UNIVERSITY OF LATVIA
ANDA IKAUNIECE
THE LONG-TERM DYNAMICS OF
MESOZOOPLANKTON IN THE GULF OF RIGA AND
THE BALTIC PROPER AND THE CONTROLLING
ENVIRONMENTAL FACTORS
Summary of thesis
for doctoral degree in biology (Specialty hydrobiology)
RIGA 2005
The general characteristics of the thesis
Importance of the Study
The Gulf of Riga is a relevant ecosystem in the environment of Latvia
therefore its protection and sustainable use of resources is a considerable
task for the Latvian environmental policy. During the second half of 20th
century remarkable changes occurred in the Gulf - the growth of nutrient
concentrations during the gradual eutrophication and the relatively drastic
drop of nutrient content in 1990s, the increase of air temperature during
winters due to the climate change and invasion of alien species. Thus a
question of biota reaction meeting the surrounding challenges is a prior one
to answer.The numerical and qualitative structure of pelagic communities is
determined by mutual action of abiotic factors combined with food supply
and relations of producers and consumers. As an element of planktonic
community zooplankton plays a role of the only link in the pelagic chain
between primary producers and pelagic consumers. Due to the wide feeding
scope - the possibility to utilize both large phytoplankton cells and tiny
flagellates, zooplankton organisms link the traditional food-web model
with the microbial loop. Thus the energy flow to the higher trophical levels
is secured, as well as the return of regenerated nutrients to primary
producers and bacteria.
The understanding of relation between abiotic factors and plankton
communities in the coastal zone is of large importance. The coastal zone
serves as a mid-region for the land and the open sea, receiving high nutrient
concentrations and potentially also increased content of any polluting
substances, which can have a negative effect upon the development and
growth of plankton organisms. The coastal regions and their inhabitants are
also the first to receive the impact of any climatic change.
The long-term systematic or monitoring observations are irreplaceable to
obtain the most truthful scene of ecosystem structure and its natural
variability, although immediate information on changes at the population
level is not available. Still the surveys of several years are necessary to
discover the tendencies of long-term changes.
After the inclusion of alien species into the ecosystem of the Gulf of Riga
during last 15 years, the controlling system of plankton community
dynamics has received an additional factor. Clarification of impact caused
by invasive species on native communities is also one of the important tasks
in the Baltic Sea defined by Helsinki Commission.
As a brackish water body the Gulf of Riga has a small number of species
therefore changes in abundance of even one single species can essentially
influence other parts of ecosystem. A detailed investigation of one species
(Bosmina longispina in this case) ecology in the particular water basin leads
to a better understanding of species -environment and species-species
relations.
The research themes of the thesis have been linked with the Latvian
National water monitoring programme "Marine environmental monitoring",
the joint project "Protection and sustainable use of biological resources of
the Gulf of Riga" (2001-2004), funded by Latvian Council of Science and
the EU project BASYS (1996-1999).
The main hypothesis of the thesis:
• Both the hydrological factors and the nutritive conditions have the
same importance when regulating the long-term dynamics of
zooplankton at all regions of the Gulf of Riga and in the Eastern
Gotland basin;
• The changes of North Atlantic climate are manifesting also in the
zooplankton community of the Gulf of Riga.
• The abundance dynamics of cladoceran Bosmina longispina in the
Gulf of Riga is determined by the hydrological situation.
The tasks of the study:
1. To analyse the long-term tendencies of zooplankton abundance and
species structure, identifying their relation to dynamics of abiotic and biotic
factors in the Eastern Gotland basin, at the open and coastal areas of the
Gulf of Riga.
2. To investigate the effect of North Atlantic climate change on zooplankton
community dynamics at the open and coastal areas of the Gulf of Riga.
3. To clarify the seasonal dynamics of the most characteristic coastal
zooplankton species and identify the controlling environmental factors;
4. To investigate the patterns of distribution and dynamics of the dominant
summer species in the Gulf of Riga - Baltic Sea cladoceran Bosmina
longispina.
The novelty
The Gulf of Riga differs from the rest of the Baltic Sea areas with the
salinity and thermal regimes and particularly with the ratios and seasonal
variation of nutrients, which on its turn influence all links of the food-web.
Thus the conclusions on long-term environmental variation drawn for the
other parts of the Baltic Sea are not applicable for the Gulf and separate
investigations are needed. Therefore for the first time:
* the long-term dynamics of Gulf of Riga coastal zooplankton has been
numerically related to the environmental variables;
* the trends of the dominant coastal zooplankton species (Bosmina
longispina, Synchaeta baltica, Keratella quadrata) have been identified and
the regulating factors estimated;
* the response of zooplankton community on the changes of composition
and abundance in food supply - phytoplankton concentration - at early
1990s has been investigated;
* the life strategy features of cladoceran Bosmina longispina in the Gulf of
Riga have been clarified.
Aprobation
The results of the research have been presented at the following
international conferences: ICES Symposium "The temporal variability of
plankton and their physico-chemical environment" (Kiel, Germany, 1997),
"Comparison of enclosed and semi-enclosed marine systems: Biological,
physical and (geo)-chemical features and processes and Responses to
altered environmental conditions"(Mariehamn, Finland, 1997), "Secotox 97,
Ecotoxicology and Environmental Safety" (Jūrmala, Latvia, 1997), ICES
Symposium "Brackish Water Ecosystems" (Helsinki, Finland, 1998), 2nd
BASYS Annual Science Conference (Stockholm, Sweden, 1998), "The
Changing Coastal Oceans: From Assessment to Prediction" (Warnemünde,
Germany, 1998), 16th Baltic Marine Biologists Symposium (Klaipēda,
Lithuania, 1999), 3rd BASYS Annual Science Conference (Warnemünde,
Germany, 1999), ICES Young Scientists Conference (Gilleleje, Denmark,
1999), "Baltic Sea Science Congress 2001 - Past, Present and Future - A
Joint Venture" (Stockholm, Sweden, 2001), 3rd International Zooplankton
Production Symposium (Gijon, Spain, 2003), "Baltic Sea Science Congress
2003" (Helsinki, Finland, 2003), ICES Annual Science Conference (Tallinn,
Estonia, 2003).
Publications - the main results of the thesis are summarised as 4
publications in international series.
Author's input
The author has collected and counted the zooplankton samples of 19932001. Data of 1970-2002 have been statistically treated and analysed. The
estimation of impact of the abiotic factors has been performed. The samples
of the resting eggs have been collected and counted, the obtained data
treated and analysed. The first author of three of four published papers.
The volume and structure of the thesis
The thesis has 82 pages, 15 tables and 33 figures. The work consists of six
chapters: Introduction, Literature Review, Aim and Objectives, Material
and Methods, Results, Discussion. The main results are summarised as
Conclusions. The List of References contains 158 sources.
35
The most essential results and conclusions are compiled as the Summary in
Latvian and English.
Material and methods
Study areas
a) Gulf of Riga
The Gulf of Riga is located at the eastern part of the Baltic Sea and is the
third largest gulf. It differs from the Baltic Proper having two times smaller
mean depth of 26 m. The deepest place in the centre of the Gulf is 62 m.
The Gulf is reatively isolated and the water exchange occurs through two
straits -Muhu Strait with average depth of 4,5 m and width of 6-27 km, and
Irbe Strait with average width of 30 km. Therefore the mean time of water
exchange is 2 - 4 years. The Gulf is under a strong freshwater impact as 5
comparatively large and approx. 30 smaller rivers bring 31 km of freshwater
per year, making 7,3% of the Gulfs total volume. This indicator is 3 times
higher than in the Baltic Sea. Thus the relative shallowness of the Gulf
determines the characteristic annual hydrological regime - during the cold
part of the year the Gulf is homogeneous and has no halocline. The salinity
is decreased compared to the Baltic Sea due to the limited water exchange
and large freshwater flow and varies between 5.2 to 6.7 PSU (Pastors, 1975,
Берзиньш, 1980, Berzinsh, 1995, Berzinsh and Zacharchenko, 1996).
However, the Gulf is not regarded as homogeneous and has five regions
with different depth and hydrological regime (Берзиньш, 1987). The
network of sampling stations has been created to represent these regions
evenly (Fig.l). Besides, the coastal zone has its particular properties,
although not clearly distinguished by geomorphological features. The
coastal zone in the Gulf is estimated by the isoline of 10-12 m. There the
stations are located against the river mouthes and largest inhabited places i.e. the potential sources of pollution and in reference areas (Fig.2).
Fig.l. The network of stations at the open part of the Gulf of Riga
Fig.2. The stations at the coastal area of the Gulf of Riga.
b) the Gotland Deep in the Baltic Sea
The Gotland Deep is located at the central part of the Baltic Sea, it is the
largest deep of the sea with a depth of 249 m (Tep3neB H flp., 1992).
Halocline, occurring approx. at 70 m depth, divides the whole water layer
there into the upper layer under strong impact of freshwater and
meteorological conditions, and more saline deeper layer, receiving inflows
from the North Sea. During the warm part of the year the upper layer is
separated with thermocline at m 15-25 m depth into warm mixed layer and
cold middle layer. The mean temperature of the upper layer fluctuates from
-0,2°C in winter to +16°C in summer, in the deeper layer below the
halocline it is +4- +6°C all the year. The salinity in the upper layer is 7.2-7.7
PSU, in the deeper layer - 10-12.7 PSU. The annual salinity fluctuations are
small and do not exceed 0.5-0.7 PSU (Tep3HeB H up., 1992).
At the Gotland Deep the investigations were fulfilled at one station in the
eastern part (Fig.3). The station depth was 240 m and thus all the
hydrological properties of Gotland Deep were present there.
Fig. 3. The station at the Eastern Gotland of the Baltic Proper.
c) areas of benthic investigations
In the Gulf of Riga during the convective mixing the fine material settled in
spring and summer is resuspended in autumn and transported to the
accumulation bottoms. Main accumulation bottom zone is at 40 -50 m
depth, almost all of it situated in the southern or southwestern parts of the
Gulf. More shallow areas then are transportation or transportation/erosion
bottoms (Carman et al., 1996).
The sampling of Bosmina longispina resting eggs was performed at two
different locations of the Gulf of Riga - coastal and offshore, representing
transportation and accumulation bottoms, respectively. The transportation
bottom station was 21 m deep and the sediment composition was sand and
coarse sand mixed with detritus. No signs of oxygen deficiency in the
sediment were observed during sampling. The station representing the
accumulation bottom, was 44 m deep. The sediment consisted of soft mud.
The oxidized layer was the upper 2 cm there.
Sampling and treatment of mesozooplankton samples
a)
pelagic samples
Zooplankton samples were collected with two types of nets. Juday net was
used till 1993. This type of net was widely used for oceanologic
investigations of zooplankton in the former USSR but in none of the rest
countries around the Baltic Sea. When Latvia became involved into the
monitoring programme of the Baltic Sea, since 1993 zooplankton samples
are collected with WP-2 type net (UNESCO, 1968). WP-2 type net is
regarded as the only possible type for monitoring in the HELCOM
COMBINE Manual (HELCOM, 1998). Till 2001 part of the sampling was
done in parallel with both nets.
The further treatment of the sample does not differ according to the type of
net. Samples were collected in separate water layers: 0-10 m, 10-20 m, 2040 m, 40-50 m in the open part of the Gulf and 0-10 m in the coastal areas.
In the Baltic Proper the sampling layers were 0-25 m, 25-50 m and 50-100
m. Since 2001, layer of 0-40 m is sampled in the open part of the Gulf.
Immediately after collection samples were fixed in 40% formaline. For
subsampling Stempellpippette was used and organisms were counted in a
Bogorov's chamber (Богоров, 1947) under binocular microscope.
Organisms were identified to species or lowest taxonomic level possible,
development stage and sex were determined for copepods. Calculation of
species and also total biomass differed according to the net type. For Juday
net samples individual weight factors collected from various references
were used and seasonal variation was not taken into account. For WP-2 net
samples factors were used elaborated for Baltic Sea monitoring programme
(Hernroth, 1985) and having different values for Baltic Sea regions and
seasons.
Since 1992 sampling was performed 3-8 times in the open part and 4-9
times per year in the coastal zone of the Gulf (Figs. 1, 2). Till 1994 samples
were collected four times a year in the Latvian Baltic Sea zone. In 19761990 sampling and counting of samples of the Baltic Proper and the Gulf of
Riga was carried out by Latvian Fish Resources Agency. Samples were
collected 3-4 times per year to cover every season. At the coastal areas
sampling and counting of samples three times a year - in May, August and
October in 1982-1992 was fulfilled by Latvian Hydrometeorological
Agency.
b)
sediment samples
The dynamics of B.longispina resting eggs was studied from April till
September in 2001. Sampling of the resting eggs was performed at two
different locations of the Gulf of Riga - coastal and offshore, representing
transportation and accumulation bottoms, respectively. The sediment
samples were collected once a month from April till September and at the
offshore station till December.At the coastal station Van-Ween benthos grab
was used and Kajak gravity correr at the offshore to take three samples
every time. A plastic ring with an identical diameter to the correr's - 80 mm
was used to obtain the core from the grab. The upper slice of 0-2 cm of the
core was used for further treatment. Sediment samples were sieved through
0.2 mm and 0.1 mm sieves and fixed with 4% formaline immediately. In
laboratory the samples were rinsed to remove the formaline. The resting
eggs were counted under stereomicroscope (20-26x magnification).
Datasets of environmental factors
For the description and impact analysis of the environment in the Gulf and
Eastern Gotland the datasets of Marine Monitoring department, Institute of
Aquatic Ecology were used. Following parameters were considered:
hydrological - water temperature, salinity, oxygen concentration;
hydrochemical - concentration of inorganic nitrogen, phosphates and
silicates; hydrobiological - content of chlorophyll a, phytoplankton species
composition, abundance and biomass.
For the investigations of more global North Atlantic climate impact the
North Atlantic Oscillation index was used. The positive values of index
indicate stronger westerlies over the middle latitudes (Hurrell, 1995). NAOI
winter data of 1980-2002 from Hurrell database (Hurrell, 1995 un
http://wwvv.cgd.ucar.edu/~ihurrell) were used as the mean values of
December-March monthly means.
Zooplankton data analysis
Abundance and biomass of separate zooplankton species and also the total
values were calculated as ind.m-3 and mg m-3, respectively, for 0-40 m layer
in the Gulf and 0-100 m layer in the Baltic Proper. The normal distribution
of the data was checked and in cases not reached, the data were transformed
as logarithmic values. To evaluate the significance of differences between
the stations t-tests and Levene's tests were used for the determination of
dispersion homogeinity.
The mean abundance of resting eggs for each station in every month was
calculated and expressed per m2. The sinking velocity of the eggs was
calculated according to Stokes' law
F = 6πaηv,
where F is drag force, a is radius of a particle, η is viscosity and v is velocity
of the particle. At the same time
6πaηv = (4/3)7ta3pg,
where p is density. This equation was used for calculating the sinking
velocity. The dimensions of resting eggs, found by by Viitasalo and
Katajisto (1994) were used.
For the trend detection of zooplankton abundance and finding the relations
with the environmental factors a linear regression analysis was used. The
distribution normality of residuals was also checked when evaluating the fit.
In addition for the trend determination a non-linear regression model with a
breakpoint was used. The non-linear regression was performed in cases
when the relationship between the environmental variables and time proved
to have the year of discontinuity (=breakpoint). In this case the fitted model
was:
Y= B0+B1 *X+B2*(X-Breakpnt)*(X>Breakpnt),
where BO is the intercept, Bl the slope of the first section, B2 the difference
in slope between the first and the second sections, and Breakpnt the
calculated breakpoint between the first and second sections (StatSoft,
Inc.1995). The fits of the models were evaluated according to distribution of
the residuals.
A Pearson correlation was used when estimating relationship of zooplankton
community and environment variation. However, the correlation just allows
to judge whether the null hypothesis on covariation non-existance between
the data sets could be rejected. Therefore in further investigation the multiple
regression was used to determine the possible connections of environmentals
variables and particular species.
For the study of relation between zooplankton community and climate
variation of North Atlantic scale cluster analysis and multidimensional
scaling were used. Hierarchycal and k-means types of cluster analysis were
chosen to evaluate the possible grouping of the data. Multidimensional
scaling was considered in cases when normal distribution of data was
impossible to reach.
The data treatment and analysis were performed with the help of software
STATISTICA 5.0 (StatSoft, 1995).
Results and discussion
The long-term dynamics of zooplankton community at the open part of
the Gulf of Riga and the Eastern Gotland basin of the Baltic proper
The long-term changes of zooplankton in the Gulf of Riga and Baltic proper
have been considered and described several times, however as the collection
and accumulation of data has continued, there is a necessity for periodical
reviews of long-term trends in the community.
In the Gulf of Riga during the summers of 1970 -1995 the dominant species
by biomass were the copepods Eurytemora affinis, Acartia bifilosa and at the
beginning of 1970s - also Limnocalanus macrurus. Bosmina longispina had
the highest biomass in the group of cladocerans. The total values of biomass
fluctuated widely - from 400 to 1300 mg m-3. Species structure, however,
did change - the most considerable expressions were the growth of herbivors
E. affinis (till 1985) and B. longispina (gradually during the whole period)
together with simultaneous drastic decrease of L.macrurus. Dynamics of
total zooplankton biomass did not indicate a linear tendency, but had
smaller periods with differing directions - increasing in 1977-1983, varying
in 1984-1990 and decreasing in 1991-1995.
The only significant correlation found between zooplankton biomass and
environmental factors was the positive one with chorophyll a concentration
in 1972-1983 - r2= 0,64 (p=0,003, n = l l ) and in 1984-1990 - r2= 0,70
(p=0,04, n=6). After 1991 when the plankton communities indicated a
decrease of their biomass, correlation with chlorophyll a became even
stronger - r2= 0,89 (p=0,04, n=7). So in summers of 1970-1995 the
dynamics of plankton communities were similar and obviously related
(Fig.4). During the growth periods of 1977-1983 and 1984-1990 the
phytoplankton biomass had a positive correlation with total phosphorus
concentration - r2 = 0,63, p = 0.06, n=7 and r2 = 0,63, p = 0.03, n=7,
respectively. No relation was found after 1990.
Fig.4. The long-term dynamics of total biomass of plankton communities in
the Gulf of Riga, August 1970-1995.
A move towards dominance of herbivors in 1970-1990 most probably was
the response of zooplankton community on the increasing eutrophication of
the Gulf during this period. In 1991-1995 the change of nutrient ratio as a
growth of total phosphorus could be partly caused by high abundance of
Bosmina in 1988-1990 with increased nitrogen assimilation. Quite stable
concentration of nitrogen and thus the change of N:P ratio in the Gulf was
observed since 1990. To maintain the stoichiometric balance in the nutrition
environment with fluctuating C:P or N:P ratios zooplankton has to adjust its
growth strategy with effective use of limiting nutrient and fast release of
the excess one (Pertola et al., 2002).
The growth of total phosphorus content after 1990 favoured more intense
development of nitrogen fixating cyanobacteria, thus worsening the
nutrition and reproduction conditions for zooplankton. Kiorboe & Nielsen
(1994) have observed in the southern Baltic Sea that production of copepod
eggs is possible only when concentrations of diatoms and other
phytoplankton species with large cells are high but the share of flagellates
in the food of copepods is small. B. longispina, on its turn, was the species
better adjusted to the change of food composition - the cyanobacteria are
utilised as essential diet component and the species development is secured
(Pel et al., 2003).
The drastic decrease of Limnocalanus macrurus has been explained several
times by the impact of eutrophication - the drop of oxygen content under
the thermocline in summer (e.g. Костричкина и др., 1990). However, after
the improvement of situation in late 1990s, the restoration of population did
not occur indicating the role of other than abiotic controlling factors. Hirst
and Kiorboe (2002) have calculated that 60-75% of mortality of planktonic
copepods is determined by predation. In the Great Lakes of North America
where also the relation of L.macrurus abundance to the eutrophication
intensity was found, a similar maintenance of depressive abundance level
has been observed due to intensive fish predation (Kane et al., 2004). The
negative correlation of L. macrurus abundance and the herring stock in
1970-1990 (Sidrevics et al., 1993) also indicates the additional predation
control of population.
Analysis of zooplankton long-term dynamics (1976-1996) in all seasons of
the year at three different areas in the Gulf and Eastern Gotland did not
show so clear link to the phytoplankton community variations anymore.
The list of dominant species in the Gulf is replenished by rotifer
representatives Synchaeta spp. and Keratella spp., still the share of
crustaceans in the total biomass has been the highest - 51-99% in spring
(May), 84-97% in summer (August) and 68-100% in autumn(OctoberNovember). Regarding any tendencies of biomass dynamics, in the central
part of the Gulf spring biomass indicated a bimodal trend with positive
direction in 1976-1990 and the opposite on after 1990 (Table 1).
Table 1
Results of breakpoint regression analysis of zooplankton spring biomass at
the central part of the Gulf of Riga, 0-50 m layer
n
B0
t
P
20
-1510,64
-3,23
0,01
Bl
t
P
B2
t
P
Breakpnt(year)
t
P
0,77
3,24
0,01
-2,71
-0,53
0,63
1990
263,42
<0,001
During the growth period biomass correlated positively with water
temperature in 0-20 m layer - r2=0.70 (p<0,0001, n=13). However, any
more significant changes of zooplankton biomass or relation to
environmental factors and phytoplankton abundance were not found
(Fig.5).
Fig. 5. Variation of zooplankton total biomass (g m-2 ) at the central part
station of the Gulf of Riga, 0-50 m layer in three seasons of 1976-1996.
For the same time period in the Eastern Gotland the list of abundant species
was longer - Acartia longiremis and A. bifilosa, Pseudocalanus elongatus,
Temora longicornis, Centropages hamatus, Eurytemora affinis, Synchaeta
spp and appendicularian Fritillaria borealis, in summers - Bosmina
longispina. Still the biomass of crustaceans formed the largest part of the
total amount - 45-98% in spring, 94-99% in summer and 87-99% in
autumn. In the long-term aspect the spring biomass varied considerably,
still after 1990 its drop was observed due to the decrease of P. elongatus
abundance. Also there the positive correlation with water temperature (0100 m layer) was determined - r2=0.73, p=0.001, n=11. Summer biomass
did not indicate any significant tendencies but clear linear decrease was
stated in autumn - r2=0.44, p=0.01, n=12 (Fig.6). The autumn biomass was
vaguely related to the changes of salinity - r2=0.27, p=0.08, n=12.
Fig.6. Variation of zooplankton total biomass (g m-2 ) at the Eastern
Gotland, 0-100 m layer in three seasons of 1976-1994.
In Eastern Gotland due to the drop of nutrient concentrations, the
dominating diatoms in the spring phytoplankton community were replaced
by dinophlagellate Peridiniella catenata. In summer the decrease of
inorganic nutrients caused drastic drop of phytoplankton biomass, later
compensated by intense development of nitrogen fixating cyanobacteria.
So the changes of water trophy did not have a clear reflection in the
dynamics of zooplankton community neither in the both areas of the Gulf
of Riga, nor in the Eastern Gotland. The impact of hydrologic factors was
more obvious. Salinity decrease in Eastern Gotland (Table 2) caused the
drop of Pseudocalanus elongatus abundance since mid-1980s and the
increase of Bosmina longispina numbers since late 1980s what corresponds
with the conclusions of Vuorinen et al. (1998) on change of
Copepoda/Cladocera biomass ratio in favour of Cladocera at the northern
part of the Baltic Sea.
Table 2
The long-term dynamics of salinity at the Eastern Gotland and two areas of
the Gulf of Riga
Region
Eastern Gotland
Central part of
the Gulf of Riga
Southern part of
the Gulf of Riga
Winter
R = -0.89,
p <0.001,
n=19
R=-0.78,
p=0.002,
n=13
R = -0.74,
p=0.01,
n=12
Spring
R=-0.88,
p< 0.001
n=19
R = -0.76,
p<0.001,
n=22
R = -0.29,
p=0.21,
n=21
Summer
R = -0.62,
p=0.01,
n=18
R = -0.67,
p=0.001,
n=22
R = -0.42,
p=0.05,
n=22
Autumn
R=-0.56,
p=0.03,
n=16
R=-0.60,
p=0.01,
n=21
R=-0.50,
p=0.02,
n=21
Although also in the Gulf of Riga salinity decreased for 1 PSU during 20
years (1976-1996) the species structure did not respond with significant
changes. The decrease of Limnocalanus macrurus was not related directly to
salinity dynamics and also did not impact the level of total biomass. This 1
PSU change still fitted in the optimal conditions for brackish water species
of the Gulf.
The vague link with salinity could be also due to predation of planktonic fish
and mysids, especially at the end of summer and in autumn. Flinkman et al.
(1992) and Viitasalo et al. (1999) have proved that herring first-rate preys are
Temora longicornis in the Baltic Proper and Limnocalanus and Eurytemora
in more limnic bays. In the Eastern Gotland the predation by Pleurobrachia
pileus on copepods can be additional controlling factor (Graneli & Turner,
2002).
For the investigation of possible larger scale impact - the effect of North
Atlantic climate dynamics - spring and summer zooplankton biomass in
1980-1998 and NAO winter index values of the same period were used.
Total zooplankton biomass did not have any significant relation to NAO
fluctuations at any season (Table 3). The same was true for the abundant
spring zooplankton groups - rotifers and copepods.
Positive link with NAO index dynamics was determined for the cladocerans
as the dominant group of summer (Fig.7, Table 3).
Fig.7. Dynamics of cladoceran biomass (mg m-3 ) in August and NAO
winter index, 1980-1998.
Table 3
Relation of zooplankton biomass in the Gulf of Riga and NAO index (the
significant correlation in bold)
Variable
1980-1998
Total spring biomass
Copepoda biomass
Rotatoria biomass
Total summer biomass
Claducera biomass
R
R2
P
n
0.26
0.16
0.35
0.38
0.53
0.07
0.03
0.12
0.15
0.28
0.31
0.53
0.17
0.10
0.02
17
17
17
19
19
The results of cluster analysis show the separation of cladoceran summer
biomass as two main groups (Fig.8).
Fig.8. Clusters of cladoceran summer biomass (mg m-3 ) in 1980-1998.
Similarly to the macrozoobenthos of the Gulf (Dippner & lkauniece, 2001)
the impact of North Atlantic scale climate variation has not been very
obvious on the zooplankton community dynamics. Thus the importance of
local atmospheric situation prevails upon the larger scale - North Atlantic
circulation. Extremaly negative NAO deviations - severe winters with ice
cover in the Gulf- are the only signals common for the Gulf of Riga and
North Atlantic. The occurrence of ice is a strong signal of environmental
change delaying the development time of thermophylic species like
cladocerans and therefore negative NAO deviations are related to smaller
population abundance. Also the results of cluster analysis reveals the
population abundance according to the winter conditions - after severe
winters (1985, 1987, 1994, 1996) the numbers have been lower and higher
after the warmer ones, respectively. The direct link with water temperature
in winter for the abundance of cladocerans in summer is still impossible to
detect due to the shortage of winter data.
The long-term dynamics of zooplankton community at the coastal areas
of the Gulf of Riga
The first study concentrated on the long-term dynamics of zooplankton in
1982-1996 at the southern coast of the Gulf opposite the mouthes of three
rivers and the inflow location of Riga wastewater treatment plant. The aim
was to clarify whether the potential pollution sources had affected the
coastal zooplankton. Also the impact of environmental factors on
zooplankton dynamics was analysed. In total 27 identified zooplankton
taxons were present both at the coastal areas and open part of the Gulf and
species composition did not differ between the stations. Copepods were
represented by 5-6 taxons, cladocerans - also by 5-6 taxons although
Daphnia spp. was observed just episodically. Since 1992 the invasive
species Cercopagis pengoi has been found in the samples still in low
numbers (5-50 ind. rrf ). The groups of rotifers consisted of 6-7 taxons and
the rest of species was mostly of meroplankton - the larvae of the benthic
invertebrates. The larvae of polychaetes have been occurring since 1989.
Although not identified to species, most probably they were the planktonic
stage of then recently introduced polychaete Marenzelleria viridis
(M.Ceitlina, pers. comm.).
The seasonal dynamics of zooplankton groups followed a similar pattern
during the observation period - copepods or rotifers were the most abundant
ones in spring and autumn, cladocerans and rotifers - in summer. The
amount of meroplanktonic organisms was quite low during all seasons.
Zooplankton abundance in summer was always higher than in spring and
autumn (Fig.9).
Fig.9. The total abundance of zooplankton (ind. m-3) at the coastal areas of
the Gulf of Riga, 1982-1996, the mean value from 4 stations.
Results of Pearson correlations between zooplankton abundance (both in
groups and the total) and environmental factors at each station are
compiled as Table 4.
Table 4
Pearson correlation coefficients of zooplankton abundance and
environmental factors' correlations at the coastal stations opposite the river
mouthes in 1988-1996. Coefficients are multiplied by 100 and the values
with significance level p<0.05 are in italic.
The seasonal dynamics of coastal zooplankton in 1982-1996 did not differ
from the open part patterns (Kostrichkina, 1996; Line & Sidrevics, 1995)
although the environmental situation is more variable (Кице и др., 1979).
Copepods and rotifers are the dominant groups in spring and autumn at
both areas of the Gulf. The summer ratios of copepods, cladocerans and
rotifers differ as the share of copepods is lower at the coastal zone. The
reason could be found in the various life cycle strategies of these groups.
Cladocerans and rotifers can be regarded as „r selective", being more
adaptive in seasonally pulsed environments whether copepods are more
like „K selective", not so
depending on sharp short -term changes, but reproducing slower with a
wider seasonal distribution (Allan, 1976).
The difference in number of taxons found (27) from the referred ones - 132
(Лагановска, 1974) or 39 (Simm, 1995, north-eastern part of the Gulf)
could be due to the various sampling strategies (distance from the river
mouth, frequency of sampling) and the level of identification, as in present
study Cyclopoida and Daphnia were not identified to species.
In spring zooplankton abundance was influenced by water temperature,
correlating positively with amount of copepods and cladocerans. The
vaguely expressed effect of water temperature on rotifer abundance could be
due to too low sampling frequency. A negative correlation of copepods with
salinity in spring has been stated also in the coastal area of the northern
Baltic Sea (Vuorinen & Ranta, 1987; Viitasalo, 1994). The effect of very
small changes in salinity (approx. 1 PSU) upon abundance of Eurytemora
affinis has been observed, thus indicating E.affinis to be a strictly brackishwater organism.
In summer the observed positive correlation between cladocerans and
salinity, and the corresponding negative one with temperature could be due
to the dominance of Podon polyphemoides in several years, as the species
prefers more saline and colder environment (Ackerfors, 1969; Viitasalo,
1994). The coincidence of low cladoceran abundance (too late sampling in
summer) with a decreased salinity due to wind activity or increased river
run-off might be another reason for the positive cladoceran-salinity relation.
The coastal zooplankton abundance in summer and autumn was higher than
in the open part of the Gulf thus suggesting that no chronic unfavourable
environmental situation was present at the potential risk zones. Also
zooplankton community had not shown signs of any species extinction or
drastic decreasing abundances.
The next study involved the analysis of dynamics of the dominant coastal
species - Bosmina longispina, Synchaeta baltica and Keratella quadrata for
a bit longer time period till 1997, taking into account that the abundance of
zooplankton in the open part of the Gulf has decreased after 1990. The
seasonal occurrence of the species was different as B.longispina and K.
quadrata were present mostly in summer but S. baltica - from spring till
autumn (Table 5).
Table 5
The descriptive statistics of mesozooplankton species abundance (ind.m-3)
data from three coastal stations.
Species
Mean
abundance
Min
abundance
Max
abundance
n
Bosmina
longispina
80100
200
405000
46
Keratella
quadrata
29850
400
195000
48
Synchaeta
ballica
spring
summer
autumn
10590
8380
11430
100
170
140
73400
150000
61750
39
40
41
Regarding the abundance trends only directed tendency was estimated for
S. baltica in autumn - r =-0.62, p<0.02, n =13. Abundance B. longispina, K.
quadrata and S . baltica of other seasons just reflected the interannual
variation without any tendencies. The comparison of mean values and
variance of the each species abundance in time periods 1982-1990 and
1991-1997 revealed no considerable differences thus the hypothesis of
numerical decline of zooplankton also in the coastal zone after 1991 was
rejected.
Statistically significant correlation was estimated only between the summer
salinity and the abundance of B.longispina. K.quadrata though showed a
negative correlation with summer salinity. The abundance of S.baltica had
only non-significant correlations with the environmental factors.
Consequently, in multiple regression analysis only the abundance of
Bosmina was included. Temperature and salinity together gave more
information and could explain 61% of Bosmina abundance variation (Table
6).
Table 6
Pearson product moment correlation and multiple regression coefficients
between the environmental variables and the mesozooplankton species
abundance (log10(x+1) m-3).
Species
Variable
Ror
multiple R2
(*)
Bosmina
longispina
Keratella
quadrata
Temperature
0.61*
Salinity
Temperature -0.51 Salinity
0.22
Synchaeta
baltica
Spring
Temperature -0.20 Salinity
0.20
Partial
correlation
Semi-partial
correlation
0.68
0.77
0.57
0.76
P
0.06
0.02
0.93
0.30
0.70
0.70
Summer
Temperature -0.18
Salinity
0.24
0.62
0.53
The lack of abundance trends could be attributed to the unsteady
environment and the predation pressure. In the coastal areas the wind
activity in summer causes the main circulation of the water masses through
upwellings when the water from the deep parts of the Gulf is lifted up at
the shore. Thus depending from the sampling moment coastal zooplankton
community can contain just deep water few specimen or it can have an
outburst of rotifers and cladocerans. As suggested by Conde-Porcuna and
Declerck (1998), the effect of predation mostly may be indirect by
selective predation on reproductive females or by inducing longer caudal
spines against predation which are associated with metabolic and
demographic costs. Planktivorous fish larvae densely occupy the coastal
areas of the Gulf (Latvian Fishery Yearbook, 1997). Rajasilta and
Vuorinen (1987) have found that in an eutrophic area the fish larvae
selected the largest prey species (copepods) and cladocerans were
preferred only when the abundance of copepods was low. In the area under
question the share of cladocerans is higher than of the copepods therefore
the importance of Bosmina as a food item for fish larvae should be taken
into account.
The interactions with the benthic communities must also be considered as
a source of zooplankton variability. As all investigated species produce the
resting eggs then effect of benthic fauna can have contrary directions: the
consumption of eggs and the transfer of the eggs to surface for hatching.
Viitasalo (1994), however, suggests that the net effect of the benthic
animals on the hatching of mesozooplankton resting eggs may be positive.
That could be true also for the Gulf of Riga because the potential destroyer
of the eggs - the amphipod Monoporeia affinis has small abundance
numbers in the coastal zone (Gaumiga and Lagzdinsh, 1995).
The positive correlation of B.longispina and salinity contradicts to other
observations from the Baltic Sea (Vuorinen and Ranta, 1988; Viitasalo et
al. 1990). In this case the deviations of salinity coincide with the variability
of Bosmina (Fig. 10).
Fig.10. Variation of B.longispina abundance (log10 (x+1) ind m-3) and
salinity (PSU) at the coastal areas of the Gulf of Riga, mean value from 3
stations in July-August, 1982-1997.
However, a negative salinity anomaly means increased river inflow and
consequently the stratification of the water column as the freshwater stays in
the upper layer. Thus the water mixing is prevented and according to
Viitasalo and Katajisto (1994) may be also the hatching success of the
resting eggs. The higher river run-off besides indicates higher nutrient
concentrations, higher phytoplankton abundance and following higher
sedimentation which can cause the burial of the eggs. The positive
correlation of B.longispina with water salinity also supports the idea of too
low salinity (2 PSU) being even harmful to species since the number of
individuals is small (Purasjoki, 1958).
Existing, but non-significant negative correlation between Keratella
quadrata and the salinity most probably indicates the freshwater origin of
this species and also the shortage of observations for analysis. The
abundance of Synchaeta baltica in spring should be more controlled by
water temperature than the correlation reflects. After cold winters (IAE,
unpublished data) when Gulf has been covered with ice, this species is
either missing (like in 1985) or has low abundance (in 1987, 1991). Lower
abundance of S.baltica in summer than in autumn can be due to food quality
- phytoplankton species composition. Johansson (1987) observed the
increase of Synchaeta population when the phytoplankton was dominated by
large diatoms. The decrease of long-term amount of S.baltica in autumn can
be associated with the decline of autumn phytoplankton biomass containing
less large diatoms in 1990s (Kalveka et al., 2002).
Like in the open areas of the Gulf the climate variation of North Atlantic
scale has not influenced the dynamics of summer zooplankton (the best data
coverage) total abundance, at least not directly. Also the analysis of separate
species and taxonomic groups, dominant in summer - Bosmina longispina,
Keratella quadrata, Copepoda- did not indicate any significant relation with
winter NAO index (Table 7). Still, the signals of very well expressed
climatic phenomena - mainly as the very cold winters in 1987, 1991, 2001 are seen also in values of zooplankton amount (Fig.l 1).
Table 7
Results of Pearson correlation between coastal summer zooplankton
abundance (log10 (x+1) ind m-3 ) and NAO winter index
Variable
R
R2
P
n
Total abundance
0.16
0.03
0.48
21
Copepoda abundance
0.01
0.00
0.98
20
Keratella quadrata abundance 0.14
0.02
0.53
21
Bosmina longispina abundance 0.37
0.14
0.10
21
Fig. 11. Dynamics of the coastal zooplankton total abundance (log10 (x+1)
ind m-3 , mean of 3-5 stations) and NAO winter index 1982-2002.
The results of cluster analysis for abundance of B.longispina, similarly to the
open part, indicate two main groups of years (Fig. 12). Multi-dimensional
scaling shows the groups of the years depending on the water temperature in
spring (Dimension 1) and water stability in summer (Dimension 2) (Fig. 13).
Fig. 12. Clusters of B.longispina abundance (log10 (x+1) ind m-3 ), August
1982-2002.
As already stated concerning macrozoobenthos at the coastal areas of the
Gulf of Riga (Dippner & Ikauniece, 2001), the determination of climate
deviations in direct relation to biotic elements is difficult due to the
fluctuating environment and the species structure with the dominating „r
type" species. For example, in 1996 simultaneously with the lowest NAOl
value, the second highest abundance of Keratella sp. in 1982-2002 was
observed, consequently increasing the level of total zooplankton numbers.
Thus also only the cladoceran abundance revealed any grouping of years in
the cluster analysis, as the winter conditions through water temperature
regime determine the timing for the resting eggs to hatch. Multi-dimensional
scaling points out additional moment - the stability of water masses
affecting the community distribution in the Gulf. Upwellings which are
caused by wind activity change not only the water temperature, but also the
species composition, their numerical values and modify salinity and food
conditions.
Fig. 13. MDS analysis of B.longispina abundance (log10 (x+1) ind m-3 ) in
summer, 1982-2002.
Life cycle and dynamics of cladoceran Bosmina longispina in the Gulf
of Riga
The dynamics of B.longispina resting eggs was studied from spring till
autumn in 2001, comparing the abundance of the resting eggs at two
different locations of the Gulf of Riga - coastal and offshore, representing
transportation and accumulation bottoms, respectively. Abundance of the
resting eggs was the highest in April at both stations, although at the
offshore station it was approx. 7 times larger. A rapid decrease occurred
from April till May at the offshore station when the number of resting eggs
diminished for 15 times. The abundance of resting eggs somewhat
increased also in June and September at the offshore station. At the coastal
station the spring decrease was about for 2 times and the number of resting
eggs remained almost on the same level throughout the summer. No
expected increase was observed in December. In the pelagic zone the first
few specimen of Bosmina longispina were observed already in February at
the offshore station and at the end of April - in the coastal station. An
intense development of B.longispina started at the end of May and
beginning of June at both stations. At the time of maximum development
the numerical values were 2 times higher at the coastal station. The decline
of abundance was very steep and occurred during two weeks at the end of
July and beginning of August (Table 8).
Table 8
Bosmina longispina abundance dynamics in the Gulf of Riga, 2001
Date
24.02.
14.03.
29.03.
11.04.
27.04.
9.05.
18.05.
16.06.
27.06.
17.07.
25.07.
10.08.
29.08.
06.09.
Ind. m-3 open
part
16
8
4
12
18
80
64
702
455
36300
26796
65
28
14
Date
24.04.
9.05.
30.05.
14.06.
16.07.
7.08.
4.09.
Ind.m-3 coastal
part
24
189
690
1862
63357
192
78
When comparing the time of B. longispina occurrence in plankton in 19932002 no big differences are observed between the coastal and open areas,
in most cases it has happened simultaneously (Fig. 14). The timing of an
intensive species development shows some distinction, though.
Fig. 14. The appearance time of B.longispina individuals in water column
at the coastal and open areas of the Gulf of Riga, 1993-2002.
The amount of Bosmina longispina resting eggs in the upper sediment layer
stayed at summertime level also in December when the water mixing had
have happened and the sediment material transport together with the resting
eggs occurred. Assumption that in December resting eggs hadn't settled yet
and were still in the water column could hardly be true- the egg sinking rate
of B.longispina in the Gulf was calculated to be almost 19 m day -1. The
depth of sampling station was 44 m, so the sinking requires 2.31 day or 56
h. If the last individuals of Bosmina in the water column were noted at the
end of August, then the deposition of eggs was over at the beginning of
September. Females of B. longispina with the resting eggs in egg sacks are
better visible for potential predators and according the theory of sizes for
cladoceran food (Bernardi et al., 1987), these females are appropriate food
object for predatory Cercopagis pengoi.The decrease of Bosmina abundance
due to gradual growth of C.pengoi amount has been observed in the northern
part of the Gulf- Parnu Bay (Ojaveer et al., 2004). In 2001 C.pengoi was
present at all stations in the coastal and open areas, however its abundance
was 2 times lower than in Parnu Bay - approx. 180 ind. m-3 and more than
400 ind. m-3 , respectively. Still, if the maximal numbers of B. longispina
were so similar both in the open part and Parnu Bay - about 30 000 ind. m-3 ,
then C. pengoi has had an important role in the regulating of Bosmina
abundance. If, according the scale of cladoceran food objects, C.pengoi can
consume not only the adults but also the juveniles of Bosmina, then
population density decreases drastically and very rapidly (de Bernardi et al.,
1987) and the reduction of abundance for more than 400 times in two weeks
of 2001 at the open part of the Gulf is explained. The predation pressure as
the main controlling factor at this time is confirmed also by the steady
environmental situation in these two weeks and continuation of population
development - the number of parthenogenetic eggs in the eggs sacks of
females (4-6) was the maximal one for summer. In the next year of 2002 the
abundance of B. longispina at the open part was somewhat lower, but at the
coastal areas - in average higher than in 2001, reaching 15 000 ind. m-3 and
80 000 ind. m-3 , respectively. Thus, inspite of massive predation population
still had enough resources = resting eggs for successful development in the
next summer. Obviously the coastal erosion zones have the same importance
for accumulation of resting eggs as the deeper accumulation zones. The
station of the accumulation zone in the Gulf is similar to the location in the
northern Baltic Sea with a depth more than 40 m, stratification, almost
constant water temperature in the deep layer and poor water transparency
(Katajisto et al., 1998) where the estimated number of copepod resting eggs
has no relation to copepod abundance in the pelagic zone. The early
appearance of B.longispina in the water layer at winter time could be due to
water movement and resulting salinity differences if we assume that flows
could act as trigger for resting egg development. Inflow of more saline water
masses from the Baltic Sea is common in winter and also in 2001 the salinity
of bottom layer shortly increased for 0,28 PSU (Fig. 15).
Fig. 15. Variation of B.longispina abundance (eks.m-3 ) and salinity (PSU)
at the open part station of the Gulf of Riga, January-April, 2001.
If the environmental conditions are stable, then most probably the hatching
of the resting eggs in the deep part of the Gulf starts after a certain latent
period when a yolk sack is utilized (Egloff et al., 1997). As the appearance
time of cladocerans in the water layer is so close at both parts of the Gulf,
and then obviously the end of utilization period coincides with the increase
of water temperature at the coastal area. The further development of
population of the open part depends on surrounding situation (Egloff et al.,
1997). If the hatching has occurred at optimal conditions, then individuals of
accumulation zone" serve as the addition to the „erosion zone" cladocerans
spreading with the currents from the coastal areas.
Conclusions
1. The changes in nutrient concentrations occurring after 1970 in the Gulf of
Riga affected the summer zooplankton community most considerably - the
increase of food supply caused the growth of the total zooplankton biomass
and the variation in the species structure. The share of herbivorous species
Eurytemora affinis, Bosmina longispina enlarged and the abundance of
oligotrophic copepod Limnocalanus macrurus decreased drastically.
2. The dominance of B.longispina during summers of 1988-1990 together
with the ability to accumulate nitrogen was one of the factors influencing
the change of nutrient concentration ratios after 1991 and the consequent
drop of food quality for zooplankton. As nitrogen deficiency favoured the
development of cyanobacteria, the biomass of zooplankton summer
community decreased. The rapid drop of L. macrurus abundance was
determined by combination of unfavourable environmental situation and
intensive fish predation.
3. The biomass growth of spring zooplankton community till 1990 in the
open part of the Gulf of Riga was related to the water temperature
dynamics. Although during 1976 -1996 the salinity decreased for 1 PSU in
the Gulf, it still fell into the range of optimal conditions for most of the
species and thus did not cause the diminishing of zooplankton amount.
4. Although at the Eastern Gotland basin of the Baltic Proper nutrient
concentration ratios and phytoplankton species structure changed in 19761994, the variations of zooplankton community were not related to
alterations of food supply. In spring the dynamics of zooplankton numbers
were determined by water temperature, in autumn the observed negative
trend - by gradually decreasing salinity, mostly affecting the abundance of
season's dominant copepod Pseudocalanus elongatus.
5. Neither at the open, nor at the coastal areas of the Gulf of Riga
zooplankton community was directly and obviously affected by larger North Atlantic - scale changes in atmospheric situation. The only
relationship detected is the positive link between cladoceran abundance in
summer at the open part and North Atlantic Oscillation (NAO) winter index
in 1980 - 1998. The lack of relationship with other zooplankton groups is
explained by wider optimal temperature range (Copepoda) or better
adaption capabilities (Rotatoria).
6. The link of local hydrometorological conditions and North Atlantic
climatic variations is most clearly expressed as severe winters with ice
cover in the Gulf. Thus the presence or absence of ice is the factor
determining the start of the thermophylic zooplankton species. The spatial
and temporal distribution of coastal zone community is influenced also by
dynamics of water masses - the wind-caused upwellings changing the
species composition and numerical values as well as modifying the feeding
conditions.
7. In 1982-1996 at the coastal areas of the Gulf of Riga 27 taxons were
identified, including also the invasive species - polychaete Marenzelleria
viridis (larval stage, since 1989) and cladoceran Cercopagis pengoi (since
1992). Zooplankton abundance at the coastal part was always higher in
summer and autumn that at the open area of the Gulf, also any negative
species or group abundance trends were not determined, thus indicating that
no chronic unfavourable environmental situation had been present at the
potentially more polluted coastal zone. Copepods and rotifers were the
dominant groups at both parts of the Gulf in spring and autumn. The
summer
ratios of copepods, cladocerans and rotifers differed as the share of
copepods was lower ar the coastal zone due to various life cycle strategies
of the species.
8. Analysis of the coastal zone dominant species - Bosmina longispina,
Synchaeta baltica and Keratella quadrata dynamics in 1982-1997 showed
that opposite to the open part no general decrease of zooplankton abundance
has been observed after 1990. The only negative trend was detected for S.
baltica at autumn explained by changes of food quality - a lack of large
autumn diatoms in phytoplankton of 1990s.
9. Regarding the link with environmental factors, in 1982-1997 a
statistically significant relationship was detected only for the abundance of
Bosmina longispina and the coastal zone salinity which was positive and the
salinity deviations have determined the abundance fluctuations. At the
coastal areas of the Gulf a negative salinity deviation means the prevention
of water mixing or increased nutrient inflow with following higher
sedimentation which disturbs the development of B.longispina resting eggs.
10. The coastal erosion zones of the Gulf have the same importance for the
accumulation of cladoceran Bosmina longispina resting eggs and thus also
for development of population as the deeper sediment accumulation zones.
Development of B.longispina from the resting eggs at the open part in
unfavourable environmental conditions could be caused by water movement
- the inflow of more saline water masses from the Baltic Sea in the bottom
layer. In summer when the situation is favourable for the development of
thermophylic cladocerans, the abundance of B. longispina could be
considerably influenced by invasive predatory cladoceran Cercopagis
pengoi feeding both by adult and juvenile individuals of Bosmina.
List of publications
I. Ikauniece A., Ceitiina M. 1998. Zooplankton community in the zones of
ecological risk in the Gulf of Riga (Baltic Sea). Proc. Latv.Acad.Sci., 52
(Suppl.), 62-68.
II. Yurkovskis A., Kostrichkina E., Ikauniece A. 1999. Seasonal succession
and growth in the plankton communities of the Gulf of Riga in relation to
long-term nutrient dynamics. Hydrobiologia. 393: 83-94.
III.Ikauniece A. 2001. Regulation of zooplankton species abundance: the
results of marine monitoring in the coastal zone. Environment International
26, 175-181.
IV.Anda Ikauniece, E.Kostrichkina, B.Kalveka and M.Mazmacs. 2003.
Factors structuring the plankton communities in the Eastern Gotland Basin
and the Gulf of Riga, Baltic Sea. ICES CM. 2003/P14