Biotic and Abiotic Preferences of the Cladoceran Invader Limnosida Frontosa

Biotic and abiotic preferences of the cladoceran invader Limnosida frontosa

Thomas C. Jensen1, Dag O. Hessen1 & Bjørn A. Faafeng2 1Department of Biology, University of Oslo, P.O. Box 1027, Blindern, N-0316 Oslo, Norway 2Norwegian 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 A species’ distribution depends on interactions between a number of biotic and abiotic factors, which During the late 1980s and early 1990s, the clado- together form the multidimensional niche of the spe- ceran Limnosida frontosa Sars invaded several lakes cies. Though invasion may lead to extinction of native in southeastern Norway. (Walseng & Karlsen, 1997; species through competitive exclusion (Hardin, 1960), Faafeng, unpubl. data). Invasion of species has at- competing zooplankton species may also coexist (Jac- tracted much attention, because ecosystem properties, obs, 1977; Chow-Fraser & Maly, 1992). such as productivity and community structure may Differing abiotic demands among zooplankton be influenced by invading species (Mooney & Drake, species promote coexistence (Havens et al., 1993; 1989). Zooplankton invaders may also affect the native Hessen et al., 1995a). Temporal or spatial niche dif- zooplankton communities. For example, after invad- ferentiation will also allow competitors to coexist ing Lake Naivasha, Kenya, Daphnia pulex outcom- (Leibold, 1991; Angeli et al., 1995). Furthermore, bi- peted other zooplankton species (Harper, 1984), and otic factors such as size selective predation (Brooks the invasion of Bythotrephes cederstroemii in lakes in & Dodson, 1965; Zaret, 1980), age structure (Lynch, the northeastern U.S.A., strongly affected the native 1978) and intraspecific competition (Hu & Tessier, invertebrate predator Leptodora kindti as well as the 1995) have been used to explain coexistence between herbivorous zooplankton (Lehman & Cáceres, 1993; zooplankton species. Food is also an important factor Yan & Pawson, 1997). as far as the competitive outcome between species is 90 concerned, as different species utilize different kinds al., 1995). Univariate logistic regression describes the of food (Neill, 1975; Chow-Fraser & Maly, 1992) or probability (p) of an event (presence/absence) by a food size spectra (Burns, 1968; Geller & Müller, 1981; probability ratio as a linear function of the independent Hessen, 1985). This kind of niche differentiation will variable (x): promote coexistence. p log = b + b · x Limnosida was originally described by Sars (1993 10 1 − p 0 1 [1861]). The species is planktonic (Lilljeborg, 1982 This expression describes a situation where an organ- [1901]; Sars, 1993 [1861]) found from May to Octo- ism has an optimum for either high or low values of ber, though it is mainly present in mid summer (Lillje- the independent variable. borg, 1982 [1901]; Vekhov, 1987). Pejler (1965) found Logistic regression can also be used to assess the species in lakes with relatively low productivity. species preferences along the gradient axis of the inde- Limnosida is a palearctic species (Sars, 1865, 1993 pendent variable (Jongman et al., 1995). Furthermore, [1861]; Behning, 1912; Lilljeborg , 1982 [1901]; the univariate model can be extended to describe the Vekhov, 1987). probability as a function of two independent variables The objectives of this study was to examine (Jongman et al., 1995). This has been done in previous whether the distribution of Limnosida could be related zooplankton studies (Hessen et al., 1995a). Here, the to abiotic and biotic factors such as calcium concentra- above expression is extended to a quadratic polyno- tions, lake productivity parameters and fish predation mial. The bivariate model then becomes an expression on zooplankton. Co-occurrence of Limnosida with of the form: other cladocerans was also investigated. Since there is p 2 no information on the food preferences of Limnosida log b0 + b1 · x1 + b2 · x1 10 1 − p in the literature, an assay of particle size preferences + · + · 2 + · · was undertaken in order to obtain some basic in- b3 x2 b4 x2 b5 x1 x2 formation on food size selection and filtering rates where x1 and x2 are independent variables. to evaluate the potential competitive effects on other In the bivariate regression in this study, the in- zooplankton species. teraction 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, Materials and methods NC) was used for statistical calculations. The presence/absence data for Limnosida was A survey of nutrient levels and plankton communities mainly based on this lake survey. In a few lakes, in a large number of Norwegian lakes has been con- the species was not registered in our lake survey, ducted since 1988 (Faafeng & Hessen, 1993). For the but it presence has nevertheless been verified in later present study, only lakes within the distribution area of studies. For the statistical treatment, the species was Limnosida were chosen. This included a set of 65 lakes considered as present in these lakes as well. in southeastern Norway, geographically delimited to The co-occurrence between Limnosida and other the north and east within the area where Limnosida cladocerans was assessed from observations on pres- occurred. Only lakes with pH>5 were included in or- ence/absence of the species in the survey for the same der to avoid lakes with severe acidification. Samples lakes during the years 1988–1993. In order to examine for total phosphorus (total P), total nitrogen (total N) whether Limnosida was associated with some of the and chlorophyll a from July and August from 1988 other species the coefficient of association, Yule’s Q, to 1993 were included in this study. Samples for the was calculated (Freeman, 1987). Q varies from −1to analysis of calcium (Ca) were taken from August or 1. A value of 0 indicates no association, values >0 September from 1988 to 1993. Further description of indicate positive association, and values <0 indicate the sampling and analysis is given in Hessen et al. negative association. (1995a, b). The fish species composition of the lakes was cat- The relationship between distribution of Lim- egorised on basis of questionnaires and reports. Six nosida and Ca concentration and tentative lake pro- fish community categories were identified, ranging ductivity (total P) was assessed by logistic regression. from category 1 dominated by brown trout (Salmo This relates presence/absence of a species to con- trutta) to category 6 dominated by various cyprinids, tinuous or discrete independent variables (Jongman et also representing a supposed increase in fish predation 91 on zooplankton (Hessen et al., 1995b). The occurrence 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 of Limnosida as related to fish community was then to 1993. Data on calcium are from August and September samples. − assessed, based on these categories. Area as km2; total P, total N and chlorophyll a as µgl 1;Caasmg − The particle size selection of Limnosida was as- l 1 sessed both by feeding experiments and examina- Average Median Max. Min. tion of the filtering appendages. In order to study particle size preferences of the species, feeding trials Area 12.6 32.1 362.8 0.2 with fluorescent latex beads were performed (Hessen, Total P 29 15 301 3 1985). The particle size preferences of Limnosida Total N 669 510 3061 237 were compared with those of the well known mi- Chlorophyll a 16.2 7.5 121.7 1.2 crofiltrator Daphnia magna (Geller & Müller, 1981; Ca 7.8 4.3 37.3 1.7 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 is more than 15 min (Peters, 1984), we assumed that lake were collected by vertical net hauls (95 µm) from the incubation time of 10 min was shorter than GPT. the epilimnion at different dates during the summer of The selectivity index, Is (−1 to 1), of each bead 1997. They were transferred to the laboratory in lake size was calculated according to Ivlev (1961). Is varies water, where they were allowed to acclimatize for 24 from −1to1.Values>0 denotes a positive selection, ◦ h(19 C) in 12 l aquaria and fed on a suspension of and values <0 a negative selection. the green algae Selenastrum capricornutum. Formalin-preserved Limnosida from Lake Gjer- Limnosida and D. magna were exposed to fluores- sjøen were sorted according to size, critical-point cent latex beads (Fluoresbrites, Polysciences) of 0.5 dried, mounted on aluminium stubs, covered with µm, 1.0 µm and 6.0 µm at concentrations of approx. gold-palladium (Polaron SEM coating unit) and ex- 2.24·106–3.07·106,7.56·105 –1.43·106,2.88·104 – amined by scanning electron microscopy (SEM) (Jeol − 6.50·104 beads ml 1 in separate 100 ml beakers. The JSM-6400 scanning microscope). The intersetulae dis- food concentration (S. capricornutum) in these exper- tances (ISD) were measured on the 5 first thoracic − iments was approx. 0.08 mg C l 1. The number of appendages on several individuals from each size animals in the beakers varied from 10 to 21, and all group. 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 Results a dissecting binocular. Depending on size, from 3 to 13 animals of each size group were placed in vials with The occurrence of Limnosida in Norway is restricted distilled water and sonicated for five minutes (MSE to the southeastern part of the country (Fig. 1). It Soniprep 150), which caused a breakdown of the an- has been recorded in 45 lakes, and 40 of these were imal tissue. The suspension of particles was filtered on included in our survey. The 65 lakes in our survey rep- black 0.2 µm polycarbonate filters and counted with a resented a range from oligotrophy to eutrophy, with fluorescence microscope (Leitz Laborlux S). a total P concentration from 3 to 301 µgl−1,but A second series of experiments was performed to with the majority of lakes being oligotrophic (Table compare the feeding rate and selection of latex beads 1). The Ca concentration ranged from 1.7 to 37.3 mg of Limnosida to that of more natural food. 14C-labelled l−1 (Table 1). Both Ca and total P were skewed to- S. capricornutum (cell size of approx. 3 × 7 µm) was wards lower values, and became more symmetric after − added to the beakers (approx. 0.8 mg C l 1), together log transformation. Total P was correlated with chloro- with the latex beads (0.5 µm, 1.0 µm and 6.0 µm). phyll a (log (TP) vs log(Chl. a): r = 0.93, p<0.0001), In this experiment, 200 ml beakers were used and the justifying the use of total P as the single productivity number of animals was doubled. variable. Total P was also correlated with Ca (log(TP) About 10% of the animals in both experiments did vs log(Ca): r = 0.54, p<0.0001). not ingest the beads. These were probably dead or un- Univariate logistic regression testing the occur- healthy specimens. As for many cladocerans, the gut rence of Limnosida along gradients of Ca and total P passage time (GPT) for different types of natural food (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 occurred in lakes belonging to category 6, suggesting total P (Ca: p = 0.0003, total P: p = 0.039). Bivariate a relatively high resistance towards fish predation. logistic regression for the occurrence of Limnosida in Limnosida commonly co-occurred with a number relation to Ca and total P gave significant effect of Ca of abundant cladocerans (Fig. 3). Most frequent co- only (p = 0.0003). This indicates that Ca was more occurrence was recorded with Daphnia cristata, Dia- important than total P for the occurrence of Limnosida. phanosoma brachyurum, Bosmina longispina, Bos- The biotic preferences of Limnosida were related mina coregoni and Bosmina longirostris. Yule’s Q to fish and zooplankton communities as well as to the was positive for Limnosida and each of the species preferred food size spectra. The fish communities in D. cristata, Holopedium gibberum and B. coregoni most of the 65 lakes from the survey were dominated (Table 2). The occurrence of Limnosida was thus pos- by cyprinids and had thus an assumed high fish pred- itively associated with these three species, of which at ation on zooplankton. Limnosida almost exclusively 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% con- effective consumer of bacteria and the smallest algal fidence interval), for L. frontosa and each of the other species in the lake survey. Significant values (p<0.05) in bold. Q varies species. from −1 to 1. A value of 0 indicates no association, values > 0 Clearance rates calculated from the ingested latex positive association, and values < 0 negative association. Abbre- beads also varied with bead size and animal size (Fig. viations as in Figure 3. D. longiremis and D. longispina occurred 5). Both Limnosida and Daphnia showed increased in less than 5 of the 65 lakes, so Yule’s Q was not calculated for these and L. frontosa clearance rates with increasing particle size. There was also a tendency for increased clearance rates with Species combination Yule’s Q increasing animal size for both species. Limnosida L. fro. and D. cri. 0.570.39 had considerably lower clearance rates than D. magna L. fro. and H. gib. 0.480.33 (Fig. 5a,c). The combined experiments with beads and 14 L. fro. and B. cor. 0.430.29 C-labelled algae gave similar clearance rates for the L. fro. and B. log. 0.190.43 two largest sizes of beads and algae (Fig. 5b), indic- L. fro. and Chy. 0.140.57 ating that the feeding response of Limnosida to beads L. fro. and D. bra. 0.050.51 and to natural food were comparable. L. fro. and C. spp. −0.140.60 An increase in Limnosida clearance rates was ob- L. fro. and B. lon. −0.190.61 served during the summer. The animals collected at L. fro. and D. cuc. −0.190.61 the different dates have different histories with respect L. fro. and D. gal. −0.260.94 to parameters, such as food conditions and temper- L. fro. and D. hya. −0.481.02 ature. 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 65 lakes from the survey covered a limited range the 5 first appendages. 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 The food size preference in Limnosida was in- regression is complicated by the correlation of Ca and ferred from filter mesh sizes and the size spectrum of total P. Bi- and multi-variate logistic regression takes ingested particles. The intersetulae distances (ISD) of this into account (Jongman et al., 1995), and Ca ap- Limnosida ranged from 0.4 to 1.2 µm depending on peared to be a more important parameter than total P animal size and site on the filters. ISD increased with for the occurrence of Limnosida. animal size, and variations in ISD were less in the Limnosida’s preference for lakes of low productiv- smallest animals (Fig. 4). Based on these morpholo- ity with low Ca concentrations corresponds well with gical studies, Limnosida would not be considered an 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 14C-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 14C-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 require- preferred lakes of low productivity. Lakes of in- ments compared to other species (Wærvågen et al., creasing productivity will have an increasing biomass unpubl. data). The observed preference of Limnosida of planktivorous fish (Johansson & Persson, 1986; for lakes with low Ca concentrations could be an in- Jeppesen, 1998). As a consequence, these lakes could direct effect of decreased competitive abilities from also have an increasing predation pressure on zo- species with higher Ca demands, such as certain daph- oplankton. Limnosida thus seems to be fairly resistant nids, at low Ca levels (Hessen et al., 1995a; Wærvågen to predation from fish and are surely able to coexist et al., unpubl. data). with cyprinids. Nevertheless, the predation pressure Considering the biotic properties of the lakes, Lim- from fish in the most productive lakes might be too nosida apparently preferred lakes dominated by dif- high to allow for persistence of Limnosida in these ferent cyprinids. Migration barriers restrict the occur- lakes. rence of these fish to southeastern Norway (Huitfeldt- The spreading of Limnosida do apparently not Kaas, 1924). Consequently, the distribution of lakes cause strong effects on the zooplankton communit- in category 6 coincide with that of Limnosida. These ies. The differences in co-occurrence and association lakes had a relatively high supposed fish predation between Limnosida and other cladocerans in the lake pressure on zooplankton. However, Limnosida also survey (Fig. 3) is probably partly caused by the 97 geographic distribution of species and partly by the ism in the particle capture of many cladocerans (Geller differences between species in demands to abiotic & Müller, 1981). parameters, resistance to predation and general com- Limnosida has previously been found in lakes of petitive abilities. The occurrence of Limnosida was relatively low productivity (Pejler, 1965). The present positively associated with H. gibberum, which has a study supports this observation. Decreased competi- more restricted occurrence. Like Limnosida, H. gib- tion from cladocerans with higher Ca demands as well berum is mainly found in lakes of low productivity as moderate fish predation may be important factors. and Ca levels (Pejler, 1965; Hessen et al., 1995a). H. The food preferences of the species could add to this. gibberum is probably also a superior competitor at low It has been suggested that high efficiency bacteria Ca, because of its low Ca requirements (Wærvågen feeders could have a competitive advantage in more et al., unpubl. data). This could explain this species’ productive lakes (Geller & Müller, 1981). Species positive association with Limnosida. The associated capable of utilising small particles will be favoured, occurrence of the two common species D. cristata and when the distribution of food particles changes from B. coregoni with that of Limnosida could be partly ex- being dominated by medium sized algae in relative oli- plained by the vulnerability of these species to fish. gotrophic lakes to microalgae and bacteria combined Like Limnosida, D. cristata and B. coregoni are fairly with large inedible algae in eutrophic lakes (Hessen et resistant to predation (Hessen et al., 1995b), and al., 1986). Low efficiency bacteria feeders, like Lim- they would therefore be less preyed upon in the lakes nosida, could thus be better adapted to the food regime dominated by cyprinids. in less productive lakes. In the feeding experiments, Limnosida had by far We found no sign of competitive exclusion by Lim- lower clearance rates for all sizes of beads than D. nosida. In general, zooplankton communities did not magna, which is known to have rather high size- differ between lakes with or without Limnosida.In specific clearance rates (McMahon & Rigler, 1965; Lake Gjersjøen Limnosida have coexisted with the Kersting & Van Der Leeuw, 1976). Though clearance native zooplankton since it invaded the lake in 1985, rates determined with artificial particles in laboratory although it may occur in fairly high biomasses in experiments does not mimic natural conditions, it still some samples (Faafeng, unpubl. data). In 1997, Lim- indicates that Limnosida has lower clearance rates than nosida also showed a pronounced seasonal and/or D. magna. spatial niche overlap with D. brachyurum, D. cristata, Larger individuals of Limnosida hadhighclear- B. longispina and B. longirostris in this lake (Jensen, ance rates compared with other cladocerans (Burns 1999). One mechanism that could reduce resource & Rigler, 1967; Ganf & Shiel, 1985). Filter area competition and thus promote coexistence between (Korínekˇ & Machácek,ˇ 1980; Ganf & Shiel, 1985) and Limnosida and other species is niche differentiation mesh size (Korínekˇ and Machácek,ˇ 1980; Geller & with respect to food size spectra. Since Limnosida Müller, 1981; Brendelberger & Geller, 1985) both in- was found to be a low efficiency bacteria feeder, the crease with body size. According to Crittenden (1981), invasion of the species may not interfere significantly the discharge rate increases disproportionately with with high efficiency bacteria feeders like D. brachy- mesh size. Furthermore, the thoracic beat rate (Watts urum and many daphnids (Geller & Müller, 1981; & Young, 1980) depends on animal size. All this may Hessen, 1985). The effect on other zooplankton spe- contribute to increased clearance rates with animal cies with high Ca requirements might be most adverse size. in lakes with low Ca where these species have reduced The differences in mesh size between size groups competitive abilities due to the suboptimum calcium of Limnosida were too small to cause a difference in concentrations. It seems that the invasion of Limnosida particle size selection between size groups. However, does not pose a serious threat to native zooplankton larger individuals of Limnosida will probably have a species. broader food size range than smaller ones, since lar- Invasions of so-called ‘exotic species’, not natur- ger individuals will be able to ingest larger particles ally occurring in that geographical area, have often (Burns, 1968). had major consequences for the system they invaded Particle size selection of Limnosida seemed to cor- (Baskin, 1992; Yan & Pawson, 1997). In the cases relate well with filter mesh size, and this study thus cited above, species have come together recently, and gives support to the sieving model, where mechanical so the evolutionary forces have had a short time to filtering is supposed to be the most important mechan- bring balance to species interactions. When Limnosida 98 appears in new lakes, it is often found together with Burns, C. W. & F. H. Rigler, 1967. Comparison of filtering rates of species naturally occurring within the same geograph- Daphnia rosea in lake water and in suspensions of yeast. Limnol. ical range. In this case, species interactions are old, Oceanogr. 12: 492–502. Chow-Fraser, P. & E. J. Maly, 1992. Size divergence and diet- and the evolutionary forces might have brought bal- ary partitioning enhance coexistence of two herbivorous species ance to the interactions between the species. The of Diaptomus (Copepoda: Calanoida) in some shallow Quebec prehistory of the species interactions may explain why lakes. Can. J. Zool. 70: 1016–1028. Crittenden, R. N., 1981. Morphological characteristics and di- Limnosida does not seem to affect native cladocerans mensions of the filter structures from three species of Daphnia upon invasion, though this remains speculative. (Cladocera). Crustaceana 41: 233–248. In conclusion, Limnosida preferred lakes with low Faafeng, B. A. & D. O. Hessen, 1993. Nitrogen and phosphorus Ca and low total P. Invading new lakes it will most concentrations and N:P ratios in Norwegian lakes: perspectives on nutrient limitation. Verh. int. Ver. Limnol. 25: 465–469. likely be found in soft water lakes of low productiv- Freeman, D. H., 1987. Applied categorical data analysis. Marcel ity. This is probably due to reduced competition from Dekker, Inc., New York: 318 pp. species with higher Ca requirements and a lower fish Ganf, G. G. & R. J. Shiel, 1985. Feeding behaviour and limb mor- predation on zooplankton in these lakes compared phology of two cladocerans with small intersetular distances. Aust. J. mar. Freshwat. Res. 36: 69–86. to more productive lakes. Furthermore, Limnosida Geller, W. & H. Müller, 1981. The filtration apparatus of Clado- was found to be a low efficiency bacteria feeder, so cera: Filter mesh-sizes and their implications on food selectivity. the invasion of the species may not interfere signi- Oecologia 49: 316–321. ficantly with microfiltrators like D. brachyurum and Hardin, G., 1960. The competitive exclusion principle. Science 131: 1292–1297. many daphnids. This was supported by community Harper, D., 1984. Recent changes in the ecology of Lake Naivasha, analysis. Limnosida commonly co-occurred with other Kenya. Verh. int. Ver. Limnol. Verh. 22: 1193–1197. filter-feeding cladocerans. Havens, K. E., N. D. Yan & W. Keller, 1993. Lake acidification: Ef- fects on crustacean zooplankton populations. Envir. Sci. 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