Zooplankton growth and trophic linkages
Transcript of Zooplankton growth and trophic linkages
Zooplankton growth and trophic linkages: Implications for fish feeding conditions in the Baltic Sea
Towe Holmborn
ii
Doctoral Thesis in Marine Ecology, 2009
Towe Holmborn, [email protected]
Department of Systems Ecology
Stockholm University
SE-106 91 Stockholm
Sweden
© Towe Holmborn, Stockholm 2009
ISBN 978-91-7155-908-1
Printed by US-AB, Stockholm, Sweden
Cover: Zooplankton, by T. Holmborn
v
ABSTRACT
The aim of this Thesis was to improve our understanding and assessment of feeding
conditions for zooplanktivorous fish in the Baltic Sea.
We investigated (papers I, II) the usefulness of biochemical proxies for assessments of
growth and metabolic rates in the dominant Baltic copepod Acartia bifilosa. A predictive
model (paper I) for egg production rate (EPR), based on body size, RNA content, and water
temperature, was established using females of different geographical origin. This model
demonstrates the usefulness of RNA content as a proxy for growth in zooplankton and,
together with abundance data, it could be used to evaluate fish feeding conditions. Further
(paper II), using A. bifilosa exposed to a food gradient, we evaluated responses of
physiological rates and other biochemical proxies for growth and established correlations
between physiological and biochemical variables. EPR and ingestion rate were most
significantly correlated with RNA content. As assayed variables saturated at different food
concentrations, food availability may affect assessments of physiological rates using
proxies. In paper III, we explored the effect of high EPR and ingestion rate on astaxanthin
content in A. bifilosa. We found that the astaxanthin content decreased at high feeding
rates, most likely due to decreased assimilation efficiency. This may impact the quality of
zooplankton as prey.
The invasion of Cercopagis pengoi, a zooplanktivorous cladoceran, has altered the trophic
linkages in the Baltic Sea food web. In paper IV, we evaluated the feeding of
zooplanktivorous fish on C. pengoi and found that irrespective of size both herring and
sprat feed on it, with large herring being more selective. In turn, C. pengoi feeds mainly on
older copepods (paper V), which are acknowledged important in fish nutrition. These
results indicate that C. pengoi may compete with fish due to the diet overlap.
Keywords: AARS activity, biochemical markers, Clupea harengus, copepod physiology,
food web interactions, non-indigenous species, RNA-based indices, Sprattus sprattus,
stable isotopes.
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SAMMANFATTNING
Denna avhandling syftar till att förbättra analysmetoder för och utvärdering av
födoförhållanden för Östersjöns djurplanktonätande fisk (tex stömming och skarpsill). I
studie I och II undersökte vi om biomarkörer kan användas för att mäta tillväxt (I, II) och
metabolisk aktivitet (I) hos den vanliga hoppkräftan Acartia bifilosa. Vi fann att RNA
innehåll i hoppkräftan väl speglade äggproduktionen, oberoende av honornas geografiska
härkomst (I). En prediktiv modell baserad på RNA-innehåll, honans storlek och
vattentemperatur förklarade 51% av variationen i äggproduktion. Vidare (II) undersökte vi
fyra olika biomarkörers förmåga att prediktera äggproduktion, respiration, och födointag i
ett experiment med olika födotillgångar. Honans RNA-innehåll beskrev äggproduktionen
och födointaget bäst. Men, eftersom olika variabler nådde sitt maxvärde vid olika
födokoncentrationer, kan prediktering av fysiologisk aktivitet med hjälp av biomarkörer
(som i modellen i studie I) vara missvisande vid höga födokoncentrationer (som tex under
en algblomning). Förutom kvantiteten av djurplankton är kvaliteten av de samma en viktig
faktor för fiskens födoförhållanden. En viktig antioxidant heter astaxanthin och bildas
bland annat av hoppkräftor efter födointag av ”byggstenar” som finns i alger. I den tredje
studien (III) undersökte vi om födokoncentrationen påverkar mängden astaxantin i A.
bifilosa. Vi fann att även om produktionsstatus och födointag ökade med ökad
födokoncentration så ökade bara astaxantininnehållet till en viss gräns innan det minskade
igen. Kontentan är att vid höga födokoncentrationer produceras många hoppkräftor, men av
sämte kvalitet, med avseende på astaxantin. I de två sista arbetena (IV, V) fokuserade jag,
via fältstudier, på konsekvenser för det pelagiska ekosystemet av den nyligen introducerade
rovvattenloppan Cercopagis pengoi. Vi fann (IV) att de två vanligaste djurplanktonätande
fiskarna i Östersjön (skarpsill och strömming), oavsett ålder, åt C. pengoi. Därför, beroende
på om C. Pengoi äter samma djurplankton som dessa fiskar, eller om de föredrar mindre
byten, kan deras närvaro i Östersjön minska alternativt öka födotillgången för fisk. I papper
V undersökte vi därför vad C. pengoi äter. C. pengoi föredrog stora hoppkräftor men även
till viss mån hinnkräftor och mindre djurplankton (hjuldjur). Totalt sett utgjorde stora
hoppkräftor den stösta andelen föda. Resultaten tyder på att C. Pengoi kan bidra till ökad
födotillgång för fisk, eftersom de bättre utnyttjar de små djurplanktonen, men även till en
ökad risk för konkurrens med fisk, då de framförallt äter samma typ av föda.
Informationen i denna avhandling kan hjälpa oss att förstå den viktiga länken mellan
djurplankton och fisk i den fria vattenmassans födoväv. Den typen av information är
nödvändig för att på ett hållbart sätt kunna förvalta Östersjöns fiskbestånd samt för att
förstå och prediktera framtida påverkan på ekosystemet orsakat av tex övergödning,
klimatförändringar och nyintroducerade arter.
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CONTENTS
ABSTRACT v
SAMMANFATTNING (in Swedish) vi
CONTENTS 7
LIST OF ABBREVATIONS 8
PROSPECT OF THESIS 9
LIST OF PAPERS 10
AN INTRODUCTION TO THE STUDY SYSTEM 11
The study area – The Baltic Sea 11
Crustacean mesozooplankton in the Baltic proper 11
Zooplankton in the Baltic Sea pelagic food web 13
ASSESSING ZOOPLANKTON GROWTH AND METABOLIC ACTIVITY 14
Using biochemical macromolecules to assess growth and metabolic activity in zooplankton 16
Creating a model to assess in situ egg production rate (paper I) 17
Comparing usefulness of different biomarkers (paper II) 18
Applicability of RNA-based models for in situ growth assessments in the Baltic Sea 19
QUANTITY – QUALITY 20
Carotenoids in the food web 20
Factors affecting astaxanthin levels in copepods 21
Copepod astaxanthin content in relation to food concentration (paper III) 21
THE ROLE OF NON-INDIGENOUS ZOOPLANKTON IN THE BALTIC SEA
PELAGIC FOOD WEB 23
C. pengoi as a prey (paper IV) 23
C. pengoi as a predator (paper V) 24
The overall impact of cladoceran NIS in the Baltic Sea pelagic food web 26
CONCLUSIVE REMARKS AND FUTURE PERSPECTIVES 28
ACKNOWLEDGEMENTS 30
REFERENCES 32
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LIST OF ABBREVATIONS
AARS Aminoacyl-tRNA synthetases
EPR Egg production rate (eggs ind-1
day-1
)
NIS Non-indigenous species
PL Prosome length (mm)
RNA content RNA content in females (µg ind-1
)
RNA:DNA Ratio of RNA and DNA content
RNA:protein Ratio of RNA and protein content
spAARS Protein specific AARS activity (nmol PPi mg protein-1
h-1
)
T Temperature (°C)
YOY Young-of-the-year
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PROSPECT OF THESIS
The overall aim of my Thesis was to improve assessments of fish feeding conditions
in the Baltic Sea and to increase our understanding of the link between zooplankton
and fish. To do this, I conducted studies on (1) physiological and biochemical
determinants of quantity and quality of copepod production, and (2) effects of a non-
indigenous zooplankton species on the pelagic food web and fish feeding conditions
in the Baltic Sea. This was, more specifically, done by:
Exploring the possibilities of using biochemical proxies to assess growth
and metabolic status in copepods (papers I, II). This approach could, for
example, provide us with useful analytical tools for assessments of in situ
zooplankton growth and nutrition, which are necessary for evaluating fish
feeding conditions and to refine food web models.
Investigating the consequence of high feeding and production rates on the
quality of zooplankton as prey. The quality aspect in this study (paper III)
concerned the important antioxidant astaxanthin. Studies of this kind will
help us understand connections between quantity of zooplankton and its
quality as a prey for higher trophic levels, including fish. In the Baltic Sea,
this is relevant with respect to the eutrophication that has altered the
general productivity status but also to the natural seasonal variations in
productivity.
Investigating top-down and bottom-up effects of the non-indigenous
predatory cladoceran Cercopagis pengoi in the Baltic Sea pelagic food web
(papers IV, V). Studying trophic interactions of this recently introduced
species with native prey and predators is crucial for understanding and
predicting the impacts of this non-indigenous species on the Baltic Sea
pelagic food web and fish feeding conditions.
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LIST OF PAPERS
The Thesis is based on the following papers, referred to in the text by their Roman
numerals (published papers are reprinted with kind permissions of the publishers):
I Holmborn T, Gorokhova E (2008) Relationships between RNA content
and egg production rate in Acartia bifilosa (Copepoda, Calanoida) of
different spatial and temporal origin. Marine Biology 153(3): 483–491.
©Springer
Holmborn T, Gorokhova E (2008) Erratum to: Relationships between
RNA content and egg production rate in Acartia bifilosa (Copepoda,
Calanoida) of different spatial and temporal origin. Marine Biology
153(5): 1007–1008. ©Springer
II Holmborn T, Dahlgren K, Holeton C, Hogfors H, Gorokhova E.
Biochemical proxies for growth and metabolism in Acartia bifilosa
(Copepoda, Calanoida). Submitted to Limnology and Oceanography:
Methods. Conditionally accepted manuscript
III Holeton C, Lindell K, Holmborn T, Hogfors H, Gorokhova E (2009)
Decreased astaxanthin at high feeding rates in the calanoid copepod
Acartia bifilosa. Journal of Plankton Research 31(6): 661–668. ©Oxford
Journals
IV Gorokhova E, Fagerberg T, Hansson S (2004) Predation by herring
(Clupea harengus) and sprat (Sprattus sprattus) on Cercopagis pengoi in
a western Baltic Sea bay. ICES Journal of Marine Science 61(6): 959–
965. ©Oxford Journals
V Holliland P, Holmborn T, Gorokhova E. Assessing diet of the non-
indigenous predatory cladoceran Cercopagis pengoi using stable isotopes.
Manuscript
My contributions to the papers were:
I Participation in planning of the study, all fieldwork, all analysis and data
processing, main part of the writing.
II Participation in planning and execution of the experiment (responsible for the
egg production and egg viability analyses), most data processing, main part of
writing.
III Participation in planning and execution of the experiment (responsible for the
egg production and egg viability analyses), commenting on the manuscript.
IV Participation in planning of the study, all analysis, except the one of the
zooplankton community, most data processing, writing of the first draft.
V Participation in planning of the study, microscopic analysis of the zooplankton
community, commenting on the manuscript.
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AN INTRODUCTION TO THE STUDY SYSTEM
The study area – The Baltic Sea The Baltic Sea is one of the largest brackish water seas in the world. It has a natural
salinity gradient with higher salinities in the south (Jansson and Velner 1995), and
therefore, the organisms living in the Baltic Sea is a mixture of freshwater and
marine species. Compared to fully saline or fresh water areas, the species diversity is
very low in areas with a salinity of 6–7 (PSU, A. Remane, according to Ackefors
1965), a salinity that corresponds to the conditions of my study areas; coastal
regions of the northern Baltic proper (Fig. 1).
BALTIC SEA
SWEDEN
FINLAND
I-V
.. I
Figure 1. Schematic map of the Baltic Sea. The black dots indicate areas in the northern Baltic
proper used for field sampling that provided data for this Thesis. The Roman numerals denote
the paper(s) in question for the sampling site. For a more detailed description of the sampling
sites see the respective papers.
Crustacean mesozooplankton in the Baltic proper Zooplankton is a diverse group with respect to e.g., taxonomy, life history traits,
behavior, and size. The size group of zooplankton called mesozooplankton (0.2–2
mm) consists mainly of small crustaceans, such as copepods and cladocerans. They
constitute a major link between primary producers (e.g., planktonic algae) and
higher trophic levels (e.g., mysids and fish).
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The calanoid copepods are among the most abundant and productive zooplankton
groups in the Baltic proper (Ackefors 1971, Ackefors and Hernroth 1972). They are
generally present in the water column throughout the year being more numerous
during summer (Ackefors and Hernroth 1972). There are several species of calanoid
copepods abundant in the northern Baltic proper; however, in coastal areas, only a
few species are found in great numbers, e.g. Acartia bifilosa and Eurytemora affinis
(Hessle and Vallin 1934, Ackefors 1981). The copepods of genus Acartia are
broadly distributed around the world (Bradford 1976) and are numerically dominant
or co-dominant copepods in most estuaries (Turner 1981, and references therein).
Acartia are free-spawning, opportunistic omnivores (Castel 1981) that feed on
phytoplankton, detritus and small heterotrophs depending on availability (Turner
1984, and references therein).
A. bifilosa (paper I, II, III; Fig. 2a) is a dominant species in many European
estuaries (e.g., Irigoien and Castel 1995, Burdloff et al. 2002) and can also be found
elsewhere in the northern hemisphere (Razouls et al. 2005–2009). In the Baltic Sea,
it occurs in salinities between 4 and 8 (Hessle and Vallin 1934, Viitasalo et al. 1994)
and tolerates a wide range of temperatures. However, it is rarely found in cold
waters or below 50 m depth (Hessle and Vallin 1934). Therefore, in the Baltic Sea,
A. bifilosa is abundant in offshore areas but is far more numerous and important in
coastal areas (Hessle and Vallin 1934, Hernroth and Ackefors 1979, Ackefors 1981).
In fact, it has been suggested that A. bifilosa is the most important copepod in
coastal areas of the Baltic proper (Ackefors 1981) and it is also recognized as an
important prey for fish (Turner 1984, and references therein, Arrhenius 1996, Voss
et al. 2003).
The cladocerans found in the northern Baltic proper are usually only present in the
water column during the warm season and overwinter as diapause eggs (Ackefors
1971). However, during the warm season they can be found in large numbers
(Hessle and Vallin 1934, Ackefors 1981). In archipelago areas, Pleopsis
polyphemoides, Bosmina maritima, and Cercopagis pengoi are the most abundant
species (Hessle and Vallin 1934, Litvinchuk and Telesh 2006).
C. pengoi (paper IV, V; Fig. 2b) is a predatory cladoceran native to the Ponto-
Caspian region (Rivier 1998). It was probably introduced form the Black Sea
(Cristescu et al. 2001) via the Volga-Baltic waterway (Leppäkoski and Olenin
2000). In 1992, the first specimens were recorded in the Gulfs of Finland and Riga
(Ojaveer and Lumberg 1995, Krylov et al. 1999), and in 1997, the first specimen on
the Swedish coast was found (Stockholm archipelago and Gotland basin; Gorokhova
et al. 2000). It has since spread to the southern regions of the Baltic proper (Bielecka
et al. 2000, Litvinchuk and Telesh 2006, Olszewska 2006), and from the Baltic Sea
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to the North American Great Lakes (MacIsaac et al. 1999, Cristescu et al. 2001). In
the Baltic Sea, C. pengoi is especially abundant in coastal areas (Litvinchuk and
Telesh 2006) and it is generally more numerous in the upper part of the water
column (down to 10 m depth) than in deeper layers (Krylov et al. 1999), which may
indicate its preference for warmer temperatures.
Figure 2. Species in focus in this Thesis: a) Acartia bifilosa, adult (CVI) female, the model
organism in paper I, II, and III; b) Cercopagis pengoi, gamogenetic female (barb stage III)
carrying two diapause eggs, the species in focus in paper IV and V.
Zooplankton in the Baltic Sea pelagic food web Generally, the population dynamics of fish stocks depends on their reproductive
success, i.e. successful spawning and survival of embryos and larvae (Fogarty and
O´Brien 2009). The reproductive success, in turn, depends on a variety of abiotic
variables, but also on feeding conditions for larvae (Kalejs and Ojaveer 1989,
Ojaveer and Lehtonen 2001). Nearly all fish species, including piscivorous fish, feed
and depend on zooplankton in their early life, as larvae and/or juveniles. The major
zooplanktivorous fish in the Baltic Sea are sprat (Sprattus sprattus) which is a
holozooplanktivore, and herring (Clupea harengus), whose diet also includes
mysids, amphipods, and small fish (Rudstam et al. 1992, Thurow 1997).
Due to the central position that zooplankton have in the Baltic Sea pelagic food web,
studies on zooplankton production, in terms of both quality and quantity, would
facilitate assessments of energy flow through the pelagic ecosystem, increase our
understanding of pelagic interactions and enhance predictive capacity of fish stock
modeling. However, during 1990–2006, the importance of zooplankton dynamics
and production was somewhat ignored and zooplankton monitoring was excluded
from the national monitoring programs. Recently, however, as a result of drastic
changes in the reproductive success, population dynamics, and physical condition of
many commercially important fish species, such as herring, sprat, cod, pike and
perch, there has been a growing interest in the dynamics and production of
zooplankton.
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ASSESSING ZOOPLANKTON GROWTH AND
METABOLIC ACTIVITY
Production assessments in continuously reproducing wild populations (such as most
zooplankton; Winberg et al. 1971) includes sampling, identification and counting of
different life stages (Winberg et al. 1971, Runge and Roff 2000), and calculations
based on an estimated or measured growth rate. Consequently, the production
estimate is a function of the growth rate estimate. Although assessment of in situ
growth may help us understand food web structure and dynamics, few such studies
on zooplankton exist. The reason for this is partly the lack of reliable and convenient
methods.
Today, common methods to assess growth include temperature-dependent models,
weight-dependent models, physiological or laboratory-derived budget models,
cohort or artificial cohort weight increase or moulting rate, and (for e.g. copepods
and rotifers) egg production assessment (reviewed by Winberg et al. 1971, and
Runge and Roff 2000). All these methods have shortcomings and their accuracy and
reliability for in situ growth assessment are often questioned. The temperature and
weight dependent models are simplified empirical growth models based on
temperature and/or body weight. The major problems with these models therefore, is
that the independent variables are limited to temperature and/or body weight only,
while other variables, such as food quantity and quality (Kleppel 1993), salinity
(Calliari et al. 2006), and physiological condition (health; e.g., Fahmi and Hussain
2003), age/life stage; Calbet et al. 2000) also may affect zooplankton growth. The
physiological method, on the other hand, which relies on previously determined
relationships between growth and e.g. weight, temperature, food availability,
respiration, and assimilation for in situ extrapolation have other problems. The major
problem, as suggested by Huntley and Lopez (1992) and Huntley (1996) is difficulty
in parameterizing the impact of different variables in the combined physiological
equation. The cohort or artificial cohort weight increase and moulting rate methods
use the dynamics of a single stage, cohort or a whole population to establish weight
increase or moulting rate over time in field sampled specimens incubated in the
laboratory (Runge and Roff 2000). The same rationale is employed in the egg
production method, where egg production in adult females represents the growth
(Runge and Roff 2000). In juvenile copepods, growth consists of somatic growth
(i.e., increase in body-mass and building exoskeleton), while in adults the growth is
generative (i.e., formation of sexual products; Carlotti and Nival 1992). The egg
production method can therefore be used only for assessing production in adult
female copepods, while the cohort or artificial cohort weight increase or moulting
rate methods should be used to assess growth in juvenile life stages. However,
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assuming a constant specific growth over different life stages during non limiting
food conditions, as suggested by Sekiguchi et al. (1980) and tested by e.g. Berggren
et al. (1988), the egg production method can also be used to approximate juvenile
growth. This assumption and therefore applicability of the egg production method
for the copepod production assessment has been challenged by many physiologists
(e.g., Richardson and Verheye 1999, Calbet et al. 2000). The major drawbacks with
the egg production and moulting methods are related to the risk of introducing
artifacts due to handling of the animals and to the enormous amount of labor
inherent to the methods. Nevertheless, the egg production method is generally the
least laborious of these methods, and is probably the most employed method for
direct measurement of copepod growth in field and laboratory studies (Runge and
Roff 2000).
Although direct growth measurements are crucial for production assessments, other
physiological variables are also useful for interpreting the condition and production
status of zooplankton. For example, a number of variables of metabolic activity such
as the rate of which an individual ingest food, egests or excrete non-assimilative
food products, and respire, all give us clues about what might inhibit or enhance
growth (Blažka 1971, Fig. 3).
Ingestion Egestion
AssimilationRespiration
Juvenile growth
(somatic + moulting)
Adult growth
(generative)
Trophic
transfer
Energy
Excretion
Figure 3. Schematic figure of energy flow through a copepod. The shaded boxes represent
variables assayed in paper I and II of this Thesis.
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Of particular interest is the ingestion rate as it sets the upper limit for all
physiological processes including growth (Fig. 3). Although these metabolic
indicators are valuable for understanding key mechanisms of growth-related
responses, the assessment of these variables are by nature as laborious as direct
growth measurements and often difficult to employ in field studies. Therefore,
alternative, easy to employ, yet reliable, methods for direct assessment of in situ
growth and metabolic activity in zooplankton could facilitate the accuracy of
zooplankton production estimates. This, in turn, would improve our ability to
produce more data, which would allow for a better understanding of food web
interactions; a prerequisite for reliable predictions of ecological models including
those evaluating fish feeding conditions.
Using biochemical macromolecules to assess growth and
metabolic activity in zooplankton There is an increasing recognition that biochemical indices can provide a suitable
alternative and/or complement to existing in situ methods for assessment of growth
and physiological condition in zooplankton (Runge and Roff 2000). In general, use
of these indices to assess physiological performance, such as egg production,
somatic growth, ingestion, respiration, and stress, are based on key components of
synthetic and/or metabolic pathways. These pathways are usually either directly or
indirectly linked to cell growth and synthesis of important biological
macromolecules. During recent decades, as a result of significant progress in
analytical methods (Caldarone et al. 2006), analysis of bulk ribonucleic acid (RNA)
has been increasingly used to estimate growth in a variety of small animals,
including cladocerans ( Gorokhova and Kyle 2002, Vrede et al. 2002) and copepods
(Nakata et al. 1994, Wagner et al. 1998). In copepods, the RNA concentration has
proven to be a sensitive indicator of both reproductive (Nakata et al. 1994, Saiz et
al. 1998, Gorokhova 2003, papers I and II) and somatic growth (Wagner et al.
2001), as well as a measure of metabolic activity in response to nutritional
conditions (Wagner et al. 1998, Gorokhova et al. 2007, paper II), salinity stress
(Calliari et al. 2006) and toxic substances (Gardeström et al. 2006). Studies
employing RNA-based indices usually standardize the RNA content of an individual
to either its DNA or protein contents. The underlying rationale for using RNA-based
indices is that RNA concentration, primarily, is a function of ribosome number
correlating with protein synthesis and hence with growth rate (Buckley et al. 1999).
The amount of DNA, on the other hand, is considered semi-constant and may
therefore be an indicator of the cell number, which is a rough estimate of the body
size. The RNA:DNA ratio therefore indicates the amount of RNA per cell. The
RNA:protein ratio reflects the number of ribosomes per amount of protein and hence
the cytoplasmic ribosome concentration (Bremer and Dennis 1996). Moreover, a
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wide range of enzymes, such as the metabolic enzymes trypsin, citrate synthase,
lactate dehydrogenase, phosphofructokinase, and a moulting enzyme, chitobiase,
have been suggested as proxies for somatic growth, and physiological condition in
crustaceans (Mayrand et al. 2000, Sastri and Roff 2000, Lemos et al. 2002, Cullen et
al. 2003). The rationale of using metabolic enzymes is that the activities of these
enzymes are linked to adenosine triphosphate (ATP) production, which is required
for elevated growth. The rationale for using the moulting enzyme activity, on the
other hand, is related to the moulting cycle as a part of somatic growth process in
arthropods. Furthermore, in recent years, another enzymatic indicator of
zooplankton growth based on the activity of the aminoacyl-tRNA synthetases
(AARS) has been introduced and applied for copepod growth analysis (Yebra et al.
2005, paper II). The AARS are a group of enzymes important in catalyzing a critical
step of protein synthesis; i.e. the activation and attachment of amino acids to the
tRNA (Ibba and Söll 2000).
Creating a model to assess in situ egg production rate (paper I)
To produce robust predictive models, relationships between growth/physiological
condition and biochemical indices must be tested and validated before they can be
used for growth assessments of wild populations under varying environmental
conditions. In paper I, we evaluated factors regulating the earlier proposed RNA–
egg production rate (EPR) relationship in Acartia bifilosa (Gorokhova 2003) and
developed a model for in situ EPR assessment. This was done by measuring EPR
and RNA content in individual adult females sampled at geographically distant areas
(station effect) during spring and summer (season effect). We also measured surface
water temperature (T) and prosome length (PL). Multiple linear regressions were
generated to create a model that predicts EPR from RNA content, PL, station,
season, and T. We found that PL, RNA content, and season explained 53% of the
variation in EPR, nearly half of which was explained by RNA content alone. The
significance of season indicates the importance of factors varying with season. If
RNA content and EPR saturate at different food concentrations (as later found in
paper II), it is reasonable to believe that the RNA–EPR relationship is also affected
by food availability and possibly also food quality. Therefore, effect of the season
variable found in paper I could be, at least partially, related to the differences in food
between the seasons. Another factor that varies with season is temperature. Since
surface water temperature, which is a continuous and more precise variable than
season, was measured in this study, the season variable was replaced by the
temperature variable. This replacement did not cause a substantial drop in
explanatory power of the model. The effect of spatial origin (station) on the RNA–
EPR relationship was never significant. This implies that it may be possible to use
this model on the entire Baltic population of A. bifilosa as long as all variables are
within the range of assayed variables in paper I.
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Comparing usefulness of different biomarkers (paper II)
Although many studies have suggested, developed and refined biochemical methods
for assessment of growth and physiological condition, the results are often
contradictory and intercalibrations are much needed (Runge and Roff 2000). In
paper II, using A. bifilosa as a model species, we evaluated the functional response
of EPR, egg viability, ingestion, and respiration rates and four different commonly
used biochemical proxies related to protein synthesis [individual RNA content,
RNA:DNA ratio, RNA:protein ratio, and protein specific AARS activity
(spAARS)], in response to a broad spectrum of food concentrations. Then, a
correlative approach was used to evaluate the linkages between the biochemical
indices and physiological rates and thus the predictive capacity of these indices for
the physiological variables. There were three main findings in this paper: First,
although all variables (except egg viability) increased with increasing food
concentration either linearly (spAARS) or hyperbolically (all other variables), there
were substantial differences in saturating food concentrations among the variables.
Therefore, applicability of biomarkers as proxies of physiological rates should be
restricted to the non-saturated phase of the functional response of either variable,
unless both variables saturate at similar food concentrations. This restriction may
have implications for assessing copepod physiological rates at high food availability,
as during algal blooms. Second, RNA content and RNA:protein ratio were the best
proxies of egg production and ingestion rates, while RNA:DNA ratio and spAARS
activity were less suitable. The superior predictability of RNA content and
RNA:protein ratio is in line with previous findings in this species (Gorokhova
2003). Overall, the best correlation was observed for ingestion rate and RNA
content, a relationship not previously described for this species. Earlier, egg
production was suggested to be a more sensitive indicator of nutritional quality than
RNA:DNA ratios in Acartia tonsa (Speekmann et al. 2006). The strong relationships
between RNA content and ingested food quantity (II) and between EPR and
ingested food quality (Speekmann et al. 2006) confirms the importance of food on
the EPR–RNA relationship as proposed above (page 17). Third, RNA:DNA ratio
and spAARS activity were non-correlating variables, which implies that they could
be used jointly as co-variables in multiple regression models to predict ingestion
rate. In theory, joint use of non-correlating biochemical indices could be beneficial
to improve the predictive ability of models for growth and physiological condition,
but this needs to be explored further. Therefore, by investigating other biochemical
indices theoretically related to growth and metabolic pathways, but uncorrelated to
protein synthesis (e.g., compounds or rates related to ATP or DNA synthesis), we
may find other co-variables that can be used in such combined models.
19
Applicability of RNA-based models for in situ growth assessments in
the Baltic Sea
To better understand production processes in the Baltic Sea, knowledge of factors
governing zooplankton production is a prerequisite. Therefore, development of
robust models for growth assessment in zooplankton is an important issue for many
zooplanktologists. The findings of paper I and II provide good evidence that
individual RNA content can be used to assess in situ EPR in the common Baltic
copepod A. bifilosa, but much work still needs to be done before we can use this
approach to assess growth of the entire zooplankton community. The EPR-method
assumes that growth rates are the same for all copepod developmental stages, an
assumption proved to be incorrect when available food is not equally suitable for
juveniles and adults (Richardson and Verheye 1999, Calbet et al. 2000). In the
calanoid copepod Centropages typicus, this was especially pronounced when
copepods were feeding on particles larger than 5 µm (Calbet et al. 2000). For
production assessment of the entire zooplankton community, the growth–RNA
relationship for each species and each developmental stage needs to be defined.
Nevertheless, the model(s) proposed in paper I can be used “as is” to give a rough
measure of the productivity status of the zooplankton community. Moreover, our
findings reported in papers I and II suggest that RNA-based models for growth
assessment of A. bifilosa could be used over larger geographical areas, as long as
abiotic (e.g., temperature and salinity) and biotic (e.g., body size, food availability,
and food quality) factors are accounted for. Therefore, robust models of this kind
may be implemented in diverse monitoring programs, for construction of
productivity maps of fish prey. However, further area of concern with respect to
copepod population recruitment is that the EPR model described in paper I does not
discriminate between viable or total EPR, which has crucial implications for
estimating population recruitment. Yet, as shown in paper II, the proportion of
viable eggs was generally high and not related to total EPR or RNA levels. Indeed,
in our further study, that evaluated how egg viability is reflected in individual RNA
content of field collected Acartia tonsa females, no significant effect of egg viability
on the EPR–RNA relationship was observed (Hogfors et al., in prep.). On the other
hand, as egg viability decrease has often been observed in copepods feeding on
diatoms (Ianora et al. 2003), while our copepods were fed with a green algae
(Tetraselmis suecica, paper II) or ambient summer plankton (Hogfors et al., in
prep.), this needs further experimental studies with other prey. In the Baltic Sea,
diatoms are very abundant during spring blooms and therefore, caution should be
taken when inferring recruitment from biochemical proxies during diatom blooms,
in line with the recommendation to restrict use of biochemical assays for growth
assessment to unsaturated feeding conditions (paper II).
20
QUANTITY – QUALITY
Not only the quantity of zooplankton (addressed in papers I and II), but also their
nutritional quality are essential for determining feeding conditions for higher trophic
levels, such as zooplanktivorous fish and, consecutively, predatory fish, humans,
and seabirds in the Baltic Sea. An altered nutritional quality for zooplanktivorous
fish can result from an altered zooplankton community composition, as different
species may have different macro- and micronutrient contents (Persson and Vrede
2006). However, it may also reflect alterations in nutritional quality of certain taxa.
Effects of nutritional deficiencies in fish diet have been addressed earlier by many
studies in different aquatic systems, including the Baltic Sea. For example, changes
in the diet composition, and thus altered nutritional value, have been suggested to be
responsible for the decrease in the weight-at-age of Baltic sprat and herring (e.g.,
Raid and Lankov 1995, Rönkkönen et al. 2004). Although it is not clear why some
prey species seem to enhance fish growth, it may be related to species specific
variations in C:N:P ratio (Walve and Larsson 1999), their ability to store fatty acids
(Persson and Vrede 2006) or other biochemical differences.
Carotenoids in the food web There are many aspects of food quality, besides the energetic value, and fatty acid
and amino acid composition; these aspects include quantities and composition of
other essential macromolecules, trace elements, and minerals. During the last
decades, carotenoid pigments have been recognized to play an important part of the
food quality in aquatic food webs (Pettersson and Lignell 1999, Liñán-Cabello et al.
2002, Vuori and Nikinmaa 2007). Apart from being pigments necessary for
photoprotection, carotenoids have also showed characteristics of being antioxidants
and vitamin A precursors (Schiedt et al. 1985, Liñán-Cabello et al. 2002). The
carotenoid astaxanthin is acknowledged to be one of the strongest naturally existing
antioxidants (Edge et al. 1997), and has proved to be an efficient protector against
UVA and UVB radiation (Davenport et al. 2004). It is abundant in many marine
animals, but seems to be particularly important for crustaceans and salmonids
(Matsuno 1989). In the Baltic Sea, failed reproduction in salmon (Salmo salar) has,
at least partly, been associated with an early mortality syndrome (M74). This disease
seems to be connected with low levels of astaxanthin (Amcoff et al. 1998) and
thiamine (Pettersson and Lignell 1999) in the eggs and fry of affected females. Low
thiamine levels in Baltic salmon have been suggested to indicate an oxidative stress
(Vuori and Nikinmaa 2007), a condition that was possible to cure with an
astaxanthin enriched diet (Nakano et al. 1995). The diet of Baltic Salmon was,
however, very similar before any signs of M74 was seen and during the period when
this symptom peaked (Hansson et al. 2001). This suggests that any dietary
21
difference may be related to the quality of the salmon prey (primarily sprat and
herring).
In nature, astaxanthin is almost exclusively synthesized by animals from carotenoid
precursors, mainly β-carotene and zetaxanthin (Katayama et al. 1973, Foss et al.
1987) that must be supplied to the animals. In the Baltic Sea pelagic ecosystem, as
in most marine pelagic systems, copepods are likely to be the major producers of
astaxanthin. The astaxanthin produced by copepods is transferred to the higher
trophic levels. Of particular interest, therefore, are factors affecting astaxanthin
content in copepods.
Factors affecting astaxanthin levels in copepods
As astaxanthin production in copepods is dependent on the availability of precursors
in the diet, some studies dealing with factors affecting astaxanthin content in
copepods have focused on diet effects (e.g., Andersson et al. 2003, Van Nieuwburg
et al. 2005). Andersson et al. (2003) found the astaxanthin content per copepod to
increase at higher phytoplankton biomass and diversity, while it decreased at lower
phytoplankton biomass or high phytoplankton biomass dominated by diatoms. Van
Nieuwburg et al. (2005) on the other hand found a decreased astaxanthin content in
copepods feeding in nutrient (NP or NPSi) enriched macrocosms as compared to the
natural concentrations and proposed the lack of need for copepod photoprotection in
the higher algal biomass (and therefore lower water transparency) to be a plausible
explanation for the latter result. Moreover, they found no difference in astaxanthin
content per copepod between the two enriched treatments, dominated by different
algae. Other studies have looked at the importance of algae in starved/fed
experiments and found a positive relationship between availability of algae and
copepod astaxanthin content (Davenport et al. 2004, Sommer et al. 2006). Also, as
astaxanthin is recognized as a strong antioxidant with photoprotective properties, the
effect of light on astaxanthin production has been investigated. These studies found
that light was not a prerequisite for astaxanthin production (Davenport et al. 2004,
Sommer et al. 2006), although it seemed to enhance the astaxanthin content in
copepods (Sommer et al. 2006). Therefore, it is proposed that the main function of
astaxanthin is to improve the antioxidant protection of storage lipids, also in
situations where photoprotection is not required (Sommer et al. 2006). If this is the
case, astaxanthin content should be more strongly regulated by food intake than by
light.
Copepod astaxanthin content in relation to food concentration (paper III)
Although no study has investigated the response curve of astaxanthin content to
elevated food concentrations, it is reasonable to believe that an increased food intake
will contribute to a higher supply of astaxanthin precursors, which will support
22
higher astaxanthin production, and thus a higher astaxanthin content, at least up to a
saturation point. In paper III, we used A. bifilosa as a model species, to investigate
the effect of feeding activity on individual astaxanthin levels. In adult female
copepods exposed to a broad range of food concentrations, ingestion rate and EPR
along with astaxanthin content were measured. While both EPR and ingestion rate
increased with increasing food concentration, as expected, a different response was
observed for the astaxanthin content: It increased in concert with increasing food
concentrations up to 150 µg C L-1
, however at the two highest food concentrations
(600 and 1200 µg C L-1
), the astaxanthin content dropped significantly and became
similar to the concentrations observed in starved individuals. The decrease was
significant, even after adjustment for astaxanthin deposition in eggs, and coincided
with lower carbon assimilation efficiencies at these food concentrations. Although
the mechanisms of this decrease need further investigation, we propose that the
reduced astaxanthin accumulation resulted from reduced uptake of precursors,
because of decreased assimilation efficiency at the higher feeding rates. However,
irrespective of the mechanism, the ecological consequences of this phenomenon are
extremely relevant to eutrophication and fish feeding conditions. Indeed, in a
eutrophicated system, copepods of poor nutritional quality (with respect to
astaxanthin content) may reproduce at high rates and sustain high population
densities. Therefore, although this high zooplankton production may be considered
positive for the fish feeding conditions, the low quality of the prey may cause
astaxanthin deficiency in the predators. These findings also suggest ecological
effects on a seasonal scale as copepod quality (but not quantity) may decline during
algal blooms or in nutrient enriched environments with high productivity. In line
with this, in previous studies (Van Nieuwburg et al. 2005), reduced astaxanthin
content in copepods exposed to high food concentrations (and therefore low water
transparency) was proposed to be a result of a lowered demand for photoprotection.
An alternative explanation to the observed decrease could be the same physiological
mechanisms as those proposed in our study (III). However, further experiments
investigating these responses using other zooplankton and algal species, in mono
and mixed cultures, would greatly improve our understanding of factors affecting
qualitative aspects of food web interactions. Furthermore, it is plausible that other
important biochemical compounds for zooplankton and their predators (such as
other carotenoids, Liñán-Cabello et al. 2002, Sies and Stahl 2005; fatty acids, Kainz
et al. 2004; vitamins and microelements, Guillaume et al. 2001) may exhibit the
same response as seen for astaxanthin in paper III, thus exerting additional negative
effects on diet quality for the higher trophic levels. Therefore, response of other
essential elements and compounds to food concentration as well as ecological effect
of these responses need to be carefully investigated in controlled laboratory
experiments as well as in field surveys.
23
THE ROLE OF NON-INDIGENOUS ZOOPLANKTON
IN THE BALTIC SEA PELAGIC FOOD WEB
The Baltic Sea ecosystem, like any other aquatic ecosystem of low salinity, low
biodiversity and few specialized niches, is very vulnerable to introductions of non-
indigenous species, NIS (Carlton and Geller 1993). Today, about 30 NIS are
recorded in the Swedish waters of the Baltic Sea (Anon. 2009), including the
mesozooplankton species: Acartia tonsa (Copepoda), Cercopagis pengoi
(Cladocera), and Evadne anonyx (Cladocera) (Anon. 2009). In the eastern parts of
the Baltic Sea, the cladoceran Cornigerius maeoticus maeoticus, has also been
recently recorded (Rodionova et al. 2005). Since the biology of this species
resembles that of E. anonyx and C. pengoi (Rivier 1998), a further spread of C. m.
maeoticus in the Baltic Sea is likely.
The magnitude and mechanisms and thus the consequences of these introductions on
the native Baltic Sea food web are generally poorly understood. However, it could
be hypothesized that introduced predatory zooplankton species (such as C. pengoi,
E. anonyx and C. m. maeoticus; Rivier 1998) will alter the feeding conditions for
zooplanktivorous fish, either by competing with fish for food or by becoming an
additional prey for fish. In the Baltic Sea, most studies investigating the ecological
impact of these planktonic NIS have so far focused almost exclusively on C. pengoi,
as it was introduced much earlier than the other two cladocerans, and as it is still the
only planktonic NIS present in different sea areas every summer in substantial
quantities. However, it cannot be ruled out that the other newcomers will increase
their abundance with time and that already today their food web effects, albeit
perhaps less pronounced, are similar to those of C. pengoi, because of the
similarities in feeding biology of these species (Rivier 1998).
C. pengoi as a prey (paper IV) In the Gulf of Riga, Ojaveer and Lumberg (1995) have found herring (but not
young-of-the-year, YOY, herring) to feed on C. pengoi to a great extent. This has
also been reported from the northern Gulf of Finland, where C. pengoi became a
main food source from August to mid October for larger herring (Antsulevich and
Välipakka 2000). In the Gulf of Riga, other fish such as three-spined stickleback,
nine-spined stickleback and smelt were found to feed somewhat on C. pengoi, while
sprat, white bream and bleak were not (Ojaveer and Lumberg 1995, Ojaveer et al.
2004).
In paper IV, we investigated feeding of herring and sprat, the two most common
zooplanktivorous fish in the Baltic Sea, on C. pengoi. Contribution of C. pengoi to
24
fish diet was estimated by examining stomach content of fish from a coastal area of
the northern Baltic proper (Himmerfjärden Bay). The stomach content was then
compared to the ambient zooplankton community abundance and structure to
estimate prey selectivity. We found that both herring (5.2 to 25.2 cm) and sprat (5.7
to 11.6 cm) feed on C. pengoi. Overall, the proportion of fish with C. pengoi in the
stomach was 70 % and 61 % for sprat and herring, respectively. Moreover, herring
proved to become more selective for C. pengoi with increasing size. The fact that
YOY of both herring and sprat feed on C. pengoi, indicates that this prey is not too
large for fish as small as 5 cm long, as suggested earlier (Ojaveer and Lumberg
1995, Bushnoe et al. 2003). These results imply that trophic position of
zooplanktivorous fish has shifted up as a result of the invasion, a conclusion later
supported by Gorokhova et al. (2005). They used stable isotopes of C and N to
elucidate food web interactions between C. pengoi and potential prey and predators
and found that since the introduction of C. pengoi into the food web, the trophic
position of YOY herring has shifted from 2.6 to 3.4. Also, even smaller fish such as
the sand goby (1.4 cm; Ehrenberg 2008), sticklebacks (3.2 cm; Ojaveer et al. 2004),
and herring (4.1 cm; Ojaveer et al. 2004) have now been reported to feed on C.
pengoi. Therefore, it seems reasonable to believe that many other fish species at
most ages can utilize C. pengoi as a prey. Moreover, in addition to the impact that C.
pengoi may have on the diet of zooplanktivorous fish, it may also influence the diet
of other zooplanktivores, such as mysids. Indeed, Baltic mysids (Neomysis integer,
Mysis mixta, and M. relicta) were reported to feed on C. pengoi (Gorokhova 2006,
Gorokhova and Lehtiniemi 2007). This variety of predators indicates that C. pengoi
is well integrated into the Baltic Sea pelagic food web. However, whether this
actually contributes positively to the overall availability of prey for e.g. fish is
dependent on whether C. pengoi competes with fish for the same prey or not.
C. pengoi as a predator (paper V) As C. pengoi is zooplanktivorous, it is important to know its diet and prey
preferences, in order to evaluate its effects on the feeding conditions of
zooplanktivorous fish.
In the eastern Gulf of Finland, the impact of C. pengoi predation on the zooplankton
community has been evaluated and monitored (Telesh et al. 2001, Litvinchuk and
Telesh 2006). Their results, suggest that since the introduction of C. pengoi to the
area, its predation pressure on other zooplankton such as herbivores and suspension
feeders has increased exponentially. However, the data set used in these studies is
inadequate with respect to sampling frequency, and therefore modeling output is
questionable. In another study performed in the Gulf of Finland, correlative statistics
on field data suggested that predation by C. pengoi may affect seasonal dynamics
and/or spatial distributions of native cladocerans and rotifers (Põllumäe and Kotta
25
2007). In particular, Bosmina maritima tended to stay below the thermocline when
C. pengoi was abundant in surface waters. This was suggested by the authors to be a
predator avoidance response triggered by direct predation of C. pengoi on B.
maritima. Moreover, the authors suggested that a positive correlation observed
between abundances of B. maritima and C. pengoi may indicate a beneficial effect
of C. pengoi on B. maritima. This was proposed to be a result of C. pengoi preying
on other species that compete with B. maritima, such as Pleopsis polyphemoides and
Evadne nordmanni (as indicated by their negative correlations with C. pengoi).
Moreover, in the Gulf of Riga, the abundance and phenology of B. maritima has
changed after the introduction of C. pengoi (Ojaveer et al. 2004). The B. maritima
population has decreased and disappears from the zooplankton community several
weeks earlier than before the invasion (Ojaveer et al. 2004). A shift in the phenology
was also apparent in the copepod E. affinis who started to develop about three weeks
earlier following the introduction of C. pengoi (Ojaveer et al. 2004). Experimentally
determined feeding rates on E. affinis support the proposed negative impact of C.
pengoi on the E. affinis population (Lehtiniemi and Gorokhova 2008). As indicated
by the studies above, most research on C. pengoi feeding in the Baltic Sea pelagic
food web has employed correlative statistics on field data. When interpreting
correlative statistics it is important to remember that it only verifies co-varying
variables rather than expresses a dependency relationship. As there is a risk that two
variables, although independent of each other, co-vary as a result of another/or
several other external forces, the credibility of correlations to investigate
dependency relationships is fairly weak. Nevertheless, these studies suggest
plausible interactions and indicate what kinds of data are needed to verify these
interactions and increase our understanding of the impact of C. pengoi in the Baltic
Sea pelagic food web.
Stable isotope compositions can be used to assign trophic positions in food webs,
thus contributing to understanding energy flows and ecological relationships. This
approach employs relative concentrations of C and N isotopes in organisms to assess
dietary connections. The ratio between different isotopes of carbon and nitrogen
differs between organisms and their diets because of a slight selective retention of
the heavy isotope and excretion of the lighter isotope. As a result, organisms tend to
become enriched in heavy isotopes as compared with their food (Owens 1987). In
the Baltic Sea, this approach was used to evaluate food web interactions after the
introduction of C. pengoi (Gorokhova et al. 2005). It was concluded that
mesozooplankton (mainly copepodites) where the main prey of larger C. pengoi
while smaller C. pengoi fed equally much on microzooplankton (mainly rotifers and
nauplii) and mesozooplankton.
26
In paper V, we further investigated prey preferences of Cercopagis pengoi during
June–August using stable isotope analysis. The study was carried out in a coastal
area of the northern Baltic proper (Himmerfjärden Bay). Diet composition of C.
pengoi was determined from stable isotope signatures of the predator and possible
prey organisms, using two approaches: IsoSource mixing models (Phillips and
Gregg 2003) and temporal tracking of prey (Melville and Connolly 2003). In
parallel, zooplankton composition and abundance were analyzed to estimate
selectivity for different zooplankton prey. On a seasonal basis, the main contributors
to C. pengoi diet were copepods Acartia spp. and E. affinis, while importance of
cladocerans and microzooplankton was less apparent. C. pengoi behaves, overall, as
an opportunistic generalist predator, with a nutrition substantially overlapping that
of commercially important zooplanktivorous fish.
The overall impact of cladoceran NIS in the Baltic Sea
pelagic food web Earlier analysis on stable isotopes, conducted in the same area as our study (paper
V), suggested that C. pengoi feed, to a large extent, on copepods (i.e., the same food
items as YOY herring; Gorokhova et al. 2005). We found that copepods indeed
dominate in the diet of C. pengoi (paper V). Therefore, as not only YOY herring but
also other zooplanktivorous fish (e.g. sprat) at different age feed intensely on
copepods (e.g., Arrhenius 1996, Voss et al. 2003); this indicates a potential food
competition between C. pengoi and fish. However, C. pengoi appears to select
positively for podonids and also occasionally for microzooplankton, i.e. prey which
is less preferred by fish. Thus, during periods of low copepod abundance C. pengoi
may provide an energy link between lower trophic levels and fish.
It is clear that C. pengoi is well incorporated into the Baltic Sea pelagic food web,
where it acts as both an opportunistic predator (paper V) and a prey for fish (paper
IV) and mysids (Gorokhova 2006, Gorokhova and Lehtiniemi 2007), with many
complex interactions (Fig. 4). However, the overall effect of C. pengoi on fish
feeding conditions is still poorly understood. By integrating these results on fish
(paper IV) and C. pengoi (paper V) diets with field data on C. pengoi, fish and
zooplankton abundances collected in concert, the strength and outcome of the
interactions between these groups could be addressed in trophic interactions models.
Nevertheless, it is quite clear that C. pengoi alters the quantity and composition of
zooplankton available for zooplanktivores. It has, however, been suggested that
since C. pengoi, in the Baltic Sea, is only temporarily present in the water column
(from mid- to late summer) its overall impact will be limited to this period (Orlova
et al. 2006). Although this in principle might be true, it is important to acknowledge
that this short-term impact during summer may leave traces in the food web, which
27
may be significant all year round. This may be the case if the presence of C. pengoi
alters the feeding condition for fish and/or impacts the phenology of zooplankton, as
suggested for B. maritima (Ojaveer et al. 2004).
Zooplanktivorous fish Mysids
C. pengoi
Cladocerans (other
than C. pengoi)
Rotifers + copepod nauplii
Copepodites
1
IV
V
2
V
IV IV
V
IV
4
5
4
3
Figure 4. Pelagic food web interactions involving C. pengoi in the Baltic Sea. This schematic
food web is not complete and created mainly to visualize the findings of this Thesis. Arrows
represent confirmed interactions, and the number refers to the source of information; 1: Rivier
1998, 2: Gorokhova and Lehtiniemi 2007, 3: Arrhenius 1996, 4: Barz and Hirche 2009, 5:
Viherluoto and Viitasalo 2001. The Roman numerals represent papers in this Thesis.
The impact of the other newly introduced cladoceran species in the Baltic Sea, C. m.
maeoticus and E. anonyx remains to be investigated to see if these species will affect
the food web in similar ways, or if they will have other impacts. Moreover, the
unexpected (due to its lack of invasion history and previously described salinity
tolerances) successful establishment of E. anonyx into the Baltic Sea may indicate
that other common Ponto-Caspian onychopods (e.g. Podonevadne trigona,
Podonevadne camptonyx, Podonevadne angusta, Polyphemus exiguous and Evadne
prolongata) may exert an additional invasion threat towards the Baltic Sea (Panov et
al. 2007). Furthermore, due to prevailing climatic change, the establishment and
population abundance development of these species, originating from warmer
climate, may be reinforced in the future.
28
CONCLUSIVE REMARKS AND FUTURE
PERSPECTIVES
In the first two papers (I, II), we found that RNA content is a suitable biomarker for
assessing growth (expressed as EPR) in adult Acartia bifilosa females. The proposed
predictive model(s) for EPR assessment (I) could, therefore, as is, easily be
implemented in monitoring programs to assess zooplankton production, i.e. food
availability for zooplanktivores such as fish. However, to receive a more complete
picture of zooplankton availability for zooplanktivores, similar models should be
developed for other important zooplankton species and expanded to include juvenile
stages. Moreover, in order to use the model on a larger geographical scale (i.e,. the
entire Baltic Sea), the effect of salinity on the EPR–RNA relationship needs to be
tested and accounted for. This would greatly improve the usefulness of the model
because it would allow for productivity comparisons between different sub-areas of
the Baltic Sea. This information will help us understand variations in productivity
and recruitment success between different sub-populations of Baltic fish.
In paper III, we found that high food intake in copepods may lead to decreased
astaxanthin content. There may, however, be other factors, such as temperature,
salinity, light, and presence of algal or man-made toxins, which may further
modulate astaxanthin content in zooplankton. How, and to what extent, these factors
may affect astaxanthin content in copepods needs to be further explored. Moreover,
to fully understand factors affecting the quality of zooplankton as prey, the proposed
studies should also focus on other essential substances in a broader spectrum of
species.
Papers dealing with quantitative (I, II) and qualitative (III) aspects of copepod
production emphasize the importance of food quality and food quantity available for
the copepods. In the Baltic Sea, under conditions prevailing during a spring bloom
(i.e., high food concentrations and dominance of diatom species), the proposed
EPR–RNA model(s) for predicting A. bifilosa recruitment (paper I) may be less
reliable, due to the high food concentration (paper II) and the possible effects of
diatoms on egg viability (Ianora et al. 2003). Moreover, at high algal concentrations,
a decreased quality of the copepods in terms of astaxanthin concentration might be
possible (paper III). It is necessary to validate these findings in field as it will
impact the feeding conditions for zooplanktivorous fish.
Cercopagis pengoi is well incorporated into the Baltic Sea pelagic food web, acting
as both an opportunistic predator (paper V) and a prey for zooplanktivorous fish
(paper IV). Although the Baltic Sea holds a relatively small number of species,
29
which reduces the number of possible interactions, the trophic linkages of C. pengoi
are numerous (Fig. 4) and rather complex. Therefore, the overall effects of the C.
pengoi introduction on fish feeding conditions are likely to vary both seasonally and
regionally, depending on the food web structure. To evaluate these effects, long term
data for zooplankton, C. pengoi, and fish abundance/biomass that cover periods
before and after invasion should be integrated with the diet data (Holmborn et al., in
prep.).
In previous studies, correlation statistics on field data has been used extensively to
investigate food web interactions involving C. pengoi. We used fish stomach
analysis (paper IV) and stable isotope approach (paper V) to further understand
these interactions. Although IsoSource mixing models, especially combined with
temporal tracking of prey (as used in paper V), using stable isotope data provide
stronger proof of actual interactions between species in food webs than do
correlation studies, there are still some uncertainties with these methods. Therefore,
stomach analysis of C. pengoi using genetic markers of potential prey may be an
additional and even more reliable way to define and quantify these interactions.
The findings of this Thesis contribute to increase our understanding of processes
important for assessment and evaluation of fish feeding conditions and trophic links
between zooplankton and fish. This knowledge is crucial to make informed
ecosystem based management decisions concerning the Baltic Sea fisheries; an
approach that hopefully will improve and secure future harvest of Baltic sea-food.
Moreover, the knowledge gained in this Thesis will also help us identify and
understand future impact on the ecosystem caused by e.g. prevailing climate change,
eutrophication and introductions of non-indigenous species.
30
ACKNOWLEDGEMENTS
As Isaac Newton so neatly put it; “If I have seen further it is by standing on the
shoulders of giants”. In my case those giants are personified by my dear supervisors
Ass. Prof. Elena Gorokhova and Prof. Sture Hansson. Elena, thank you for countless
hours of interesting discussions during which you shared your vast knowledge with
me. Thanks also for using your sharp eye, excellent research skills, and scientific
curiosity to give constructive criticism and feedback on my work and for your ability
to always, and I mean always, be available for my questions and ideas, big or small.
Thank you also for facing everything with a smile, it made everything a lot easier!
It´s been great fun working with you and I hope the future will bring more
opportunities to work together. Sture, thank you for believing in me and for
introducing me to the department, and Elena, in the first place. Thank you also for
sharing your knowledge on fish ecology and for always encouraging and supporting
me through good and bad times.
Big hug to my amazing co-authors: Kristin Dahlgren (née Lindell), Elena
Gorokhova, Sture Hansson, Hedvig Hogfors, Claire Holeton, and Per Holliland.
Special thanks to the “copepod girls”; you made the most intense and productive
week of my PhD a great memory for life. I never knew it could be that fun to work
endless hours in the middle of the night with very tiny crustaceans! Thanks also to
Lisa Kosinkova, and Karolina Eriksson-Gonzales for various assistance in the
laboratory.
To all colleagues and friends at the Department of Systems Ecology – thank you for
creating a warm and productive atmosphere. Special thanks to my fellow PhD-
students. Thanks also to my former room-mates Lisa Almesjö and Marc Andersen
Borg for their patience over the years. I would also like to acknowledge the help I
have received from the staff at the chemistry laboratory. A special thanks to Berndt
Abrahamsson, Leif Lundgren, Stefan Svensson, Svante Nyberg, and Ulf Larsson,
who are all involved in the zooplankton monitoring. I would also like to
acknowledge the administrative staff that makes the whole research machine work
smoothly. Moreover, thanks to Börje Larsson, who caught all the fish for stomach
analysis, and Magnus Petersson, who kindly introduced me to methodological issues
concerning fish stomach analysis. Many thanks also to Jan-Olov Persson for
interesting discussions concerning statistics. Staff and colleagues at Tvärminne
Zoological Station (Finland) and Askö Field Station, thank you for everything! Also,
thanks to all friends and colleagues who challenged me in the weekly adventures
taking place in the floor-ball court. You gave me energy to tackle the work week! A
special thanks to Helena for introducing me to the happening of the week!
31
Jonas, you are the love of my life, my family, my friend and my steady rock. I know
that I will always have you there to pull me back up (or bring me back down) when
the road gets bumpy, and I know that by experience ;-). Thank you for your loving
support and for your way of always putting my scientific defeats in perspective .
Dear mum and dad, thank you for always supporting me and for encouraging me to
follow my own path. Theres, my beloved sister, thank you for all your love and
support. Thomas, Janice, Tilda, and Albin, thank you for making life happier and for
preparing me for an alternative career (SingStar® )! Thanks also to all other
friends and relatives who have supported me, you know who you are!
The work within this Thesis was kindly funded by: The Swedish Research Council
for Environment, Agricultural Sciences and Spatial Planning (Formas); Göte
Borgströms foundation; EU (through Swedish Board of Fisheries); the World Wide
Foundation (WWF); the Swedish Environmental Protection Agency
(Naturvårdsverket, through AquAliens and the Swedish National Monitoring
program); Walter and Andrée de Nottbecks foundation (Finland); Stockholm Marine
Research Centre (SMF); and the Royal Swedish Academy of Agriculture and
Forestry (KSLA).
32
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