Download Studies on Baltic Sea mysids Martin Ogonowski Department of Systems Ecology

Studies on Baltic Sea mysids
Martin Ogonowski
Department of Systems Ecology
Stockholm University
Doctoral thesis in Marine Ecology
Martin Ogonowski, [email protected]
Department of Systems Ecology
Stockholm University
SE-106 91 Stockholm, Sweden
©Martin Ogonowski, Stockholm 2012
ISBN 978-91-7447-510-4
Printed in Sweden by US-AB, Stockholm 2012
Distributor: Department of Systems Ecology, Stockholm University
Cover and chapter dividers: ©Ruggero Maramotti
Abstract
Mysid shrimps (Mysidacea, Crustacea) are efficient zooplanktivores in both marine and
freshwater systems as well as lipid rich prey for many species of fish. Although some efforts
have been made to study the role of mysids in the Baltic Sea, very few studies have been
carried out in recent time and there are still knowledge gaps regarding various aspects of
mysid ecology. This thesis aims to explore some of these gaps by covering a mixture of
topics.
Using multifrequency hydroacoustics we explored the possibility to separate mysids from
fish echoes and successfully established a promising and effective method for obtaining
mysid abundance/biomass estimates (paper I). An investigation of the current mysid
community in a coastal area of the northern Baltic proper (paper II) demonstrated that the
formerly dominant, pelagic mysid Mysis mixta had decreased substantially (~50%) in favor
for phytoplanktivorous, juvenile Neomysis integer and Mysis relicta sp.
By examining different aspects of mysid behavior, we studied the vertical size
distribution of mysids in the field and found that size increased with depth/declining light,
irrespective of temperature; indicating that their vertical size distribution primarily is a
response to predation (paper II). In paper III, a combination of ecological and genetic
markers was used to investigate intraspecific differences in migratory tendency. Both marker
types indicated that some part of the Mysis salemaai population is sedentary on the bottom
and that this strategy is a phenotypically plastic but persistent trait, analogous to the partial
migrations seen in many birds and fishes.
In paper IV a temperature and weight specific respiration model was developed for the
littoral Praunus flexuosus. Routine respiration was moreover elevated by post-prandial effects
(specific dynamic action) for longer times than previously suggested. Consequently, ignoring
such effects could significantly bias respiration measurements.
Keywords: Mysids, hydroacoustics, Baltic Sea, abundance, stable isotopes, specific dynamic
action (SDA), diel vertical migration, partial migration, trophic interactions, physiology,
benthic-pelagic coupling, protein:DNA, C:N ratio, genetic structure.
Contents
1. List of papers .......................................................................................................................... 5 2. Contribution to papers ............................................................................................................ 5 3. Introduction ............................................................................................................................ 6 3.1 Objectives ......................................................................................................................... 7 4. Background ............................................................................................................................ 8 4.1 Distribution and habitat choice ........................................................................................ 8 4.2 Diet ................................................................................................................................... 9 4.2.1 Mysis relicta/Mysis salemaai .................................................................................. 10 4.2.2 Mysis mixta .............................................................................................................. 10 4.2.3 Neomysis integer/Praunus flexuosus ....................................................................... 10 4.3 Life history and growth .................................................................................................. 11 4.4 Migration patterns .......................................................................................................... 12 4.4.1 Effects of Light ........................................................................................................ 13 4.4.2 Vertical size distribution ......................................................................................... 14 4.4.3 Temperature ............................................................................................................ 14 4.4.4 Chemical cues ......................................................................................................... 15 4.4.5 Niche differentiation and partial migration ............................................................ 15 4.6 Bioenergetics .................................................................................................................. 16 4.7 Abundance ...................................................................................................................... 17 4.7.1 Sampling methods ................................................................................................... 18 4.7.2 Hydroacoustics ........................................................................................................ 18 5. Summary of papers............................................................................................................... 20 6. Conclusions .......................................................................................................................... 22 7. Acknowledgments ................................................................................................................ 24 8. References ............................................................................................................................ 25 4
1. List of papers
I
Axenrot, T., Ogonowski, M., Sandström, A. and Didrikas, T. 2009 Multifrequency
discrimination of fish and mysids. ICES Journal of Marine Science 66: 1106–1110.
II
Ogonowski, M., Hansson, S. and Duberg, J. 2012 Status and vertical size distributions
of a pelagic mysid community in the northern Baltic proper (accepted for publication
in Boreal Environment Research within a year).
III
Ogonowski, M., Duberg, J., Hansson, S. and Gorokhova, E. 2012 Persistent lack of
diel vertical migration in a pelagic mysid population –– a case of partial migration
(Unpublished manuscript)
IV
Ogonowski, M., Andersson, K. and Hansson, S. 2012 A weight and temperature
dependent model of respiration in Praunus flexuosus (Crustacea, Mysidacea). (Journal
of Plankton Research, in–press).
2. Contribution to papers
I
I planned the study, collected field samples, and performed data analysis, all in close
collaboration with the co-authors.
II
I planned the study in collaboration with Sture Hansson. I collected and prepared all
data except for isotopic samples (Jon Duberg). I performed all the data analyses and I
wrote the manuscript in close collaboration with SH.
III
I formulated the hypotheses and designed the study together with Elena Gorokhova
and SH. JD and I conducted the field work. JD generated stable isotope data, EG and I
performed molecular analyses. I performed statistical analyses and wrote the
manuscript in close collaboration with the co-authors.
IV
I designed the study together with SH and executed the experiments together with
Kristoffer Andersson. I performed the data analysis and wrote the manuscript in
collaboration with the co-authors.
Published and accepted papers are reprinted with kind permission from the publishers: (I, IV)
Oxford University Press and (II) Boreal Environment Research.
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3. Introduction
Many aquatic ecosystems have undergone considerable changes during the last century due to
variations in anthropogenic and environmental factors, with eutrophication and overfishing
being two of the most prominent forces. This in turn, is reflected in changed species
composition at several trophic levels. In the case of the Baltic Sea, top predators such as the
cod (Gadus morhua) that dominated in the 1980s have been depressed to very low levels and
the system was shifted towards being dominated by planktivorous clupeids (herring (Clupea
harengus membras) and sprat (Sprattus sprattus)). At the same time, the mesozooplankton
community changed from being dominated by Pseudocalanus sp. to Temora longicornis and
Acartia spp. (in the Gotland Basin and Gdańsk Deep). Solid explanations for these changes
are lacking but the observed changes in zooplankton species composition have been linked to
a deteriorating condition in herring, which is one of the most important commercial species in
the Baltic Sea (Möllmann et al. 2004; Möllmann et al. 2005). Even though herring
predominantly feed on different species of copepods and cladocerans, older herring consume
substantial amounts of larger invertebrates, such as mysid shrimps (Mysidacea, Crustacea)
(Aneer 1975), and a decrease in large prey like mysids could be one explanation to the
decreased growth in herring (Arrhenius and Hansson 1993). The rapid ongoing increase in the
cod stock (Cardinale and Svedang 2011) will provide good possibilities for studying and
testing these and other hypotheses regarding the role of trophic interactions in the structuring
of the Baltic Sea ecosystem.
Mysids are, due to their high content of polyunsaturated fatty acids (Arts and Johannsson
2003) believed to be an important part of pelagic fishes’ diet during autumn and winter when
other food sources are scarce (Aneer 1980; Lankov and Kukk 2002; Posey and Hines 1991;
Raid and Lankov 1995; Szypula 1985) and by that have the potential of decreasing
overwintering mortality (Snyder and Hennessey 2003). Holliday et al. (1989) further proposed
that a mixed diet was crucial for a good WAA (weight at age) in older herring.
Population dynamics is a cornerstone in ecology. Feeding interactions between species are
often complex and cascading effects between trophic levels are common. In studies of
seasonal population dynamics and trophic interactions in the Baltic pelagic system, mysids
have been only vaguely considered (Möllmann et al. 2004; Möllmann et al. 2005). The reason
for this is the lack of long term data on mysid abundances. Very few continuous monitoring
surveys have been conducted on mysid populations in the Baltic and there is thus little
information on temporal and spatial population dynamics. There is however strong evidence
that mysids have an exceptional potential of structuring zooplankton communities; directly by
consuming zooplankton but also indirectly by competing with herring for food. Rudstam et al.
(1986) found that Mysis mixta could consume 23-51% of net annual zooplankton production
in a coastal area of the Baltic proper. Mathematical models on intra guild predation (IGP)
further suggest that intermediate predators like mysids must be superior competitors for a
shared resource in order to persist in the system (MacLennan and Holliday 1996).
However, recent anecdotic and indirect information suggests a significant decrease in mysid
abundance compared to the 1980’s, in several parts of the Baltic Sea. A recent study by
Dziaduch (2011) reported that the occurrence of mysids (primarily Mysis mixta) had
decreased considerably in both herring and cod stomachs in 2007 and 2008 (southern Baltic
Sea); from being a very important food item during the 1980s and early 1990s to a minor
component in 2007 and 2008. Möllmann et al. (2005) also observed a steady decrease in
mysid biomass in herring stomachs, during autumn, from 1987 and onwards. This observation
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overlaps with the demise of the cod stock, the low WAA of herring and the increase in sprat
stocks.
Since mysids play such a significant role in the Baltic food-web it is important to understand
how, when and by which factors fish and mysids interact with each other. Despite a fair
understanding of general mysid ecology, most knowledge is based on experimental studies
and time series data on abundances and biomass are lacking due to sampling difficulties
associated with patchy distributions and gear avoidance during day-time; thereby making it
difficult to accurately assess long-term population dynamics and food-web functions.
3.1 Objectives
This thesis, aims to fill some of the current gaps in mysid ecology by covering a wide range of
topics. A fundamental step towards a better understanding of food-web interactions is access
to reliable data on distributions and abundances. In paper I, we investigated the possibilities
of a novel technique which may provide such data efficiently; namely multifrequency
hydroacoustics. Sonar technology has traditionally been used for the study of fish populations
since it covers large areas effectively and is a non-invasive method, minimizing bias common
to different types of towed gear.
With their swim bladder, fish are efficient reflectors of sound, but recent advances in
hardware development and post-processing software have made it possible to roughly
distinguish other groups of organisms aside from fish. This may be achieved by combining
echoes from different frequencies, thereby producing “finger prints” of different organisms
such as zooplankton, mysids and fish. The study was conducted in Lake Vättern, the second
largest lake in Sweden, which hosts a similar composition of functional groups as the Baltic
Sea, including mysids and planktivorous, pelagic fish.
Although this technique provides extensive improvements on biomass estimates it relies on
known target strengths (the strength of the received echo, TS) of individual mysids for
abundance estimation. Since TS is more or less proportional to the size of objects, it is
important to understand how, when and where different sizes are distributed in the water
column. For this reason, efforts were made to decipher the underlying factors that govern
vertical size distributions of mysids (paper II). Moreover, since recent mysid abundance data
is lacking and the Baltic Sea in many ways has changed since the last mysid investigations in
the 1980s, paper II also presents new data on mysid abundances, species composition and
trophic position from a formerly well studied coastal area of the northern Baltic proper.
This vertical dispersal of mysids is strongly linked to the nocturnal diel vertical migrations
(DVM) from deep dark waters towards the surface at night and is performed by mysids as
well as many other pelagic organisms. The behavior is generally proposed to be a trade-off
between experiencing higher temperatures and food concentrations close to the surface which
promote growth and reproduction at costs associated with greater predation pressure. Even
though DVM generally is accepted to be working on a population level there is considerable
and commonly ignored individual variation as some individuals do not seem to migrate. In
paper III, we investigated whether this lack of migration is temporary or in fact stable over
longer time periods and what ecological and evolutionary consequences a resident versus
migratory strategy may have on ecosystem functioning.
7
In the last paper (paper IV) we examined the effects of fasting on respiration in a common
littoral mysid species (Praunus flexuosus) and constructed a model of respiration as a function
of temperature and body size. When animals are collected in the field, their feeding history is
seldom known which means that basal metabolic rates may be overestimated due to elevated
respiration related to what and how much they had been feeding before collection (specific
dynamic action, SDA). The establishment of a precise basal metabolic rate is important in
larger modeling contexts since it stands for a major part of an animal’s energy expenditure.
4. Background
4.1 Distribution and habitat choice
Opossum shrimps (Mysids) are common crustaceans in many marine and fresh water
environments. They can be found all the way from shallow coastal areas down to depths of
several thousand meters. Some are strictly pelagic, while others are benthic. Altogether there
are more than 1000 species distributed worldwide (Mauchline 1980).
In the Baltic Sea there are 19 known species of mysids. Ten of these are restricted to the
entrance region of the Baltic Sea (the Kiel and Mecklenburg bights) due to limited tolerance
of low salinity water (Köhn 1992). The by far most abundant species in the Baltic proper are
Mysis mixta, Mysis relicta (pelagic species), Neomysis integer and Praunus flexuosus (littoral
species). Furthermore, Mysis relicta has recently been found to constitute a complex of four
sibling species that hardly are distinguishable by morphology, but have genetic and life
history differences (Väinolä and Vainio 1998). Two of these species are found in the Baltic
Sea (M. relicta and M. salemaai) whereas the other two are restricted to North American fresh
water systems (M. diluviana and M. segerstralei). In general, M. relicta prevails in coastal and
peripheral areas of the Baltic whereas M. salemaai is most common in the pelagic where it
coexists with M. mixta (Väinölä 1992). Unless otherwise stated, the M. relicta species
complex will hence forth be referred to as M. relicta.
Mysis mixta is originally a marine species and its distribution in the Baltic is limited
northwards, up to the Northern Quark area due to low salinities (Salemaa et al. 1990). The
freshwater glacial relict M. relicta, on the contrary, is limited southwards by increasing
salinity and does not occur where salinities are greater than 12 ppm (Ackefors 1969). The
littoral N. integer and P. flexuosus are abundant all along the Baltic coasts.
Low bottom-oxygen concetrations have also been coupled with low mysid abundances
(Salemaa et al. 1986; Salemaa et al. 1990). A current hypothesis is that access to bottom could
be important for the maintenance of mysid populations. Avoiding predation by hiding on or in
the bottom sediment could be one of the reasons for this coupling. In later studies, however,
substantial mysid densities have been observed in areas with low bottom-oxygen
concentrations (Välipakka 1992). These occurrences could be explained by horizontal
migration/drift of animals from areas with better bottom-oxygen conditions or by the
existence of strictly pelagic mysids that do not depend on benthos but rather a light refugium
to avoid predation from visual predators.
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4.2 Diet
Feeding of pelagic mysids is strongly connected to their pronounced, vertical migration
(DVM) and feeding tends to occur on a diurnal basis with a peak during night. Light itself has
been shown to reduce feeding rates for pelagic mysids (Gorokhova and Hansson 1997;
Lasenby et al. 1986; Viherluoto and Viitasalo 2001a) and is most likely an anti-predator
response linked to DVM (Aneer 1980; Lasenby et al. 1986). However, littoral species such as
Neomysis integer and Praunus flexuosus that do not rely entirely on DVM for predator
avoidance, do not display reduced feeding rates in bright conditions. This implies that neither
pelagic nor littoral mysids use vision but rather mechanoreception for foraging (Viherluoto
and Viitasalo 2001a).
Studies on the diet of Baltic mysids are in general few in comparison with fresh water systems
such as the Laurentian Great lakes. The diet of Baltic mysids has been shown to be of a
mainly omnivorous character, ranging from detritus to zooplankton (Grossnickle 1982;
Rudstam and Hansson 1990; Rudstam et al. 1992; Salemaa et al. 1986; Viherluoto et al.
2000). They feed on phytoplankton and detritus by creating a suspension feeding current but
can also capture prey by raptorial feeding (Grossnickle 1982; Mauchline 1980; Murtaugh
1981). The extent of raptorial feeding has been shown be positively correlated with mysid size
(Grossnickle 1982; Viherluoto et al. 2000).
The recent debate on the effects of toxic cyanobacteria blooms on mysids is also worth
mentioning. Recently, high proportions of mysids (M. mixta and M. relicta) containing the
potentially toxic Nodularia spumigena have been observed (Gorokhova 2009). The proportion
of individuals ingesting cyanobacteria was however shifted towards juveniles and sub-adults.
This in turn, may be explained by a higher encounter rate by smaller mysids since smaller
individuals are found higher up in the water column (M. relicta: Kotta and Kotta 1999;
Lasenby and Fürst 1981; Teraguchi 1969); (M. mixta: Grossnickle and Morgan 1979; Kotta
and Kotta 2001; Rudstam et al. 1989; Salemaa et al. 1986; Shvetsova and Shvetsov 1990),
where cyanobacterial concentration can be relatively high. Moreover, small mysids feed
predominantly by suspension feeding (Lasenby and Langford 1972) which enables a high
encounter rate of dominating food particles. Cyanobacteria may, however, clog the mysid’s
feeding apparatus and thus have an impairing effect on feeding, resulting in a time/energy cost
for cleaning the feeding apparatus (Engström et al. 2001). At high concentrations of
cyanobacteria, it is possible that juvenile mysids will consume more cyanobacteria because
the cost/benefit relationship makes it profitable to consume even this food of relatively poor
quality compared to selecting only food that are scarce but of good quality. Even though toxic
species were ingested, it has been shown that mysids actively choose other food if available
(Demott 1995; Engström et al. 2001; Gorokhova and Lehtiniemi 2007). It has further been
demonstrated that mysids consistently feed less on copepods when cyanobacteria are present
(Engström et al. 2001). The reason for this is however unclear. Decreased feeding on high
quality food could be caused either by clogged feeding appendages or a generally decreased
feeding rate to reduce the intake of toxins. Nevertheless, it has been suggested that mysids,
just like several cladocerans (Fulton 1988; Hanazato and Yasuno 1987; Starkweather and
Kellar 1983) are tolerant to the ingested toxins produced by cyanobacteria (Engström et al.
2001) and that these phytoplankters, may be a valuable source of nitrogen during late
summer; either directly as food (Gorokhova 2009) or possibly also indirecly as fuel for
primary producers.
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4.2.1 Mysis relicta/Mysis salemaai
Even though more studies on mysid diets have focused on M. diluviana in lakes (Boscarino et
al. 2006; Boscarino et al. 2007; Bowers and Vanderploeg 1982; Johannsson et al. 2001;
Johannsson et al. 1994; Lasenby and Shi 2004), some diet studies have also been conducted
for its sibling species (M. relicta sp.) in the Baltic Sea. Viherluoto et al. (2000) compared the
diets of M. mixta and M. relicta from the Northern Baltic proper. Their diets overlapped to a
high degree (75%, Schoener's index), but M. relicta fed significantly more on benthic
particles and phytoplankton than M. mixta that relied more on planktonic crustaceans. This
effect could however be partly explained by interspecific size differences as M. mixta grew
faster and reached a larger size than M. relicta. This in turn could be explained by copepods
and cladocerans being better quality food than benthic and plant material.
4.2.2 Mysis mixta
Mysis mixta is the most studied mysid in the Baltic Sea with several reports on its feeding and
diet. Salemaa et al. (1986); Rudstam and Hansson (1990); Hansson et al. (1990); Viherluoto
et al. (2000) and Lehtiniemi et al. (2002) studied gut contents in wild-caught mysids. More
recent papers have mainly reported results of experimental studies (Viherluoto and Viitasalo
2001a; Viherluoto and Viitasalo 2001b; Viitasalo 2007; Viitasalo and Viitasalo 2004).
Salemaa et al. (1986), Rudstam and Hansson (1990) and Hansson et al. (1990) found
cladocerans (Bosmina spp. and Pleopsis spp.) and copepods (Eurytemora spp. Temora spp.
Acartia spp. and Pseudocalanus spp.) to be the predominant food source (90-100% by
weight) in adult M. mixta. Smaller amounts of detritus, phytoplankton and benthic copepods
were however also present. A more recent experimental study also indicated a strong
preference for the copepod Eurytemora affinis and cladocerans (however, to lower extent).
The other abundant copepod, Acartia spp. was not readily ingested (Viherluoto et al. 2000) in
contrast to the earlier findings (Hansson et al. 1990; Rudstam and Hansson 1990; Salemaa et
al. 1986). The authors explain this by the fact that Acartia is a fast swimmer (Viitasalo and
Rautio 1998) and thus a hard prey to capture. Even though the same is valid for Eurytemora
(Viitasalo et al. 1998), there are indications that Eurytemora produces stronger hydromechanical signals which are more easily detected by non-visual predators like mysids.
(Viherluoto pers. observation, but see also: Gorokhova et al. 2005; Gorokhova and Lehtiniemi
2007). Under experimental conditions however, Mohammadian et al. (1997) found clearly
higher capture rates for Acartia than for Eurytemora.
Viherluoto and Viitasalo (2001b) further stated that prey preference was related to mysid size
and prey species composition. Small mysids preferred rotifers to a high extent since they are
small prey and easy to capture. As mysids grew larger, the diet composition varied more.
Viherluoto and Viitasalo (2001b) suggested that larger mysids are less selective simply
because their size does not limit them from capturing evasive and large prey. The switch to
larger prey occurred after a threshold length of 8-11 mm.
4.2.3 Neomysis integer/Praunus flexuosus
Both Neomysis integer and Praunus flexuosus differ from Mysis spp. in habitat choice,
occurring mainly in the littoral where N. integer often forms swarms in more open areas
10
whereas P. flexuosus is more closely associated with the phytobenthos. Recent studies
however, show that N. integer also can be abundant in the pelagic environment (Kotta and
Kotta 2001; paper II in this thesis). The diet preferences are similar to that of Mysis spp. Both
species are omnivores and consume everything from detrital matter to algae and zooplankton
(Bremer and Vijverberg 1982; Fockedey and Mees 1999; Lehtiniemi and Nordström 2008).
Food utilization has been coupled to the availability of different food objects, e.g.
phytoplankton spring bloom and zooplankton peak abundances in late summer (Lehtiniemi
and Nordström 2008). Food preference is furthermore size regulated to some extent.
Interestingly, small and extremely large Neomysis integer consume significantly less
phytoplankton than intermediate sized animals (Lehtiniemi and Nordström 2008). It is thus
attractive to hypothesize whether these diet differences are a response to predation pressure,
bioenergetical needs, a result of an overlap in size distribution or a combination of these
factors. Hakala et al. (1993) and Lehtiniemi and Nordström (2008) found juvenile Neomysis
consuming a higher proportion of rotifers as opposed to adult animals which consumed
mainly cladocerans and copepods by weight. However detrital and algal particles dominated
by numbers. Similar diet preferences could be demonstrated for the pelagic M. mixta
(Viherluoto et al. 2000).
4.3 Life history and growth
Many features of an organism’s biology are genetically constrained, e.g. the potential for
growth, egg carrying capacity etc. Indeed, growth rates and generation times vary
substantially among the dominating Baltic species. Neomysis has an asynchronous breeding
season with more than one cohort annually (Mauchline 1980); whereas the pelagic M. mixta
usually produces one brood per year but may supposedly reproduce a second time, one year
later producing two cohorts. (Salemaa et al. 1986; Shvetsova and Shvetsov 1990). The
iteroparous lifestyle described by these authors is however debated. Viherluoto et al. (2000)
studied an M. mixta population throughout the growing season, from June to October. They
found two distinct cohorts forming during late summer and then merging into one cohort
again in late autumn. This finding could thus not be explained by a portion of the population
having different generation times but rather by intra cohort differences in growth rates.
Additionally, Simm and Kotta (1992) and Rudstam and Hansson (1990) found no evidence
for a two year life cycle in M. mixta. Simm and Kotta (1992) explain the observations of very
large, gravid females in autumn by Salemaa et al. (1986) and Shvetsova and Shvetsov (1990)
by erroneous comparisons of specimens from geographically distinct areas with differing
potentials for growth rather than prolonged life cycle and the authors’ understanding is that M.
mixta have a one year life cycle in the Baltic and that it rarely lives longer than 16-17 months.
However, aberrantly large gravid females (22-23 mm) have been found together with much
smaller individuals (12-14 mm) at several localities in Stockholm archipelago during JulyOctober, (Ogonowski, M. and Gorokhova, E. G. pers. obs.). These findings contradict the
conclusions of Simm and Kotta and are not plausibly supported by the idea of different
growth rates (Viherluoto et al. 2000) due to the great difference in size. Thus, there are two
explanations to these findings: (i) some M. mixta grow past the first spawning season without
reproducing to spawn the following winter or, (ii) they survive the act of reproduction and
spawn a second time. It is thus still debatable whether M. mixta has a strict one-year life cycle
in the Baltic Sea or not.
The M. relicta species-complex on the other hand is known to have a varying life cycle.
Populations with differing generation times have been identified in the Baltic and vary with a
11
12, 18 or 24 month life cycle (Hakala 1979; Välipakka 1990). It has been proposed that this
variation may be due to variable food quality and primary production in different areas, where
availability of good quality food is positively correlated with shorter generation times. The
oligotrophic Lake Tahoe in California, for example, harbors an introduced population of M.
diluviana, which has a generation time of at least four years, whereas an isolated much more
productive bay of the same lake holds mysids with a one year life cycle (Morgan 1980). Life
history differences of the sub-populations do not seem to be effects of evolutionary adaptation
but rather plasticity since both groups in Lake Tahoe stem from the same ancestral population.
Moreover, mysids preferred the same temperature strata in both areas indicating that
temperature was of little importance for the reported differences in generation times. In the
Baltic, similar patterns have been observed. In the Bothnian bay, M. relicta and M. salemaai
are sympatric and both are winter-breeders, with a two year life cycle. Southwards however,
where productivity is substantially higher (Samuelsson et al. 2006), one year life cycles
predominate and M. salemaai breeding occurs throughout the year in the Gulf of Finland
(Väinolä and Vainio 1998; Välipakka 1990; see also: Hessle and Vallin 1934; Shvetsova and
Davidyuk 1987; Teraguchi 1969) but probably not in the northern Baltic proper (pers. obs,
paper II and III in this thesis).
Shvetsova et al. (1992) followed the population dynamics of two generations of M. mixta
during a year in the Gulf of Riga. Their calculations indicate that the mysid mortality rate was
at its highest during September-December, coinciding with a diet shift in herring (Aneer
1975; Rudstam et al. 1992) This further indicates that as mysids compete with herring for
zooplankton during the summer months, they also become the prey for older herring in the
autumn and predation pressure on the shared resource progressively decreases when predation
on mysids increases (Rudstam et al. 1992).
4.4 Migration patterns
Nocturnal diel vertical migration (DVM) is a well-known phenomenon performed by many
invertebrates in both freshwater and marine ecosystems. It is a widespread behavior and is
manifested by feeding in the surface waters (epilimnion) at night and then inhabiting deeper
and darker waters (hypolimnion) in daytime. This behavior reduces the risk of being eaten by
visual predators like fish (Lampert 1989; Lampert 1993).
However, not all pelagic mysids migrate. Rudstam (1989) (Mysis mixta), Bowers (1988) and
Morgan, (1980) (Mysis relicta) all found mysids residing on or close above the bottom during
night. Until recently, it has been unknown whether these mysids ever migrate or not.
Ogonowski et al. (Paper III), found that Mysis salemaai caught on the bottom at night had a
significantly different isotope signature in muscle tissue from pelagic mysids collected at the
same date and site (coastal northern Baltic Proper). These findings indicate that the food
ingested by these two groups of mysids differs and that pelagic mysids may have a higher
proportion of zooplankton in their diet, indicated by a higher 15N:14N ratio.
The vertical migration of mysids (M. relicta, in particular) has been studied extensively
(Ackefors 1969; Beeton 1960; Boscarino et al. 2006; Boscarino et al. 2007; Debus et al. 1992;
Lasenby and Langford 1972; Teraguchi 1969) because of their important role, both as food
for many fish species and also because of their potentially high predation on other
zooplankton species (Mauchline 1980). Mysid DVM has mainly been studied in pelagic
systems but is evident in littoral species as well, even though the extent of vertical migration
12
in this habitat may be just in the range of 3-25 m (Kotta and Kotta 2001), while it can be
>100 m in pelagic species. In pelagic systems, downward migration is believed to provide a
darkness refuge that helps them avoid fish predation. In littoral systems, this explanation does
not seem to be adequate, since light extinction does not change to the same magnitude as in
the pelagic. Littoral downward migration during daytime could be coupled to a refuge in form
of dense macrophyte coverage and/or association to benthic substrate.
Littoral mysids, such as Neomysis integer, also perform horizontal migrations. Intense
schooling (up to 50 000 ind.·m-2) in the littoral during day (Rasmussen 1973) and dispersed
individuals in offshore areas during night have been observed (Debus et al. 1992). One to two
hours prior to sunrise, these mysids seemed to return to the littoral. At such high mysid
densities, it is possible that food resources become locally depleted in the littoral, thereby
forcing mysids to expand their feeding grounds to the pelagic environment during night when
predation pressure relaxes. Horizontal migrations were also observed in another littoral mysid,
Paramysis lacustris, and the pelagic Mysis relicta. These migrations were however not
performed on a diurnal basis, but rather on a seasonal. Paramysis and juvenile Mysis relicta
migrated into coastal areas during autumn when decaying plant material was abundant
providing a food source (Beeton and Bowers 1982; Lesutiene et al. 2008; Morgan and
Threlkeld 1982). In the case of juvenile Mysis relicta, migration to shallower waters could in
addition be an escape reaction from predation by adult mysids that prefer deeper waters
(Morgan and Threlkeld 1982; Quirt and Lasenby 2002). However, such active horizontal
translocations are, to my knowledge, not known to occur in the Baltic Sea for neither M.
relicta nor M. mixta. This could, in contrast to Morgan and Threlkelds’ situation be explained
by the presence of other, adult littoral mysid species posing a threat to juveniles.
4.4.1 Effects of Light
The questions concerning the mechanisms behind DVM, and the variables that govern it, have
been investigated by several authors. Lasenby and Fürst (1981) studied mysids in situ with a
high frequency echosounder. They observed mysids to avoid migration into the densest
zooplankton layer during full moon and speculated that mysid feeding may be inhibited by
light (see also: Debus et al. 1992). Several authors suggested light intensity to be the principal
variable governing DVM in pelagic mysids (Boscarino et al. 2009; Bremer and Vijverberg
1982; Rudstam et al. 1989; Salemaa et al. 1986). Rudstam and Hansson (1990) observed M.
mixta to avoid light levels above 10-4 lux, whereas for M. diluviana, these levels were variable
from 10-6 lux (Boscarino et al. 2009) to 0.02–0.05 lux (Teraguchi et al. 1975). In the Baltic
proper, the light preferences for M. relicta remain unknown, but recent observations indicate
that M. relicta in pelagic water increased with depth and dominated at depths exceeding 150
m (pers. obs.) thus indicating that M. relicta could be more light sensitive than M. mixta;
dissimilarities in light tolerance may however be attributable to the different subspecies of M.
relicta (Audzijonyte et al. 2005; Pahlberg et al. 2005). Similar observations have also been
reported by Ojaveer et al. (1999). Consequently, these observations suggest that M. relicta in
the Baltic Sea may have a lower tolerance to light than M. mixta; alternatively the partial,
vertical separation is a response to lower food availability potentially driven by competition.
Wiebe et al. (1996) investigated the effect of light on M. diluviana DVM and realized that
standard light measuring equipment could be inadequate due to the fact that “lux” is a scale
measure related to the visual spectrum of the human eye. M. relicta eye sensitivity has
different spectral optima, ranging from 505-570 nm (Dontsov et al. 1999; Jokela-Maeaettae et
13
al. 2005; Lindström and Nilsson 1988). Dontsov et al. (1999) further demonstrated similar
peak sensitivities for M. salemaai and M. mixta. Lindström et al. (2000), Dontsov et al.
(1999) and Wiebe et al. (1996), concluded that peak sensitivity may vary among populations
of a single species due to adaptations to specific optical environments. Moreover, Beeton
(1959) and Jokela-Maeaettae et al. (2005) observed that juveniles are much less sensitive to
light, which might explain their vertical separation from adults during day time. This feature
could be an adaptation to (1) avoid cannibalism, (2) stay higher in the water column and feed
on small sized phytoplankton, (3) encounter higher temperature that promotes growth; a
combination of these factors is also likely.
4.4.2 Vertical size distribution
Predation risk by visual predators like herring reasonably increases with light intensity. It
would be expected, however, that small, less conspicuous mysids are more difficult for fish to
detect and that they may migrate higher up in the water column in search for high quality food
and at the same time escape predation from conspecifics (Brooks and Dodson 1965; Rajasilta
and Vuorinen 1983). Rudstam et al. (1989) found small, juvenile Baltic M. mixta higher up in
the water column than large individuals. Similar observations have been made by Hessle and
Vallin (1934); Salemaa et al. (1986); Kotta and Kotta (1999) (M.mixta); Grossnickle and
Morgan (1979); Teraguchi (1969) and Bowers (1988) (M. relicta). The mechanisms behind
this behavior are however not clear. If the behavior is a result of predation avoidance from
visual predators, then a vertical separation between sexes should also be prominent, since
egg/embryo carrying females are far more conspicuous than males. However, no such
differences have been found (Teraguchi 1969).
Although observations regarding the more extensive DVM of juvenile mysids, indicating
vertical size differences are well described in the literature, few attempts have been made to
study vertical size distribution explicitly. We need to know under which circumstances and
how different sizes of mysids disperse in order to accurately be able to incorporate them into
bioenergetical models and energy budgets. Consequently, a detailed knowledge of vertical
migration and size distribution is of importance for understanding the energy flows between
trophic levels in pelagic ecosystems and benthic-pelagic coupling.
4.4.3 Temperature
Although light intensity has been proven an important factor restricting mysid migration to
top surface layers, limits in terms of temperature also seem to be present and some authors
have considered temperature to be the primary underlying factor governing the extent of
DVM in mysids (Lampert 1989; Maurer and Wigley 1982). In a study by Salemaa et al.
(1986), most M. mixta were caught below the thermocline and rarely passed into warmer
water than 10°C. Other studies though, have found mysids well above the thermocline (Grabe
and Hatch 1982; Kotta and Kotta 1999; McLaren 1963; Teraguchi 1969). Rudstam et al.
(1989) noted that mysids that migrated and passed the thermocline primarily were small
juveniles. An absence of juveniles in the collections of Salemaa et al. (1986) could explain
why they suggested that mysids do not pass the 10°C boundary. Strong temperature gradients
have been proposed to limit the DVM in mysids. Beeton (1960) found mysids avoiding
passage through temperature gradients of 2°C · m-1. When the thermocline was weak or
disrupted, mysids were distributed throughout the water column. However, in a more recent
14
study by Boscarino et al. (2007), M. diluviana from Lake Ontario showed strong preference
for 6–8°C and did not seem to be affected by temperature gradients although absolute
temperatures limited mysid vertical migration. Consequently, the effects of temperature on
mysid behavior manifest some degree of variation and the ways it affects mysid migrations
are not clear.
4.4.4 Chemical cues
While DVM in zooplankton has received much attention in the past, (e.g. Hays 2003;
Hutchinson 1967; Lampert 1989) focus has been on the behavior of the average population on
exogenous stimuli. Since predation by visual predators most probably occurs at the
boundaries of a DVM-prey’s distribution (Boscarino et al. 2007), other means have to be
employed in order for these effects to be studied.
The presence of chemical substances from fish (kairomones) has shown to further increase the
migration of zooplankton and mysids away from fish (Boscarino et al. 2007; Cohen and Ritz
2003; Dodson 1988; Loose and Dawidowicz 1994; Loose et al. 1993). In the absence of such
chemical cues, zooplankton, usually stay in the epilimnion/metalimnion continuously.
Chemical cues from fish have also shown to affect mysids on another level. Hamrén and
Hansson (1999) and Lehtiniemi and Lindén (2006) observed that M. mixta and M. relicta
changed their feeding rates when exposed to fish scented water. Mysids ate less and were less
selective to prey items in order to decrease their conspicuousness to predators. However, a
similar study on littoral mysids Neomysis integer and Praunus flexuosus (Lindén et al. 2003)
did not yield lower feeding rates. Instead, more time was attributed to hiding in the provided
macrophyte refuge in the presence of fish kairomones. These differences could be explained
by the very different environments that littoral and pelagic mysids live in. As pelagic mysids
do not have any structural refuge in open water, decreased feeding and thus swimming may
be ways of decreasing conspicuousness (see Gerritsen 1984; Savino and Stein 1989). Littoral
mysids on the other hand are closely associated with the macrophyte coverage and use a
different strategy to avoid predators (Lindén et al. 2003).
Mysids may also display behavioral responses to cannibalism by conspecifics (Clutter 1969)
which manifests itself in terms of ontogenetic niche separation. Juvenile and subadult mysids
usually migrate higher up in the water column during night (Grossnickle and Morgan 1979;
Rudstam et al. 1989) and besides possible effects of light and temperature (see above) this
may be attributable to chemical cues from adult mysids (Quirt and Lasenby 2002).
4.4.5 Niche differentiation and partial migration
Even though diel vertical migration commonly is accepted as being a prominent part of
zooplankton and mysid behavior, it is generally treated as a population level trait, i.e.
individual variation is disregarded. However, several authors have reported a bimodal nighttime vertical distribution in mysid populations (North American lakes: Morgan (1980),
Bowers (1988); the Baltic Sea: Rudstam et al. (1989)), with part of the population close to the
bottom even at night, suggesting that some individuals may be sedentary. Morgan (1980)
assumed this group to consist mostly of recently moulted gravid females, although this was
later rejected by Bowers (1988) who observed that the demographic structure of the benthic
part of the population generally was representative of the entire population. These
15
observations thus raise some interesting questions regarding the nature of this behavior. Are
mysids polymorphic in respect to habitat choice and resource use or can there be other factors
explaining these observations?
A division into pelagic and benthic forms is actually not uncommon in nature, especially
among fishes (Robinson and Wilson 1994; Skúlason and Smith 1995) and the cause for such
segregation has been proposed to be a release from competition promoted by the discrete
nature of benthic and pelagic habitats. Although niche differentiation of this form often is
related to intraspecific morphological differences, it is sometimes only expressed as an
intraspecific behavioral difference without any noticeable morphological or genetic
discrepancies (behavioral plasticity) (Bolnick et al. 2003). As niche partitioning often is
discussed in the context of persistent traits where species, early in life diverge into different
forms to specialize in specific habitats, temporary competitive release may be achieved by a
part of the population migrating to other habitats on a seasonal basis.
This phenomenon is termed partial migration. Stemming from the avian literature (Lundberg
1988), it has been described in a wide array of taxa and can often be coupled to intrinsic
conditional states (e.g. sex, age or ontogeny) or extrinsic plastic traits such as physical
condition and dominance (Lundberg 1988). In the case of DVM-performing animals that
have regular and frequent migrations, very little is known in terms of persistent life history
strategies, even though bimodal vertical distributions regularly are observed in both fish and
zooplankton (see Pearre 2003 for review). In fact, Mehner and Kasprzak (2011) where the
first to propose that the absence of DVM in fish could be a manifestation of partial migration
(sensu Lundberg (1988)). Although some fish were found to be “resident”, the duration of
residency was not established and thus neither the potential magnitude of trophic interactions.
The problem of tracking individuals makes it difficult to say whether the “resident” part of the
population is resident over some considerable time period or if individuals change strategy on
e.g. a nightly, daily or weekly basis (asynchronous migration).
The third paper in this thesis addresses this problem by using stable isotope and genetic
markers to elucidate the persistence of “residency” in Mysis salemaai, providing the first line
of evidence for persistent partial migration in mysids.
4.6 Bioenergetics
Knowing how much animals eat is important for our understanding of trophic dynamics.
Estimating consumption is however not trivial, especially for small omnivores like mysids
that depend on a wide variety of small prey, making it difficult to estimate consuption
directly. Thus, indirect methods are usually applied.
Bioenergetic models are a way of estimating consumption by using a fairly straight forward
energy budget approach, using knowledge of basic physiological demands, growth and
temperature preferences. Generally, an energy budget can be stated in the following terms:
Energy consumed = Respiration + Waste + Growth
Although bioenergetic models have been used successfully among a variety of taxa, relatively
little has been presented for mysids. Rudstam (1989) estimated the consumption of Mysis
mixta with a bioenergetic model using physiological parameters mainly derived from
16
measurements on Mysis diluviana. Validations of this model produced realistic results for
both species (M. diluviana: Chipps and Bennett (2002), M. mixta: Gorokhova (1998))
although some improvements to the model were made by Gorokhova (1998). It is not
surprising that one model performed well for both of these species as both M. mixta and M.
diluviana have similar temperature preferences, behavior and life-history-traits. Regarding
littoral mysids in the northern Baltic Proper, bioenergetic approaches have only been
published for Neomysis integer (Maciejewska and Opalinski 2002) and it is questionable
whether a Neomysis-model could be applied to P. flexuosus since these species have different
lifestyles. N. integer aggregates in swarms which decreases respiration (Ritz et al. 2001) and
probably has a lower temperature tolerance than P. flexuosus; N. integer often migrate into the
pelagic during summer when temperatures become too high (Debus et al. 1992) whereas such
migrations have not been reported for P. flexuosus.
Since temperature has such a strong effect on biochemical and metabolic processes (Gillooly
et al. 2001; Winberg 1956) and respiration accounts for approximately 50% of an animals
total energy expenditure, it is crucial from a bioenergetics perspective, to know the
relationship between temperature and respiration.
Another important aspect in this context is the basal respratory rate (routine metabolic rate,
RMR), i.e. the level of respiration that is used to sustain basic metabolic processes. Although
such parameters are available in the litterature, there is a need for caution, since this rate will
be influenced by an energy expenditure related to the processing of food (specific dynamic
action, SDA), possibly introducing bias to the bioenergetic model. Because SDA is dependent
on how much and which food has been consumed, and we seldom know the feeding history of
animals collected in the wild, we need to know the duration of SDA or the magnitude of SDA
itself. The duration of SDA as well as SDA-values for mysids are at this point unavailable.
Rudstam et al. (1989) assumed a value of 18% of assimilated food which is in the range of
SDA-values reported for other zooplankton. Chipps and Bennet (2002) later performed a
sensitivity analysis showing that parameters most sensitive to Rudtsam’s bioenergetic output
were related to respiration, i.e. SDA, routine metabolic rate or a combination of both.
Assuming that RMR paramters were correct in the model, SDA could have been erroneously
estimated by 50-70%. Regarding the duration of SDA, it has been assumed that this effect
would be exhausted after just a few hours post-feeding (Kiørboe et al. 1985). Paper IV in this
thesis however, shows that this is not the case and that postfeeding effects may be much more
extended (>30 hours) than previously expected. Ultimately this means that there may be some
bias associated with currently available respiration parameters.
4.7 Abundance
Due to patchy distributions and diel vertical migrations, quantification of mysids is in general
difficult, expensive and time consuming and no standardized methods have been developed.
Few such attempts have however been made in the Baltic Sea where most of the studies have
been conducted in the Gulf of Riga (Kotta and Kotta 1999; Kotta 1984), Gulf of FinlandBothnian Sea (Salemaa et al. 1986; Salemaa et al. 1990; Simm and Kotta 1992) and inner and
outer areas of the Stockholm archipelago (Rudstam and Hansson 1990; Rudstam et al. 1986).
To date, there have only been two large scale attempts to assess mysid abundances in the
Baltic Sea. Shvetsova et al. (1992) conducted a survey covering the eastern parts of the Baltic
proper southwards to the Polish coast. Salemaa et al. (1990) concentrated most of their efforts
17
to the Gulf of Finland and the Bothnian Sea. Although the survey of Shvetsova et al. (1992)
provides good spatial and temporal resolution, there is one fundamental problem; abundances
were estimated over varying depths, from 20-100 m. thus expressing abundances in
volumetric units. Mysids perform diel vertical migrations and are rarely evenly distributed in
the water column. It is therefore much more rational to express densities on an areal rather
than a volumetric scale. Further problems arise when results from different studies are
compared. Since there are no standardized methods for mysids sampling, nearly all reported
mysid abundances are based on different gears, and sampling efficiencies of these are
generally lacking.
4.7.1 Sampling methods
Mysids are agile and quick animals and sustained swimming speeds up to 10 body lengths·s-1
are common, with bursts of up to 20 body lengths·s-1 reported for several species (Mauchline
1980). Indeed, mysids have been shown to actively avoid sampling gears through means of
intra-school communication (Clutter and Anraku 1968; Lasenby and Sherman 1991)
especially at daylight (Fleminger and Clutter 1965). The reasons for lower sampling
efficiency at daylight are not clear. One possibility is the gear avoidance described above and
another is the pronounced patchy and concentrated distribution under bright conditions. Data
on sampling efficiency of different gears is in most cases unavailable when it comes to mysids
and the need for several types of gears due to ontogenetic habitat separation and possible
schooling, further complicates abundance measurements. Eleftheriou and Holme (1984) and
Carleton and Hamner (1987) for instance, suggested sampling efficiencies of 1-10% in
epibenthic sleds. This is problematic and indicates that traditional sampling for mysids infers
gross underestimations of abundances. Large mesh nets, with high filtering efficiency, usually
miss small mysids, whereas use of smaller mesh sizes result in lower efficiency, low towing
speeds and thus higher avoidance (Jumars 2007). Consequently, both large and small mesh
sizes will tend to underestimate mysid abundances. Either by omitting juveniles in large
meshes or by higher avoidance of large individuals in small mesh sizes. Smaller mesh sizes
will additionally bias the catch towards smaller individuals.
4.7.2 Hydroacoustics
Hydroacoustics is an alternative strategy for abundance estimation and is a non-invasive
method, which omits the problem of avoidance and is vastly more efficient when it comes to
spatial coverage.
Since the development of the sonar, hydroacoustics has been used extensively in ecological
studies. The ability to study marine organisms in situ and possibility to cover large volumes of
water has come to be the most important feature of this technique. Although extensively used
in fisheries biology (Simmonds and MacLennan 2005), hydroacoustics has also been found
effective in studies of much smaller organisms, such as plankton and pelagic invertebrates
(Boswell and Wilson 2004; Gal et al. 2004; Gonzalez Chavez and Arenas Fuentes 2003;
Holbrook et al. 2006; Johnson et al. 2004).
Despite of its many advantages, species determination still has to rely on complementary
trawls or net catches and information about the studied organism’s distribution patterns and
biology is needed for a correct interpretation of the echograms. The advances made with multi
18
frequency techniques, however, allow to coarsely distinguish between organisms with
different acoustical properties, resulting in minimized physical sampling (Korneliussen and
Ona 2003).
The backscattering properties, i.e. the acoustic signature of the received echo of aquatic
organisms may vary considerably. The amount of backscattered energy depends on the
difference in density between water and the target. Although all tissues and bones in fish
reflect sound, the by far most significant source of reflection is the swim bladder. About 9095% of the backscattering can be attributed to the gas-filled swim bladder (Foote 1980). Since
mysids lack this organ, their echo strength is much lower than that of fish making them more
difficult to detect. Additionally, the target strength (TS) of most organisms is affected by its
tilt angle. Boscarino et al. (2007) observed that mysids instantaneously disappear from an
echogram whenever an artificial light source is pointed at the water surface during night. They
concluded that this phenomenon was due to a change in tilt angle in response to light
avoidance, i.e. mysids turned their heads down in order to avoid the light which drastically
decreased TS.
Due to their small size and often high densities, TS estimation of single individual mysids
becomes practically impossible. Echo integration however is a way to obtain estimates of
biomass and is often referred to as the Mean Volume Backscattering Strength (MVBS or Sv).
Even though single echo detections (SED) and TS are difficult to obtain from mysids, it is
possible to back-calculate a mean TS-value to length relationship. This relationship, combined
with data on the mysid’s actual size distribution, can sequentially be used to derive abundance
estimates from recorded Sv values (Gal et al. 1999).
The acoustic backscatter from zooplankton, including mysids and krill has shown to be more
intense when using higher frequency echosounders, while the opposite relationship is valid for
fish (Brierley et al. 2004; Gorska et al. 2005; Jech 2006; Knudsen et al. 2006; Korneliussen et
al. 2008; Korneliussen and Ona 2003). Based on this knowledge, signals from fish, which are
the strongest scatterers, can be filtered out from acoustic data by combining the information
from several, simultaneously run frequencies (Knudsen et al. 2006). Quantification of M.
relicta by multifrequency acoustics has been evaluated by Gal et al. (1999) and seems to give
reasonably good results. They calculated the average TS for M. relicta in Lake Ontario based
on in situ data for different frequencies and concluded that their results did not differ greatly
from theoretical models (e.g. Foote 1990; Stanton et al. 1993). Their experiments were
however conducted in a fairly simple ecosystem from an acoustic point of view, a system with
few acoustically similar organisms.
Since mysids are not easily distinguished from other similarly-sized invertebrates, this means
that good knowledge of the organisms constituting the ecosystem of interest is fundamental
for the data interpretation. By knowing the acoustic properties of different organisms and how
environmental factors affect migration patterns and behavior, errors in acoustic interpretation
may be minimized.
19
5. Summary of papers
Paper I
Multifrequency discrimination of fish and mysids
We investigated the possibility of estimating mysid abundances and biomass by the use of
multifrequency hydroacoustics. Fish compared to other objects, displayed different frequency
responses and could therefore be removed by masking (Korneliussen et al. 2008;
Korneliussen and Ona 2003). We found a strong, positive relationship between mysid
biomass and filtered echo-data. However, daytime data showed considerable acoustic
backscatter in the epilimnion, resulting not from mysids but from a dense layer of the fresh
water cladoceran Leptodora kindtii. This illustrates that for accurate estimates with this
technique, good knowledge is needed on distributions in relation to biotic and abiotic factors,
both for mysids and other large zooplankton.
Paper II
Status and vertical size distributions of a pelagic mysid community in the northern Baltic
proper
In the second paper, we compared historical, mysid abundance data from the 1980s (Rudstam
et al. 1986) from a coastal area of the northern Baltic proper with recent data from 2008. The
trophic position of three common mysids (Mysis mixta, Mysis relicta and Neomysis integer)
was investigated by stable isotope analysis of N and C in muscle tissue. We also examined the
vertical size distribution of these species in relation to light and temperature using linear
mixed models (LME). Our data indicate a significant decrease in M. mixta abundance
compared to historical data which also translates to significantly lower total mysid biomass in
the area. No clear differences in abundance of M. relicta or N. integer were noticeable
although their proportions relative M. mixta have increased significantly. Stable isotope
analysis indicated that Neomysis integer feeds on a lower trophic level than Mysis spp. and
that the diet consists mainly of phytoplankton, but the difference could be related to a smaller
average size of Neomysis, and not species specific diet differences. However, the fact that
juvenile Neomysis now are abundant in pelagic surface waters should make them attractive
food items for larger clupeids and possibly also lead to a decreased predation pressure on
Mysis spp. M. relicta displayed slightly higher 15N enrichment than M. mixta. This could be
an effect of a more pronounced DVM by M. mixta and by that, possibly a higher intake of 15N
depleted material associated with cyanobacterial occurrence (Gorokhova 2009), thus leading
to a relatively lower nitrogen signal. The vertical size distribution of mysids displayed a
significant size increase with depth and in situ light for N. integer but not for Mysis spp. The
vertical size increase in Neomysis correlated negatively with temperature to some extent but
the smallest juveniles were always caught higher in the water column than larger specimens
even during isothermal conditions, indicating that the vertical size distribution probably is a
response to predation more than size related temperature preferences. The lack of vertical size
differences in Mysis spp. was probably caused by very low variation in size, restricted vertical
distribution and fewer observations compared to Neomysis integer. Moreover, Mysis spp.
were almost exclusively found below the light threshold needed for visual feeding by herring
(10-4 lux) thus making any anti-predatory behavior coupled to vision such as reduction of
conspicuousness obsolete.
20
Paper III
Persistent lack of diel vertical migration in a pelagic mysid population –– a case of partial
migration
The possibility of a persistent partial diel vertical migration in Mysis salemaai was evaluated
by a combination of ecological (stable isotopes as a proxy for diet, C:N ratio as a proxy for
lipid accumulation and protein:DNA ratio as a proxy for growth) and genetic markers
(mitochondrial DNA, cytochrome oxidase I gene).
Stable isotope analysis indicated that there were significant differences between benthic and
pelagic mysids with pelagic individuals being slightly more carnivorous. This was evident
both over a longer (muscle tissue) and shorter (chitin) temporal resolution indicating that
differences in diets should persisted at least during the growth period (spring—summer).
Genetic analysis revealed a fine-scale genetic structure between the two stations and between
the benthic samples indicating that bottom-dwelling mysids were less mobile than pelagic
ones. We did however not find any differences in C:N or protein:DNA ratio between groups
which indicates that despite differences in diet and behavior, either strategy seems to convey
equal fitness benefits in terms of growth and lipid stores which is in line with current
understandings of partial migration theory.
In conclusion, our results indicate that partial diel vertical migration is a phenotypically
plastic trait and since mysids in the Baltic Sea have been shown to be food limited large parts
of the year (Mohammadian et al. 1997) it is plausible that the “choice” for a resident strategy
is induced by intraspecific competition for pelagic zooplankton.
Paper IV
A weight and temperature dependent model of respiration in Praunus flexuosus (Crustacea,
Mysidacea)
Respiration is a major component of an animal’s energy expenditure and precise
measurements of this parameter are important in modelling contexts, which is why we
measured and monitored oxygen consumption of previously fed mysids (Praunus flexuosus)
over a period of > 30 hours.
Moreover as temperature and size have been shown to influence respiration significantly we
wanted to establish a temperature and weight-dependent model of respiration which could be
used in a more complex modelling framework.
We found that post-feeding digestive processes had a significant and positive influence on
metabolic rate (specific dynamic action, SDA) and that this effect was detectable over a long
period of time (over the entire course of the experimental period and much longer after food
had been evacuated from the guts). This indicates that basal metabolic rates may be
overestimated without a proper pre-examination of SDA-effects. The temperature and weightdependent model explained a high degree of variation (r2 = 0.87) and is to our knowledge the
first one presented for this species.
21
6. Conclusions
The recent decreased condition of herring and sprat and also local recruitment problems of
littoral fish such as perch (Perca fluviatilis L.) and pike (Esox lucius L.) have raised questions
concerning food-limitation and lack of top-down regulation by large predatory fish such as
cod (Nilsson et al. 2004). Despite of the fact that mysids are known to be very effective
zooplanktivores (Hansson et al. 1990), they are rarely mentioned in such contexts. The results
of paper I show that echosounding for mysids could be a successful way of gathering
abundance and biomass estimations by covering large volumes of water, thereby reducing
bias caused by patchy distributions. However, there is a case for caution since dense
aggregations of large zooplankton may be falsely interpreted as mysids. It is therefore
important to understand the mechanisms governing the distribution of organisms in order to
make accurate interpretations of echo data. Moreover, because this technique involves
exclusion of fish echoes on a two dimensional plane, it also means that high densities of fish
may mask echoes from mysids. This was evident during a pilot study in a coastal area of the
northern Baltic proper in 2008 (author’s unpublished) where a dense layer of fish was present
from the surface down to below the thermocline where most mysids were concentrated, thus
making quantification difficult. The technique could however work more successfully in
deeper areas where mysids would be separated from most of the fish for longer periods of
time due to lower spatial overlap. Investigating the deeper areas of the Baltic would also be
advantageous for two reasons:
i.)
ii.)
Depths >30 meters are more representative of the Baltic as a whole than coastal
areas.
Pelagic mysids usually occur at depths > 30 meters.
This means that by studying the true pelagic, we would gain valuable information on the bulk
of pelagic mysid abundance in a representative environment. Additionally, the hydroacoustic
recordings would provide information on the behavior and relation of mysids to areas of deep
water hypoxia/anoxia, which have become an area of great concern in recent years.
The current abundances of Mysis mixta presented in paper II, are clearly lower compared to
historical data from the 1980’s. It is however impossible to tell whether current abundances
are at a ‘normal’ state or not since there are considerable gaps between surveys. What can be
said however, is that M. mixta was the dominant pelagic mysid in 1993-1996 (collections for
experiments; Gorokhova and Hansson 2000; Hamrén and Hansson 1999; Mohammadian et al.
1997), clearly after a supposed Baltic Sea regime shift (Alheit et al. 2005) in the end of the
1980’s. In our study, M. mixta was no longer the dominant pelagic mysid and the reason for
this decrease in is not known but the general decline is supported by indirect observations
even in the southern Baltic (Dziaduch 2011) indicating that the decrease probably is not a
local phenomenon. Conversely abundances of Neomysis now show tendencies of increase
even though they sporadically were high during autumns in 1983-1985 (Rudstam et al. 1986).
As the bulk of individuals were small juveniles feeding on phytoplankton we would expect a
low degree of niche overlap between Neomysis and Mysis spp. This combined with high
abundances of Neomysis in the surface layers would further decrease predation pressure on
Mysis spp. in favor for predation on Neomysis. Altogether, this makes it even more difficult to
understand the decrease of Mysis mixta.
Advances in understanding the mechanisms behind the vertical migration of mysids have also
been made recently (Boscarino et al. 2006; Boscarino et al. 2007; Gal et al. 2004). However,
22
the aspect of size as well as size specific interactions of mysids and fish have generally been
underappreciated in vertical migration models. This implies, that models like those described
by Boscarino et al. (2007) would produce false predictions of mysid DVM if temperature and
light preferences would be linked to size; which also was acknowledged by Boscarino (2009).
An optimization of current mysid DVM models by including aspects of vertical size
distribution would provide means to create more precise bioenergetics models, both for fish
and mysids, and thus aid in the construction of more accurate, large-scale food-web models.
Our efforts to disentangle the relative importance of light and temperature as cues driving the
vertical size distribution (Paper II) revealed that in situ light is more important than
temperature as mysid size increased linearly with light levels throughout the sampled
temperature gradient. Even though the smallest individuals potentially aggregated in warmer
surface waters to optimize their scope for growth, mysids still displayed an increasing size
with depth (i.e. with decreasing light levels) within that homothermal layer. Ultimately, this
indicates that there is a trade-off between occupying warmer waters where food and growth
conditions are favorable and avoiding predation and that predation avoidance is the primary
factor driving mysid vertical size distributions.
The existence of mysids with divergent migration strategies (paper III) further illustrates an
aspect of DVM which has been overseen in the past. Both ecological and genetic markers
indicate that a division into benthic and pelagic forms, i.e. resident and migrating individuals
is an environmentally induced plastic trait. We do not yet know which factors actually induce
these different behaviors or whether they are reversible or not, but buy looking at previous
studies on partial migration in e.g. fishes, we may suspect that some form of conditional cues
like growth rate and food availability may be responsible (Brönmark et al. 2008; Skov et al.
2010).
As mysids in the Baltic Sea have been shown to be food limited large parts of the year
(Mohammadian et al. 1997) and niche partitioning (via partial migration) is a way to decrease
competition, it is plausible that the observed benthic and pelagic forms of mysids may be
prevalent during times of low zooplankton availability. Consequently, we would expect the
proportion of migrants/residents to vary with food availability which in turn may affect
trophic dynamics. A recent paper by Brodersen and colleagues (2012) demonstrated that
seasonal partial migration by roach (Rutilus rutilus), i.e. a temporary migration away from
their natal habitat, induced a trophic cascade whereby zooplankton size and abundance
increased as a direct consequence of decreased zooplankton predation by roach. If partial
DVM in mysids has the same effect on trophic dynamics in the Baltic as in lakes, it will
become even more important to understand the circumstances under which alternative
migration strategies are formed and maintained as well as the quantification of migrants and
residents. Not only do our results put DVM of mysids in a new perspective but also in a more
general context as these findings open up for the possibility of partial migration being an
inherent life-history strategy in omnivorous diel vertical migrators per se.
Finally, paper IV presents the first model of respiration for a littoral mysid (Praunus
flexuosus) that despite its commonness and probable importance in Baltic coastal
communities has received undeservedly little attention in comparison to other species. The
study also demonstrates that the energy required for the processing of food (SDA) may be
present and reflected in respiration over a long period of time (duration and amplitude
depending on what and how much has been ingested) which may bias respiration values
unless accounted for. In the end, biased basal respiration rates will influence bioenergetics
model performance in a negative way (Chipps and Bennett 2002).
23
In conclusion, this thesis has covered many aspects of mysid biology and ecology. Behavior,
physiology, sampling methodology, and monitoring, which are all important factors for a
better understanding of mysids as integral components in the Baltic Sea ecosystem.
7. Acknowledgments
First of all, I would like to thank my wonderful supervisors, Sture Hansson, Elena Gorokhova
and Tomas Didrikas without whom I surely would have been lost. Sture, you have always
been there for me when things where rough, when echosounders were failing and data was
messy. Your positive spirit and great enthusiasm always kept me going. Thank you for
inspiring me and for introducing me to the world of science. Had it not been for that fisheries
biology course in 2002, I would probably have been doing something completely different
right now. I am still looking forward to that remote controlled airship project with mounted
lasers . We should do something about that Sture! Elena, I don’t know what kind of
batteries you are on but I sure would like to have some of them. I am still amazed by how you
manage to be “on-line” 24-7. No matter where you are and no matter what time, you always
take your time to help me and you always seem to have a brilliant idea in your pocket. The
trip to Chile was amazing and we should definitely go on more conferences together. Tomas,
sorry for all the late night calls during the hydroacoustic surveys. I was really going mad with
all the malfunctions and you really helped me out countless times. I have learnt so much from
working with you all and I hope that it won’t end here. So thank you for being such great
supervisors and most of all, wonderful friends!
Hedvig, what would I have done without you? Your super-memory kept me away from
calendars which I greatly appreciate because I never seem capable of using them anyway. I
feel privileged to have been able to share the office with you and having interesting
discussions not only about science but also about philosophy, art, your floating sauna projects
and Guinea fowl farms . The trips we made with Pelle and Ida through deserts and Rocky
Mountains, spiritual encounters with Cherokee cowboys, mountain lions and wild caught
rainbow trout sushi on the banks of the Dolores river…the climbing of an active volcano in
Chile, chasing rare frogs in the cloudy rainforest…those are the things that I always will
remember and keep close to my heart. Thank you guys for sharing these adventures with me.
To Jon, Annica, Maria, Micke and all the other colleagues at the department, thanks for
making my time here so much more pleasant and fun.
Thanks also to Ragnar Elmgren for being the open library that you are and for all the
interesting papers you put in my mailbox over the years, the staff at SMF Askö field station
(Suss, Mattias, Eva and Eddie) for all the late night cruises and help during the field work.
To my beloved family: Mamma, Pappa, Sandra, thank you for always believing in me and
supporting me throughout the years. I feel fortunate to have such a wonderful and loving
family and I couldn’t have done this without you! Jasmin my love, thank you for your
understanding, your love, and support! ♥.
The work in this thesis was funded by the Department of Systems Ecology, Stockholm
University, Stockholm Marine Research Centre (SMF) and the former Swedish Board of
Fisheries (Fiskeriverket).
24
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