al. 2001). Cyclopoid copepods can exhibit
sporadic swimming with periods of rest,
whereas some calanoid species swim nearly
continuously for extended periods (Hwang
& Turner 1995). Daphnia spp. (cladocerans)
however, are relatively slow-swimming
animals and are unable to escape predation as
rapidly as copepods (Drenner et al. 1978). In
degraded visual surroundings, pike larvae are
more likely to capture the slowly swimming
cladocerans since copepods can escape from
the predators reduced visual field of range.
22
4.1.3 Growth
In the experiment studying the effect of
turbidity with two different zooplankton
assemblages (from inner and outer
archipelago sites), the larvae showed
highest wet weight in clear water with
outer site zooplankton as prey and lowest
growth in turbid water feeding on inner site
zooplankton (III). The wet weight of the
larvae increased significantly over time in
all treatments (III). There was a significant
interaction between time and turbidity,
as well as between time and zooplankton
assemblage, indicating that both zooplankton
and turbidity had a significant effect on larval
wet weight over time (III). The early growth
of pike is usually extremely rapid under
favourable conditions (Bry et al. 1991). In
our experiment the density differences of
the two sites were ignored and the amount
of food was made equal in both studies,
which made it possible to evaluate the
differences in food quality and zooplankton
community structure rather than the real
differences in the densities of proper food
between the two sites. The amount of good
prey species was higher in the inner site, but
due to eutrophication the quality of the food
may have been different. The zooplankton
community-caused growth differences were
especially notable in turbid water, whereas
almost no differences were found in growth
between clear water treatments (III). It seems
that the zooplankton community is pivotal
to the pike larvae when the water is turbid,
whereas it is not of primary importance in
clear water. The poor growth of pike larvae
in turbid conditions can be partly explained
by previously mentioned effects of turbidity,
i.e., prey selection and body condition.
Similar results show that growth seems to
be negatively affected by turbidity even
though attack rates increase (Engström-Öst
& Mattila 2008).
Many studies have shown that turbidity
reduces growth (Vøllestad et al. 1986,
Sweka & Hartman 2001, Sandström 2004),
whereas others found no effect of turbidity
on growth (Van de Meutter et al. 2005), and
some reported positive effects (Sirois &
Dodson 2000). Rapid growth is essential for
larvae, since growing larvae becomes more
aware of the surroundings, and are therefore
more able to avoid contact with predators
and escape from attacks (Litvak & Legget
1992). A poor growth rate among larvae may
sustain an adult biomass in pike population,
when larval densities are high and prey is a
limiting resource (Craig 1996). In the inner
archipelago areas prey can be a limiting
resource due to poor visual surroundings,
but as the amount of larval pike is high (IV),
the adult population is viable. In the outer
archipelago areas, the adult population has
been decreasing and larval densities are also
lower (I, IV). In my experiment the amount
of prey was adequate for good growth as
opposed to the reported prey abundances in
the field (IV).
4.2. Prey quantity and quality
There were clear differences in food quantity
between the different sites in the archipelago
area (I, IV). The amount of proper food
is higher in the inner archipelago sites (I,
IV). There was significant difference in food
quality between inner and outer archipelago
site that together with varying turbidity
affected the growth of larval pike (III).
The food quantity in the beginning of the
exogenous feeding phase of larvae is crucial
for the survival of the larvae (Ljunggren et al.
2005). The fish larvae of top-predators must
pass a number of ontogenetic diet shifts, and
23
are suggested to be sensitive to predation
during their early life stage, as well as to
competition with specialised planktivores for
zooplankton resources (Persson & Greenberg
1990). Recruitment of young pike depends
partially on an adequate relationship between
nutritional requirements and prey quantity/
quality, particularly in the beginning of
the exogenous feeding (Desvillettes et al.
1994). The quality of prey changes with
changing phytoplankton species community
composition, and is therefore affected
by eutrophication. In surveys made in
the Baltic Sea, the proportion of rotifers
generally increases at low total numbers of
zooplankton, which indicates that the amount
of proper zooplankton prey decreases along
with total zooplankton abundance, having
negative effects on larval pike (Rönkkönen
et al. 2004, Ljunggren et al. 2010).
4.2.1 Zooplankton density and selection
Pike is a generalist feeder that selects a variety
of prey of appropriate size (Mamcarz et al.
1998). My results support the size-selection
hypothesis (Brooks & Dodson 1965), stating
that planktivores should select the largest
prey items, because it is energetically the
best choice. Main prey of pike larvae was
different copepods (calanoid, cyclopoid) and
cladocerans, of which Chydorus sp. was
the main taxon (I). Throughout the studied
archipelago prey preference was very similar,
though there were some differences due to
density and availability of prey species,
and the amount of pike larvae in the area.
Rotifers were strongly ignored and copepod
nauplii only rarely selected (I). My findings
on prey selection were supported by earlier
studies (Samardina 1957, Lehtiniemi et al.
2007). Among micro-crustaceans identified
as possible prey for young pike at the onset of
exogenous feeding, small cladocerans, such
as Chydorus sphaericus (Chydoridae) are
found in littoral zones among macrophytes
(reviewed by Bry 1996). Chydorus sp. was a
frequent prey for pike larvae in my study (I).
Chydorus sp. may be tempting prey for first
feeding larvae due to their slow swimming
and dark coloration.
Adequate density of prey is essential to
support efficient growth. The total amount of
zooplankton, as well as the number of most
preferred prey (cladocerans and cyclopoid
copepods) diminished towards the outer
archipelago (I, IV). In the outer archipelago,
zooplankton community consisted of three
taxa, whereas in the inner archipelago,
twelve zooplankton taxa were present (I). In
the inner zone, rotifers, cyclopoid copepods
and cladocerans predominated, while rotifers
and calanoid copepods dominated the
zooplankton community in the outer zone
(I). Earlier studies from the northern Baltic
Sea pelagic areas have shown that cyclopoid
copepods and cladocerans are more abundant
in the less saline inner bays than in the open
sea (Viitasalo et al. 1995, Vuorinen et al.
1998, Koski et al. 1999, Telesh 2004).
Consequently, the zooplankton community
in the outer archipelago consisted of prey that
either was not preferred by pike larvae, was
not available to them, or occurred in too low
densities. This may explain why there were
few larvae in the outer archipelago (I, IV).
According to Ljunggren et al. (2005), prey
quantity is a central factor for pike larval
success.
4.2.2 Differences in prey quality between
inner and outer archipelago sites
In total, there were higher concentrations
of fatty acids in the outer archipelago site
samples than in inner site samples (III).
24
The amounts of polyunsaturated fatty
acids (PUFAs) and monounsaturated fatty
acids (MUFAs) were also higher in the
outer archipelago site samples (III). There
were, however, no significant differences
in saturated fatty acids (SAFAs) (III). Of
single fatty acids, 18:3ω6 was the only
one found in outer archipelago site, and
when significant differences between other
individual fatty acids were found, the
amounts were always higher in the outer
site (III). The results indicate a higher quality
of prey species in the outer site. This was
also reflected in the growth of larval pike.
In the turbid environment the growth of
larvae in inner archipelago zooplankton was
especially low (III). Species assemblages
in both phyto- and zooplankton can cause
these quality differences, since different
species store different amounts and types
of fatty acids (Desvillettes et al. 1997b,
Arts et al. 2001, Ikawa 2004). There are
also intra-specific differences in the fatty
acid composition of a single species, due
to differences in the food they consume in
different regions (Sekino et al. 1997). In the
Baltic Sea, cyanobacteria, chrysophytes, and
chlorophytes have increased since the end of
the 1970s (Suikkanen et al. 2007); of these
cyanobacteria and some chlorophytes are
considered poor quality food for herbivorous
zooplankton (Brett & Müller-Navarra 1997,
De Mott & Müller-Navarra 1997, Brett et
al. 2000).
There were also differences between
the zooplankton community structures
between these sites (III). The amount of
cyclopoids and insects were higher in the
samples from the outer site samples, whereas
cladocerans dominated the inner archipelago
site zooplankton community (III). It has been
demonstrated that qualitative differences
exist among invertebrate prey ingested by
pike larvae (Desvillettes et al. 1997b, Brett
et al. 2006). Desvillettes et al. (1997b)
suggested that larvae fed with copepod
Eucyclops serratus, cladocerans of the genus
Chydoridae and chironomid larvae were in
better condition nutritionally and had a faster
rate of growth than the ones fed with E.
serratus and the cladoceran Bosmina sp. as
food (Desvillettes et al. 1997b). Some studies
show that copepods contain a larger fraction
of DHA and less EPA, while cladocerans
are rich in EPA but slightly poorer in DHA
(Farkas 1970, Ballantyne et al. 2003, Persson
& Vrede 2006). Research with young yellow
perch (Perca flavescens) has demonstrated
that equal weights of different zooplankton
prey do not provide an equal amount of
energy for the fish (Confer & Lake 1987, Arts
& Sprules 1989). Furthermore, a zooplankton
community, dominated by cladocerans
may constitute suboptimal food for many
fish species, which contain and therefore
presumably require larger amounts of DHA
(Ballantyne et al. 2003, Persson & Vrede
2006). Since the stomach content of the larvae
and the specific fatty acid content of each
prey species were not analysed it is difficult
to evaluate whether the poor growth in turbid
conditions was caused by the poor food
quality of a single prey species or reduced
predation abilities in total due to water
turbidity. In our experiment, particularly in
turbid conditions where the ability to capture
copepods is poor (II), it is possible that with
the high amount of cladocerans in the inner
archipelago site samples, the food ingested
is mainly constituted of cladocerans. This
rather monotonous diet of a poorer quality
may result in poorer growth. Most organisms
grow better on mixed diets rather than one
type of food (Brett & Müller-Navarra 1997).
Since the experiment was conducted only at
two sites, more sites should be surveyed to
determine whether the quality differences
are a major influencing factor. The effect
25
of the different zooplankton community
densities on growth should also be taken into
account when considering the larval growth
of pike in the coastal zones of the Baltic
Sea. Nevertheless, according to my study,
quality and prey community differences exist
between sites and together with turbidity
these differences affect the growth of larval
pike in general.
4.3. Larval habitats
The focus of my thesis has been to evaluate
the effects of turbidity, food quantity and
quality on the ecology of pike larvae. There
are, however, some other aspects, related
to heavy eutrophication that can affect the
survival of pike. The effects of eutrophication
on pike populations are well known
throughout the world. Low eutrophication
levels may even support the increase of
the pike population due to elevated levels
of macro-vegetation, leading to increased
amount of spawning and nursery areas. But
the long-term decline of pike populations in
many areas, such as Oneida Lake, New York,
the Bay of Quinte in Lake Ontario, the Große
Müggelsee near Berlin, and Lake Constance
(reviewed by Bry 1996) has been connected
with eutrophication. Bry (1996) suggested
that the negative effects of eutrophication
on pike populations are partly mediated by
the progressive disappearance of aquatic
macrophyte vegetation.
4.3.1 Degradation of the nursery grounds
In the study area, pike were only observed on
reed-covered shores (IV). No pike larvae were
detected in bladder wrack (Fucus vesiculosus)
shores or shores lacking vegetation (IV).
Pike are dependent on vegetation, especially
in their early life stage. The relationship
between water depth and size of pike during
the first year is highly correlated. The larger
the pike gets, the deeper water it inhabits
(Casselman & Lewis 1996). In a preface
to an International Pike Symposium it was
stated, that “altered recruitment processes
associated with changes and losses in critical
habitats and flow regime characteristics,
water quality declines, and climate change
threatens this species worldwide” (Farrel et
al. 2008). Human-induced processes, such
as loss of wetlands, reduction of shoreline
cover and structure, cultural eutrophication,
and siltation have both negatively affected
water transparency and the abundance of
macrophyte habitats, and this process causes
further reductions in pike body condition
and abundances (Casselman & Lewis
1996). The same processes are also seen
in the Baltic Sea. Reduced catches of pike
have been reported in some parts of the
outer archipelago (Lehtonen et al. 2009)
and there are many implications of coastal
changes: eutrophication, loss of macrophytes
(Eriksson et al. 2004, Munsterhjelm 2005),
increase of turbidity (I, II, III), and climate
change (Rönkkönen et al. 2004).
On the other hand, the amount of softbottom reed bed shores has increased
especially in the outer archipelago areas.
Although pike eggs and larval pike have been
found in the outer archipelago (Lappalainen
et al. 2008, I, IV), the reed bed shores in
the outer archipelago areas may be unfit for
successful pike nursery areas. In addition,
adult pike are philopatric, which affects the
distribution of pike larvae in the archipelago
in general. Larvae show high site fidelity and
usually remain to a large extent in the area
where they are hatched (Karås & Lehtonen
1993). According to our study, there are
fewer larvae in the outer archipelago reed bed
shores (I, IV) and the few specimens found
26
in the outer archipelago are usually in poor
condition (I). The amount of zooplankton
is also lower in the outer than in the inner
archipelago (I, IV), even though the food
quality might be higher there (III). It seems
that the occurrence and density of cyclopoid
copepods in the reed bed shores significantly
explained the distribution of larval pike.
The increasing exposition to the pelagic
circumstances also diminishes the amount
of larval pike in the outer archipelago areas
(IV). Zooplankton communities in the outer
archipelago reed beds were more similar
to communities in pelagic waters, which
lack freshwater zooplankton, such as larger
copepod species and most of the cladocerans
(Viitasalo et al. 1995). Most of the outer
archipelago reed beds are usually small and
narrow, and therefore have little effect on
stabilising the pelagic conditions, and in
spring time some of these reed beds may even
dry out due to low water levels (Lappalainen
et al. 2008). It has earlier been suggested that
reproduction in the inner areas has been so
important and efficient that the inner areas
functions as a source of young pike that
migrate to the outer areas (Lappalainen et
al. 2008). With degrading conditions in large
areas in the inner archipelago, the annual
amount of larvae produced has diminished,
which might weaken this mentioned sourcesink system (Lappalainen et al. 2008).
A newly discovered threat to larval
habitats is climate change that affects the
winter and spring conditions. Winter ice
coverage time is shorter and the onset of
spawning may be altered. The timing of
spawning is important for establishing good
growth conditions for the larvae. As there
must be enough zooplankton when the yolksac is fully absorbed and, also, enough insect
and fish larvae later in summer to sustain
fast growth. Changes in temperature may
interfere with the timing of spawning and lead
to a mismatch with springtime zooplankton
appearance. The timing of the spawning
of roach may also change and change the
status of roach larvae as prey to a competitor,
especially in turbid environments. Due to
climate change the timing of floods may also
shift from snowmelt in spring to summer,
autumn or even wintertime (Bergström et
al. 2001).
4.3.2 Interactions with other fish species
Due to eutrophication, the fish fauna
composition of the Baltic Sea has changed.
The catches of two important coastal
predators, pike and perch (Perca fluviatilis),
decreased by 80 % along the west coast of
the Baltic proper in the 1990s (Ljunggren et
al. 2010). In addition to this decline, coastal
communities consist of high abundance of
small-bodied facultative planktivores, such
as the three-spined stickleback (Gasterosteus
aculeatus) (Eriksson et al. 2009). These
changes in the community structure may
lead to a new and interesting situation in the
nursery grounds, when pike larvae are in the
zooplanktivorous stage. According to recent
studies the recruitment failure of pike may
be driven by limited food availability for
larvae, which again may have been caused
by competition with sprat (Sprattus sprattus)
and three-spined sticklebacks, competing for
zooplankton in coastal areas (Ljunggren et
al. 2010). Stickleback diet includes copepods
and cladocerans (Lehtiniemi et al. 2007).
The number of roach has increased in the
past years in the Baltic Sea (Lappalainen
2002). In general, roach feed on a variety
of prey, and seems to switch prey type when
changing abundances allow (Lehtiniemi
et al. 2007). In eutrophicated lakes, the
omnivorous roach is attributed to a high
potential growth rate with high predation
efficiency on cladocerans (Jeppesen et al.
27
2000, and references therein), and an ability
to exploit small zooplankton prey (Jeppesen
et al. 2000). To the best of my knowledge,
there are no studies available concerning
competition between roach and pike larvae. It
can only be speculated, whether the increased
number of larval or older omnivorous roach
in the Baltic Sea coastal areas has an effect
on survival and recruitment of pike larvae.
On the other hand, roach spawns slightly
later than pike. During optimal conditions,
the switching of pike from zooplankton prey
to small fish prey occurs simultaneously
with the hatching of roach and moreover
with perch and three-spined stickleback. Pike
larvae can then make use of the abundant
food resources constituted of newly hatched
larvae of these other fish species.
5.
CONCLUSIONS AND FUTURE
PROSPECTS
My results show that young and partly
undeveloped zooplanktivorous pike larvae
seem to be strongly affected by turbid
conditions. This is seen in the results of the
field studies (I), where one of the explanatory
factors for the condition of pike was turbidity.
Water turbidity has a negative effect on
pike larval growth (III) and diminishes
the capture of copepods (II). Most of the
previous work studying pike and turbidity
has been conducted with older pike that are
already in the piscivorous stage of their life
cycle, rather than the planktivorous phase,
resulting in slightly different results. Turbid
habitats impair the growth and development
possibilities of first-feeding larval pike, and
could therefore affect successful recruitment
to the adult population (Fig. 3).
According to my studies, food quality and
food quantity, in addition to turbidity, affect
pike larval life history. The occurrence and
density of important prey species explains the
distribution of larval pike in the archipelago
areas (IV) and the increasing exposition to
the pelagic circumstances diminishes the
amount of larval pike in the outer archipelago
areas (IV). According to the laboratory
experiment, the quantity of the prey is
adequate in the inner site, but the quality is
lower, and turbid conditions complicate the
search for prey. Nevertheless, more research
should be conducted to find out whether the
qualitative differences exist throughout the
Baltic coastal zones. The affect of different
zooplankton community structures should
also be evaluated. The larvae with the best
condition were found in the sheltered middle
parts of the archipelago where turbidity was
lower. The amount of suitable zooplankton
is adequate and there is no interaction with
roach (I) (Fig. 3).
Turbidity is one consequence of
eutrophication that is known to have
negative effects on the pike populations
throughout the world mainly by a decrease
of suitable reproduction and nursery habitats,
i.e. macrovegetation (Bry 1996). In the
eutrophicated Baltic Sea, the reason for
decreasing amounts of pike seems to be poor
recruitment to the adult population (Lehtonen
1986 Lehtonen et al. 2009, Ljunggren et
al. 2010). Decrease in pike catches have
also been related to predation of larvae and
eggs (Nilsson 2006), competition with other
species and toxic substances (Breitzholtz et
al 2001).
The countries surrounding the Baltic Sea
have made actions to diminish the amount
of allochtonous nutrients entering the sea.
Even though many projects have led to a
decrease of these substances, the amount of
the nutrient load is still quite high. In addition
to this, there is an on-going process of
internal loading of nutrients, which sustains
the eutrophicated and increased turbid
28
Fig. 3. Differences between inner (A) and outer (B) archipelago zones. Factors, such as water
turbidity (I, II, III), zooplankton species composition (IV), prey density (I, IV), pelagic
impact (IV), shore vegetation and reed bed size (IV) influence the success of larval pike.
Differences in other factors such as intra- or interspecific competition with other species (e.g.
with roach) and predation (e.g. by three-spined stickleback) could also be locally important
but this remains to be experimented in the future.
29
conditions of the sea for long periods of time.
It has been estimated that climate change
will increase precipitation, including rainand snowfall. Precipitation thereby increases
the amount of solids and nutrients that flow
from the land into the sea. Suspended solids
further increase turbidity of the water. On the
other hand, increased precipitation will also
decrease salinity, which could have positive
effects on pike.
However, there are other factors, most
of which are related to eutrophication that
influence successful pike reproduction in the
Baltic Sea. These missing elements are to
some extent known, but in order to obtain a
clear understanding of the processes, which
leads to the diminishing of pike in parts of the
Baltic Sea, more research must be conducted.
According to my studies in the field and
in the laboratory, high water turbidity, low
food quality and low quantity of important
prey species have a negative effect on pike
larval population that seems, for one’s part,
to restrict the amount of recruitment to the
adult population.
6.
ACKNOWLEDGEMENTS
The studies included in this thesis have been
financed by the Onni Talas Foundation, the
Walter and Andrée de Nottbeck Foundation,
University of Helsinki and Prunus Attorneys.
On our life long journey people
continuously grow and learn not only from
books but from the surrounding nature and
especially from other people. In my journey
by far I have met different kinds of people:
wonderful, challenging, encouraging,
irritating fun, et cetera. What is common
with all the people I have met is that they
all have influenced me, made me grow as
a person and in a way made me what I am
right now.
I would like to thank Dr. Anne-Christine
Utne-Palm for acting as an opponent in
the public examination of my thesis. Prof
Jorma Kuparinen for acting as a custos in
the public examination, aiding me in the
final meters of my studies and helping me
with the university bureaucracy in the thesis
process. I sincerely thank and acknowledge
the reviewers Juha Karjalainen and Hannu
Lehtonen for valuable comments on my
thesis. I thank Charles C. Beetschen for
checking the English language even though a
beautiful baby girl and work keeps him very
busy (Arigato go zai masu, ありがとうござ
います). I also thank Carl-Adam Hæggström
for editing my thesis.
My warmest thanks go to my supervisor
Jonna Engström-Öst. Making of my thesis
has been pretty colourful with so many
happenings from collecting Christmas trees
with a plankton net to braking bones and
cross ligaments and us both moving from
Helsinki and making it pretty challenging to
meet. Thank you for supporting, helping and
guiding me through all of these years. We
have come up with a lot of ideas, of which
only a minority is in my thesis, so I hope
we can continue the journey and make our
fun and interesting scientific plans become
reality!
I would like to thank people at the
Tvärminne Zoological station for supporting
and helping me through all the springs that
I spent there. I thank Marko Reinikainen
for always being there to assist whenever
some equipment or advice was needed.
Spending time making the experiments
was possible only because the station took
such a good care of my family and me. My
daughters still ask me to call the station
and ask whether we could come and spend
some time in “Muumitalo”. In addition to the
staff, I would like to thank all the colleagues
working with me in many summers. Special
30
thanks to Minna Saaristo for helping me
rearing my larvae and letting me help in
fishing some gobies and Anna Arnkil who
was an indispensable help for me with the
experiments.
Thank you for members of Ezeco and the
Finnish Marine institute for giving me the
opportunity to do the thesis. Especially the
help of Soile Saesmaa and Tarja Katajisto
were irreplaceable in zooplankton sampling.
I would also like to thank Aronia coastal
research group that has been a distant but
mellow point of reference and guidance in
these final years. Special thanks to Markus
Öst for helping with all the statistics and Anu
Vehmaa for assistance with pictures, comments
on manuscripts and thesis. Håkan Strandberg
from Trollböle hatchery kindly provided the
larvae for the experiments each year.
I never thought that I would have a
laboratorian in me, but owing to Pirkanmaa
University of Applied Sciences and the
indefatigable help of Heli Knuutila and I
found out that even a pretty complicated
analysis is doable. Thank You for all the help
with the fatty acid analysis, I would have not
survived without your help!
The first summer when I started with
the fieldwork I was very lucky to get help
from true specialists from Finnish Games
and Fisheries Institute: Meri Kallasvuo,
Lari Veneranta, Lauri Urho and Antti
Lappalainen. Jouni Tammi, I sincerely thank
you for helping, teaching, brainstorming
and supporting me with the field studies.
Antti and Meri, thank you for the valuable
comments on the finalising of my thesis. I
feel priviledged to have been able to cooperate with you in these studies.
If it wasn’t for the valuable comments on
Meri, Antti, Anu, Kirsi Kostamo, Andreas
Brutemark and Zeynep Peckan-Heckim I
would probably still be wondering whether
the text is worthy of publishing or finished or
even understandable. Thank you for the tips
and proposals of improvement. Hopefully
the end result also pleases You !
To all my dear friends, I’m deeply
grateful for the friendship and support.
Counterbalancing my thesis, sharing the
life outside the research with sports, music,
parties and discussions etc. with friends
have been priceless. My best friend Virve,
thank you for patiently listening for all the
good and bad things that has been over the
years. For the last two months when working
with my thesis, the short moments spent
crayfishing with you have been moments
of rest and fun!
I would like to thank my parents SirkkaLiisa and Mauri, who already at an early
age taught me, that everything is possible
if you really want so. They have always
encouraged me to go forward in life and
challenge myself in order to keep active
and lively. The support and help with our
baby boy that I gained when finalizing my
studies and thesis has been very important.
My brothers Sami, Toni and Jari did a good
job in making me a resistant, stubborn and
resilient woman – even though they do deny
in doing so  – Love you and your families,
Thank you for all the support!
Family is the most empowering,
strengthening and the most important force
there is. I would like to thank my daughters
Lotta and Milla for bringing a lot of joy,
laughter and happiness in my life. The smiles
and sounds that our baby boy Topi gives me
every single day, makes me strong and happy.
My husband Ville, we have been together
and made plans for our future since Lukio.
You have been my friend, my soulmate, my
competitor, my opponent and everything in
between. Without you I would never have
gotten this far, and you keep encouraging
me even further. For that I thank you – I
love you!
31
7.
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