Download Biotic and abiotic preferences of the cladoceran invader

Hydrobiologia 442: 89–99, 2001.
M. Boersma & K.H. Wiltshire (eds), Cladocera.
© 2001 Kluwer Academic Publishers. Printed in the Netherlands.
89
Biotic and abiotic preferences of the cladoceran invader
Limnosida frontosa
Thomas C. Jensen1 , Dag O. Hessen1 & Bjørn A. Faafeng2
1 Department
2 Norwegian
of Biology, University of Oslo, P.O. Box 1027, Blindern, N-0316 Oslo, Norway
Institute for Water Research. P.O. Box 173, Kjelsås, N-0411 Oslo, Norway
Key words: Limnosida frontosa, abiotic parameters, food spectrum, particle selection
Abstract
During the late 1980s and early 1990s, the cladoceran Limnosida frontosa invaded several lakes within its natural
range in southeastern Norway. In this project, we wanted to study the types of lakes preferred by Limnosida. We
also wanted to evaluate the potential competitive effects on other zooplankton species. In a survey of 65 Norwegian
lakes, Limnosida showed preference for lakes of low Ca concentrations and low productivity. This is probably due
to decreased competition from species with higher Ca requirements and a lower fish predation on zooplankton in
these lakes compared to more productive lakes. Particle size preferences of Limnosida were studied and compared
with those of the microfiltrator Daphnia magna, as there was no published information on the food preference of
Limnosida. When fed monodisperse fluorescent latex beads (0.5, 1.0, 6.0 µm), Limnosida strongly selected the
largest beads, while D. magna had a more nonselective feeding behaviour. Mesh sizes of Limnosida’s filtering
appendages were 0.4–1.2 µm depending on the animal size, and the particle selection was correlated with the
filter mesh sizes. Limnosida should thus be considered a low efficiency grazer on bacteria and µ-algae. Hence,
this species probably does not interfere significantly with microfiltrators like Diaphanosoma brachyurum and most
daphnids. This was supported by community analysis of lakes with and without Limnosida. In general, Limnosida
commonly co-occurred with a number of filter-feeding cladocerans, and we found no sign of competitive exclusion
in lakes where the species has become established.
Introduction
During the late 1980s and early 1990s, the cladoceran Limnosida frontosa Sars invaded several lakes
in southeastern Norway. (Walseng & Karlsen, 1997;
Faafeng, unpubl. data). Invasion of species has attracted much attention, because ecosystem properties,
such as productivity and community structure may
be influenced by invading species (Mooney & Drake,
1989). Zooplankton invaders may also affect the native
zooplankton communities. For example, after invading Lake Naivasha, Kenya, Daphnia pulex outcompeted other zooplankton species (Harper, 1984), and
the invasion of Bythotrephes cederstroemii in lakes in
the northeastern U.S.A., strongly affected the native
invertebrate predator Leptodora kindti as well as the
herbivorous zooplankton (Lehman & Cáceres, 1993;
Yan & Pawson, 1997).
A species’ distribution depends on interactions
between a number of biotic and abiotic factors, which
together form the multidimensional niche of the species. Though invasion may lead to extinction of native
species through competitive exclusion (Hardin, 1960),
competing zooplankton species may also coexist (Jacobs, 1977; Chow-Fraser & Maly, 1992).
Differing abiotic demands among zooplankton
species promote coexistence (Havens et al., 1993;
Hessen et al., 1995a). Temporal or spatial niche differentiation will also allow competitors to coexist
(Leibold, 1991; Angeli et al., 1995). Furthermore, biotic factors such as size selective predation (Brooks
& Dodson, 1965; Zaret, 1980), age structure (Lynch,
1978) and intraspecific competition (Hu & Tessier,
1995) have been used to explain coexistence between
zooplankton species. Food is also an important factor
as far as the competitive outcome between species is
90
concerned, as different species utilize different kinds
of food (Neill, 1975; Chow-Fraser & Maly, 1992) or
food size spectra (Burns, 1968; Geller & Müller, 1981;
Hessen, 1985). This kind of niche differentiation will
promote coexistence.
Limnosida was originally described by Sars (1993
[1861]). The species is planktonic (Lilljeborg, 1982
[1901]; Sars, 1993 [1861]) found from May to October, though it is mainly present in mid summer (Lilljeborg, 1982 [1901]; Vekhov, 1987). Pejler (1965) found
the species in lakes with relatively low productivity.
Limnosida is a palearctic species (Sars, 1865, 1993
[1861]; Behning, 1912; Lilljeborg , 1982 [1901];
Vekhov, 1987).
The objectives of this study was to examine
whether the distribution of Limnosida could be related
to abiotic and biotic factors such as calcium concentrations, lake productivity parameters and fish predation
on zooplankton. Co-occurrence of Limnosida with
other cladocerans was also investigated. Since there is
no information on the food preferences of Limnosida
in the literature, an assay of particle size preferences
was undertaken in order to obtain some basic information on food size selection and filtering rates
to evaluate the potential competitive effects on other
zooplankton species.
Materials and methods
A survey of nutrient levels and plankton communities
in a large number of Norwegian lakes has been conducted since 1988 (Faafeng & Hessen, 1993). For the
present study, only lakes within the distribution area of
Limnosida were chosen. This included a set of 65 lakes
in southeastern Norway, geographically delimited to
the north and east within the area where Limnosida
occurred. Only lakes with pH>5 were included in order to avoid lakes with severe acidification. Samples
for total phosphorus (total P), total nitrogen (total N)
and chlorophyll a from July and August from 1988
to 1993 were included in this study. Samples for the
analysis of calcium (Ca) were taken from August or
September from 1988 to 1993. Further description of
the sampling and analysis is given in Hessen et al.
(1995a, b).
The relationship between distribution of Limnosida and Ca concentration and tentative lake productivity (total P) was assessed by logistic regression.
This relates presence/absence of a species to continuous or discrete independent variables (Jongman et
al., 1995). Univariate logistic regression describes the
probability (p) of an event (presence/absence) by a
probability ratio as a linear function of the independent
variable (x):
p
= b 0 + b1 · x
log10
1−p
This expression describes a situation where an organism has an optimum for either high or low values of
the independent variable.
Logistic regression can also be used to assess
species preferences along the gradient axis of the independent variable (Jongman et al., 1995). Furthermore,
the univariate model can be extended to describe the
probability as a function of two independent variables
(Jongman et al., 1995). This has been done in previous
zooplankton studies (Hessen et al., 1995a). Here, the
above expression is extended to a quadratic polynomial. The bivariate model then becomes an expression
of the form:
p
b 0 + b1 · x1 + b2 · x1 2
log10
1−p
+b3 · x2 + b4 · x2 2 + b5 · x1 · x2
where x1 and x2 are independent variables.
In the bivariate regression in this study, the interaction between Ca and total P is considered. The
criterion for accepting an effect in the logistic models
was p < 0.05. JMP 3.2.2 (SAS Institute Inc. Cary,
NC) was used for statistical calculations.
The presence/absence data for Limnosida was
mainly based on this lake survey. In a few lakes,
the species was not registered in our lake survey,
but it presence has nevertheless been verified in later
studies. For the statistical treatment, the species was
considered as present in these lakes as well.
The co-occurrence between Limnosida and other
cladocerans was assessed from observations on presence/absence of the species in the survey for the same
lakes during the years 1988–1993. In order to examine
whether Limnosida was associated with some of the
other species the coefficient of association, Yule’s Q,
was calculated (Freeman, 1987). Q varies from −1 to
1. A value of 0 indicates no association, values >0
indicate positive association, and values <0 indicate
negative association.
The fish species composition of the lakes was categorised on basis of questionnaires and reports. Six
fish community categories were identified, ranging
from category 1 dominated by brown trout (Salmo
trutta) to category 6 dominated by various cyprinids,
also representing a supposed increase in fish predation
91
on zooplankton (Hessen et al., 1995b). The occurrence
of Limnosida as related to fish community was then
assessed, based on these categories.
The particle size selection of Limnosida was assessed both by feeding experiments and examination of the filtering appendages. In order to study
particle size preferences of the species, feeding trials
with fluorescent latex beads were performed (Hessen,
1985). The particle size preferences of Limnosida
were compared with those of the well known microfiltrator Daphnia magna (Geller & Müller, 1981;
Brendelberger & Geller, 1985). Limnosida for the experiments was collected from Lake Gjersjøen and D.
magna originated from a culture at the Department
of Biology, University of Oslo. The animals from the
lake were collected by vertical net hauls (95 µm) from
the epilimnion at different dates during the summer of
1997. They were transferred to the laboratory in lake
water, where they were allowed to acclimatize for 24
h (19 ◦ C) in 12 l aquaria and fed on a suspension of
the green algae Selenastrum capricornutum.
Limnosida and D. magna were exposed to fluorescent latex beads (Fluoresbrites, Polysciences) of 0.5
µm, 1.0 µm and 6.0 µm at concentrations of approx.
2.24·106– 3.07·106, 7.56·105 – 1.43·106, 2.88·104 –
6.50·104 beads ml−1 in separate 100 ml beakers. The
food concentration (S. capricornutum) in these experiments was approx. 0.08 mg C l−1 . The number of
animals in the beakers varied from 10 to 21, and all
grazing experiments lasted for 10 min. The animals
were then killed with hot water (60 ◦ C), filtered on 90
µm gauze, washed and sorted according to size under
a dissecting binocular. Depending on size, from 3 to 13
animals of each size group were placed in vials with
distilled water and sonicated for five minutes (MSE
Soniprep 150), which caused a breakdown of the animal tissue. The suspension of particles was filtered on
black 0.2 µm polycarbonate filters and counted with a
fluorescence microscope (Leitz Laborlux S).
A second series of experiments was performed to
compare the feeding rate and selection of latex beads
of Limnosida to that of more natural food. 14 C-labelled
S. capricornutum (cell size of approx. 3 × 7 µm) was
added to the beakers (approx. 0.8 mg C l−1 ), together
with the latex beads (0.5 µm, 1.0 µm and 6.0 µm).
In this experiment, 200 ml beakers were used and the
number of animals was doubled.
About 10% of the animals in both experiments did
not ingest the beads. These were probably dead or unhealthy specimens. As for many cladocerans, the gut
passage time (GPT) for different types of natural food
Table 1. Major characteristics for the 65 lakes. Data on total P, total
N and chlorophyll a are from July and August samples from 1988
to 1993. Data on calcium are from August and September samples.
Area as km2 ; total P, total N and chlorophyll a as µg l−1 ; Ca as mg
l−1
Area
Total P
Total N
Chlorophyll a
Ca
Average
Median
Max.
Min.
12.6
29
669
16.2
7.8
32.1
15
510
7.5
4.3
362.8
301
3061
121.7
37.3
0.2
3
237
1.2
1.7
is more than 15 min (Peters, 1984), we assumed that
the incubation time of 10 min was shorter than GPT.
The selectivity index, Is (−1 to 1), of each bead
size was calculated according to Ivlev (1961). Is varies
from −1 to 1. Values >0 denotes a positive selection,
and values <0 a negative selection.
Formalin-preserved Limnosida from Lake Gjersjøen were sorted according to size, critical-point
dried, mounted on aluminium stubs, covered with
gold-palladium (Polaron SEM coating unit) and examined by scanning electron microscopy (SEM) (Jeol
JSM-6400 scanning microscope). The intersetulae distances (ISD) were measured on the 5 first thoracic
appendages on several individuals from each size
group.
Results
The occurrence of Limnosida in Norway is restricted
to the southeastern part of the country (Fig. 1). It
has been recorded in 45 lakes, and 40 of these were
included in our survey. The 65 lakes in our survey represented a range from oligotrophy to eutrophy, with
a total P concentration from 3 to 301 µg l−1 , but
with the majority of lakes being oligotrophic (Table
1). The Ca concentration ranged from 1.7 to 37.3 mg
l−1 (Table 1). Both Ca and total P were skewed towards lower values, and became more symmetric after
log transformation. Total P was correlated with chlorophyll a (log (TP) vs log(Chl. a): r = 0.93, p < 0.0001),
justifying the use of total P as the single productivity
variable. Total P was also correlated with Ca (log(TP)
vs log(Ca): r = 0.54, p < 0.0001).
Univariate logistic regression testing the occurrence of Limnosida along gradients of Ca and total P
(Fig. 2) showed a decreased probability of Limnosida
92
Figure 1. Distribution of L. frontosa in Southern Norway (filled dots) related to all lakes surveyed (open dots). Data is mainly based on the
national eutrophication survey (cf. Faafeng & Hessen, 1993; Hessen et al., 1995b), with supplementary information from various sources
(Borgstrøm et al., 1974; Walseng & Karlsen, 1997; Wærvågen, 1998; Kjellberg unpubl. data; Walseng unpubl. data).
occurrence with increasing concentrations of Ca and
total P (Ca: p = 0.0003, total P: p = 0.039). Bivariate
logistic regression for the occurrence of Limnosida in
relation to Ca and total P gave significant effect of Ca
only (p = 0.0003). This indicates that Ca was more
important than total P for the occurrence of Limnosida.
The biotic preferences of Limnosida were related
to fish and zooplankton communities as well as to the
preferred food size spectra. The fish communities in
most of the 65 lakes from the survey were dominated
by cyprinids and had thus an assumed high fish predation on zooplankton. Limnosida almost exclusively
occurred in lakes belonging to category 6, suggesting
a relatively high resistance towards fish predation.
Limnosida commonly co-occurred with a number
of abundant cladocerans (Fig. 3). Most frequent cooccurrence was recorded with Daphnia cristata, Diaphanosoma brachyurum, Bosmina longispina, Bosmina coregoni and Bosmina longirostris. Yule’s Q
was positive for Limnosida and each of the species
D. cristata, Holopedium gibberum and B. coregoni
(Table 2). The occurrence of Limnosida was thus positively associated with these three species, of which at
least the two latter are species preferring rather large
particles.
93
Figure 2. (a) Logistic regression of L. frontosa’s occurrence in relation to Ca. Based on data from 65 lakes. Line: probability of occurrence
as predicted by the model. Dots: ranked concentrations of Ca in lakes with L. frontosa (below line) and without L. frontosa (above line). (b)
Logistic regression of L. frontosa’s occurrence in relation to total P. Based on data from 65 lakes. Line: probability of occurrence as predicted
by the model. Dots: ranked concentrations of total P in lakes with L. frontosa (below line) and without L. frontosa (above line).
Figure 3. Distribution of the 65 lakes from the lake survey divided into 4 groups according to presence or absence of L. frontosa and the other
cladocerans. The 4 groups are: L. frontosa present and the species Y present (L. fro. +/Spec. Y +), L. frontosa absent and the species Y present
(L. fro. -/Spec. Y +), L. frontosa present and the species Y absent (L. fro. +/Spec. Y -), L. frontosa absent and the species Y absent (L. fro.
-/Spec. Y -). Abbreviations are: L. fro., Limnosida frontosa; D. cri., Daphnia cristata; B. log., Bosmina longispina; D. bra., Diaphanosoma
brachyurum; B. cor., Bosmina coregoni; B. lon., Bosmina longirostris; D. cuc., Daphnia cucullata; C. spp., Ceriodaphnia spp.; H. gib.,
Holopedium gibberum; Chy., Chydorids; D. hya., Daphnia hyalina; D. gal., Daphnia galeata; D. lon., Daphnia longispina; D. log., Daphnia
longiremis.
94
Table 2. The coefficient of association, Yule’s Q (with 95% confidence interval), for L. frontosa and each of the other species in
the lake survey. Significant values (p<0.05) in bold. Q varies
from −1 to 1. A value of 0 indicates no association, values > 0
positive association, and values < 0 negative association. Abbreviations as in Figure 3. D. longiremis and D. longispina occurred
in less than 5 of the 65 lakes, so Yule’s Q was not calculated for
these and L. frontosa
Species combination
L. fro. and D. cri.
L. fro. and H. gib.
L. fro. and B. cor.
L. fro. and B. log.
L. fro. and Chy.
L. fro. and D. bra.
L. fro. and C. spp.
L. fro. and B. lon.
L. fro. and D. cuc.
L. fro. and D. gal.
L. fro. and D. hya.
Yule’s Q
0.57±0.39
0.48±0.33
0.43±0.29
0.19±0.43
0.14±0.57
0.05±0.51
−0.14±0.60
−0.19±0.61
−0.19±0.61
−0.26±0.94
−0.48±1.02
effective consumer of bacteria and the smallest algal
species.
Clearance rates calculated from the ingested latex
beads also varied with bead size and animal size (Fig.
5). Both Limnosida and Daphnia showed increased
clearance rates with increasing particle size. There
was also a tendency for increased clearance rates with
increasing animal size for both species. Limnosida
had considerably lower clearance rates than D. magna
(Fig. 5a,c). The combined experiments with beads and
14 C-labelled algae gave similar clearance rates for the
two largest sizes of beads and algae (Fig. 5b), indicating that the feeding response of Limnosida to beads
and to natural food were comparable.
An increase in Limnosida clearance rates was observed during the summer. The animals collected at
the different dates have different histories with respect
to parameters, such as food conditions and temperature. There might be an inherent seasonal effect on
the clearance rates even though the animals in all the
experiments were temperature adapted during a 24 h
period prior to the experiments.
All size categories of Limnosida showed a strong
preference for the larger beads. In all the experiments
with Limnosida, we observed a shift from negative to
positive selectivity indices between 0.5 and 1.0 µm
particle size (Fig. 6a, b). Furthermore, the indices
for 6.0 µm beads were larger than for 1.0 µm beads.
There were no marked differences in particle size selection between the different size groups of animals.
D. magna also showed a shift from negative to positive selectivity indices between 0.5 and 1.0 µm particle
size (Fig. 6c), and a preference for the largest beads.
Yet compared with Limnosida, D. magna experienced
a rather nonselective feeding behaviour.
Discussion
Figure 4. Cumulative frequencies of intersetulae distances (ISD) of
the 4 size groups of L. frontosa. Pooled data in each size group for
the 5 first appendages.
The food size preference in Limnosida was inferred from filter mesh sizes and the size spectrum of
ingested particles. The intersetulae distances (ISD) of
Limnosida ranged from 0.4 to 1.2 µm depending on
animal size and site on the filters. ISD increased with
animal size, and variations in ISD were less in the
smallest animals (Fig. 4). Based on these morphological studies, Limnosida would not be considered an
The 65 lakes from the survey covered a limited range
of Ca and lake productivity. However, Limnosida
showed a statistically strong preference for lakes with
low Ca and total P. The interpretation of the logistic
regression is complicated by the correlation of Ca and
total P. Bi- and multi-variate logistic regression takes
this into account (Jongman et al., 1995), and Ca appeared to be a more important parameter than total P
for the occurrence of Limnosida.
Limnosida’s preference for lakes of low productivity with low Ca concentrations corresponds well with
studies on the Ca content of different cladocerans,
95
Figure 5. (a) Clearance rates for different size groups of L. frontosa given 3 sizes of beads. Concentration of Selenastrum capricornutum during
the experiments was approx. 0.08 mg C l−1 . Means and standard deviations refer to the number of experiments in which the different size groups
are represented. (b) Clearance rates for different size groups of L. frontosa given 3 sizes of beads and 14 C-labeled algae. Concentration of S.
capricornutum during the experiments was approx. 0.8 mg C l−1 . Means and standard deviations as in (a). (c) Clearance rates for different size
groups of D. magna given 3 sizes of beads . Concentration of S. capricornutum during the experiments was approx. 0.08 mg C l−1 . Means and
standard deviations as in (a).
96
Figure 6. Particle size selection of L. frontosa and D. magna, expressed as the selectivity index Is . (a) Experiments where L. frontosa was
given beads (food concentrations: 0.08 mg C l−1 ). Means and standard deviations refers to all experiments at this food concentration. (b)
Experiments where L. frontosa was given beads and 14 C-labeled algae (food concentrations: 0.8 mg C l−1 ). Means and standard deviations
refers to all experiments at this food concentration. (c) Experiments where D. magna was given beads (food concentrations: 0.08 mg C l−1 ).
Means and standard deviations refer to all experiments at this food concentration.
which indicates that Limnosida has low Ca requirements compared to other species (Wærvågen et al.,
unpubl. data). The observed preference of Limnosida
for lakes with low Ca concentrations could be an indirect effect of decreased competitive abilities from
species with higher Ca demands, such as certain daphnids, at low Ca levels (Hessen et al., 1995a; Wærvågen
et al., unpubl. data).
Considering the biotic properties of the lakes, Limnosida apparently preferred lakes dominated by different cyprinids. Migration barriers restrict the occurrence of these fish to southeastern Norway (HuitfeldtKaas, 1924). Consequently, the distribution of lakes
in category 6 coincide with that of Limnosida. These
lakes had a relatively high supposed fish predation
pressure on zooplankton. However, Limnosida also
preferred lakes of low productivity. Lakes of increasing productivity will have an increasing biomass
of planktivorous fish (Johansson & Persson, 1986;
Jeppesen, 1998). As a consequence, these lakes could
also have an increasing predation pressure on zooplankton. Limnosida thus seems to be fairly resistant
to predation from fish and are surely able to coexist
with cyprinids. Nevertheless, the predation pressure
from fish in the most productive lakes might be too
high to allow for persistence of Limnosida in these
lakes.
The spreading of Limnosida do apparently not
cause strong effects on the zooplankton communities. The differences in co-occurrence and association
between Limnosida and other cladocerans in the lake
survey (Fig. 3) is probably partly caused by the
97
geographic distribution of species and partly by the
differences between species in demands to abiotic
parameters, resistance to predation and general competitive abilities. The occurrence of Limnosida was
positively associated with H. gibberum, which has a
more restricted occurrence. Like Limnosida, H. gibberum is mainly found in lakes of low productivity
and Ca levels (Pejler, 1965; Hessen et al., 1995a). H.
gibberum is probably also a superior competitor at low
Ca, because of its low Ca requirements (Wærvågen
et al., unpubl. data). This could explain this species’
positive association with Limnosida. The associated
occurrence of the two common species D. cristata and
B. coregoni with that of Limnosida could be partly explained by the vulnerability of these species to fish.
Like Limnosida, D. cristata and B. coregoni are fairly
resistant to predation (Hessen et al., 1995b), and
they would therefore be less preyed upon in the lakes
dominated by cyprinids.
In the feeding experiments, Limnosida had by far
lower clearance rates for all sizes of beads than D.
magna, which is known to have rather high sizespecific clearance rates (McMahon & Rigler, 1965;
Kersting & Van Der Leeuw, 1976). Though clearance
rates determined with artificial particles in laboratory
experiments does not mimic natural conditions, it still
indicates that Limnosida has lower clearance rates than
D. magna.
Larger individuals of Limnosida had high clearance rates compared with other cladocerans (Burns
& Rigler, 1967; Ganf & Shiel, 1985). Filter area
(Kořínek & Macháček, 1980; Ganf & Shiel, 1985) and
mesh size (Kořínek and Macháček, 1980; Geller &
Müller, 1981; Brendelberger & Geller, 1985) both increase with body size. According to Crittenden (1981),
the discharge rate increases disproportionately with
mesh size. Furthermore, the thoracic beat rate (Watts
& Young, 1980) depends on animal size. All this may
contribute to increased clearance rates with animal
size.
The differences in mesh size between size groups
of Limnosida were too small to cause a difference in
particle size selection between size groups. However,
larger individuals of Limnosida will probably have a
broader food size range than smaller ones, since larger individuals will be able to ingest larger particles
(Burns, 1968).
Particle size selection of Limnosida seemed to correlate well with filter mesh size, and this study thus
gives support to the sieving model, where mechanical
filtering is supposed to be the most important mechan-
ism in the particle capture of many cladocerans (Geller
& Müller, 1981).
Limnosida has previously been found in lakes of
relatively low productivity (Pejler, 1965). The present
study supports this observation. Decreased competition from cladocerans with higher Ca demands as well
as moderate fish predation may be important factors.
The food preferences of the species could add to this.
It has been suggested that high efficiency bacteria
feeders could have a competitive advantage in more
productive lakes (Geller & Müller, 1981). Species
capable of utilising small particles will be favoured,
when the distribution of food particles changes from
being dominated by medium sized algae in relative oligotrophic lakes to microalgae and bacteria combined
with large inedible algae in eutrophic lakes (Hessen et
al., 1986). Low efficiency bacteria feeders, like Limnosida, could thus be better adapted to the food regime
in less productive lakes.
We found no sign of competitive exclusion by Limnosida. In general, zooplankton communities did not
differ between lakes with or without Limnosida. In
Lake Gjersjøen Limnosida have coexisted with the
native zooplankton since it invaded the lake in 1985,
although it may occur in fairly high biomasses in
some samples (Faafeng, unpubl. data). In 1997, Limnosida also showed a pronounced seasonal and/or
spatial niche overlap with D. brachyurum, D. cristata,
B. longispina and B. longirostris in this lake (Jensen,
1999). One mechanism that could reduce resource
competition and thus promote coexistence between
Limnosida and other species is niche differentiation
with respect to food size spectra. Since Limnosida
was found to be a low efficiency bacteria feeder, the
invasion of the species may not interfere significantly
with high efficiency bacteria feeders like D. brachyurum and many daphnids (Geller & Müller, 1981;
Hessen, 1985). The effect on other zooplankton species with high Ca requirements might be most adverse
in lakes with low Ca where these species have reduced
competitive abilities due to the suboptimum calcium
concentrations. It seems that the invasion of Limnosida
does not pose a serious threat to native zooplankton
species.
Invasions of so-called ‘exotic species’, not naturally occurring in that geographical area, have often
had major consequences for the system they invaded
(Baskin, 1992; Yan & Pawson, 1997). In the cases
cited above, species have come together recently, and
so the evolutionary forces have had a short time to
bring balance to species interactions. When Limnosida
98
appears in new lakes, it is often found together with
species naturally occurring within the same geographical range. In this case, species interactions are old,
and the evolutionary forces might have brought balance to the interactions between the species. The
prehistory of the species interactions may explain why
Limnosida does not seem to affect native cladocerans
upon invasion, though this remains speculative.
In conclusion, Limnosida preferred lakes with low
Ca and low total P. Invading new lakes it will most
likely be found in soft water lakes of low productivity. This is probably due to reduced competition from
species with higher Ca requirements and a lower fish
predation on zooplankton in these lakes compared
to more productive lakes. Furthermore, Limnosida
was found to be a low efficiency bacteria feeder, so
the invasion of the species may not interfere significantly with microfiltrators like D. brachyurum and
many daphnids. This was supported by community
analysis. Limnosida commonly co-occurred with other
filter-feeding cladocerans.
Acknowledgements
We would like to thank Gösta Kjellberg and Bjørn
Walseng for providing unpublished data on zooplankton from previous investigations. Tom Andersen and
Ørnulf Borgan provided valuable suggestions on the
statistical methods. Torulv Tjomsland is acknowledged for help on graphic representation. The english
has been improved by Ingunn Myhre.
References
Angeli, N., B. Pinel-Alloul, G. Balvay & I. Ménard, 1995. Diel
patterns of feeding and vertical migration in daphnids and diaptomids during the clear water phase in Lake Geneva (France).
Hydrobiologia 300/301: 163–184.
Baskin, Y., 1992. Africa’s troubled waters. Bioscience 42: 476–481.
Behning, A., 1912. Limnosida frontosa G. O. Sars in der südlichen
Wolga. Arch. Hydrobiol. 8: 446–450.
Borgstrøm, R., J. A. Eie, G. Hardeng, R. Nordbakke, J. E. Raastad
& J. O. Solem, 1974. Inventeringer av verneverdige områder i
Østfold. Boksjøområdet, Berbydalen/Indre Iddefjord og Mingevatn/Vestvatn (in Norwegian). Laboratorium for ferskvannsøkologi og innlandsfiske, Report no. 17. 71 pp.
Brendelberger, H. & W. Geller, 1985. Variability of filter structures in eight Daphnia species: mesh sizes and filtering areas.
J. Plankton Res. 7: 473–486.
Brooks, J. L. & S. I. Dodson, 1965. Predation, body size, and
composition of plankton. Science 150: 28–35.
Burns, C. W., 1968. The relationship between body size of filterfeeding Cladocera and the maximum size of particle ingested.
Limnol. Oceanogr. 13: 675–678.
Burns, C. W. & F. H. Rigler, 1967. Comparison of filtering rates of
Daphnia rosea in lake water and in suspensions of yeast. Limnol.
Oceanogr. 12: 492–502.
Chow-Fraser, P. & E. J. Maly, 1992. Size divergence and dietary partitioning enhance coexistence of two herbivorous species
of Diaptomus (Copepoda: Calanoida) in some shallow Quebec
lakes. Can. J. Zool. 70: 1016–1028.
Crittenden, R. N., 1981. Morphological characteristics and dimensions of the filter structures from three species of Daphnia
(Cladocera). Crustaceana 41: 233–248.
Faafeng, B. A. & D. O. Hessen, 1993. Nitrogen and phosphorus
concentrations and N:P ratios in Norwegian lakes: perspectives
on nutrient limitation. Verh. int. Ver. Limnol. 25: 465–469.
Freeman, D. H., 1987. Applied categorical data analysis. Marcel
Dekker, Inc., New York: 318 pp.
Ganf, G. G. & R. J. Shiel, 1985. Feeding behaviour and limb morphology of two cladocerans with small intersetular distances.
Aust. J. mar. Freshwat. Res. 36: 69–86.
Geller, W. & H. Müller, 1981. The filtration apparatus of Cladocera: Filter mesh-sizes and their implications on food selectivity.
Oecologia 49: 316–321.
Hardin, G., 1960. The competitive exclusion principle. Science 131:
1292–1297.
Harper, D., 1984. Recent changes in the ecology of Lake Naivasha,
Kenya. Verh. int. Ver. Limnol. Verh. 22: 1193–1197.
Havens, K. E., N. D. Yan & W. Keller, 1993. Lake acidification: Effects on crustacean zooplankton populations. Envir. Sci. Technol.
27: 1621–1624.
Hessen, D. O., 1985. Filtering structures and particle size selection
in coexisting Cladocera. Oecologia 66: 368–372.
Hessen, D. O., B. A. Faafeng & T. Andersen, 1995a. Competition or
niche segregation between Holopedium and Daphnia: empirical
light on abiotic key parameters. Hydrobiologia 307: 253–261.
Hessen, D. O., B. A. Faafeng & T. Andersen, 1995b. Replacement
of herbivore zooplankton species along gradients of ecosystem
productivity and fish predation pressure. Can. J. Fish. aquat. Sci.
52: 733–742.
Hessen, D. O., J. P. Nilssen & T. O. Eriksen, 1986. Food size spectra and species replacement within herbivorous zooplankton. Int.
Rev. ges. Hydrobiol. 71: 1–10.
Hu, S. S. & A. J. Tessier, 1995. Seasonal succession and the strength
of intra- and interspecific competition in a Daphnia assemblage.
Ecology 76: 2278–2294.
Huitfeldt-Kaas, H., 1924. Einwanderung und Verbreitung der
Süsserwasserfische in Norwegen. Arch. Hydrobiol. 14: 223–314.
Ivlev, V. S., 1961. Experimental ecology of the feeding of fishes.
Yale University Press, New Haven: 302 pp.
Jacobs, J., 1977. Coexistence of similar zooplankton species by
differential adaptian to reproduction and escape in an environment with fluctuating food and enemy densities. Oecologia 30:
313–329.
Jeppesen, E., 1998. The ecology of shallow lakes – Trophic interactions in the pelagial. Doctor’s dissertation (DSc). National
Environmantal Research Institute, Technical report no. 247.
Jensen, T. C., 1999. Økologi og udbredelse hos cladocéen Limnosida frontosa i Norge (in Danish). Unpublished Cand. scient.
thesis. Department of Biology, University of Oslo.
Johansson, L. & L. Persson, 1986. The fish community of temperate
eutrophic lakes. In Riemann, B. & M. Søndergaard (eds), Carbon Dynamics in Eutrophic, Temperate Lakes. Elsevier Science
Publishers B. V., Amsterdam: 237–266.
Jongman, R. H. G., C. J. F. Ter Braak & O. F. R. Van Tongeren,
1995. Data analysis in community and landscape ecology. Cambridge University Press, Cambridge: 299 pp.
99
Kersting, K. & W. Van Der Leeuw, 1976. The use of the coulter
counter for measuring the feeding rates of Daphnia magna.
Hydrobiologia 49: 233–237.
Kořínek, V. & J. Machacek, 1980. Filtering structures of Cladocera
and their ecological significance 1. Daphnia pulicaria. Vestn.
cesk. spol. Zool. 44: 213–218.
Lehman, J. T. & C. E. Cáceres, 1993. Food-web responses to species invasion by a predatory invertebrate: Bythotrephes in Lake
Michigan. Limnol. Oceanogr. 38: 879–891.
Leibold, M. A., 1991. Trophic interactions and habitat segregation
between competing Daphnia spp. Oecologia 86: 510–520.
Lilljeborg, W., 1982 [1901]. Cladocera Sueciæ. Almqvist & Wiksell
International, Stockholm: 664 pp.
Lynch, M., 1978. Complex interactions between natural coexploiters – Daphnia & Ceriodaphnia. Ecology 59: 552–564.
McMahon, J. W. & F. H. Rigler, 1965. Feeding rate in Daphnia magna Straus in different foods labeled with radioactive
phosphorus. Limnol. Oceanogr. 10: 105–113.
Mooney, H. A. & J. A. Drake, 1989. Biological invasions: a SCOPE
program overview. In Drake., J. A., H. A. Mooney, F. Di Castri,
R. H. Groves, F. J. Kruger, M. Rejmánek & M. Williamson (eds),
Biological Invasions. A Global Perspective. John Wiley & Sons,
New York: 491–506.
Neill, W. E., 1975. Resource partitioning by competing microcrustaceans in stable laboratory microecosystems. Verh. int. Ver.
Limnol. 19: 2885–2890.
Pejler, B., 1965. Regional-ecological studies of Swedish fresh-water
zooplankton. Zool. Bidr. Upps 36: 407–515.
Peters, R. H., 1984. Methods for the study of feeding, filtering, and
assimilation by zooplankton. In Downing, J. A. & F. H. Rigler
(eds), A Manual on Methods for the Assessment of Secondary
Productivity in Freshwaters. Blackwell Scientific Publications,
Oxford: 336–412.
Sars, G. O., 1865. Norges Ferskvandskrebsdyr. Første afsnit. Branchiopoda. I. Cladocera Ctenopoda (Fam. Sididæ & Holopedidæ)
(in Norwegian). Cand. Philosoph. thesis. University of Oslo.
Sars, G. O., 1993 [1861]. On the Freshwater Crustaceans Occurring
in the Vicinity of Christiania. University of Bergen, Bergen: 197
pp.
Vekhov, N. V., 1987. Range, biotop distribution and life cycles of
warm-water cladocerans in subarctic waters of Europe. Hydrobiologia J. 23: 12–16.
Walseng, B. & L. R. Karlsen, 1997. Reetablering av forsuringsfølsomme invertebrater etter kalking av ferskvann i Østfold (in
Norwegian). Norwegian Institute for Nature Research, Oppdragsmeldning 490: 32 pp.
Watts, E. & S. Young, 1980. Components of feeding behaviour. J.
Plankton Res. 2: 203–212.
Wærvågen, S. B., 1998. Biologisk mangfold og utbredelse til
pelagiske planktonorganismer i relasjon til vannkvalitet og
fiskebestandsklasser. Regional undersøkelse av 59 innsjøer i
Hedmark Fylke høsten 1996 (in Norwegian). Høgskolen i Hedmark: 35 pp.
Yan, N. D. & T. W. Pawson, 1997. Changes in the crustacean zooplankton community of Harp Lake, Canada, following invasion
by Bythotrephes cederstroemi. Freshwat. Biol. 37: 409–425
Zaret, T. M., 1980. Predation and Freshwater Communities. Yale
University Press, New Haven: 187 pp.