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［Japanese Journal of Water Treatment Biology Vol.53 No.4 119－128 2017］

Combined Impacts of Algal Density and Copepod Predation on the Community of Small-Sized Zooplankton

TAKAMARU NAGATA1* and TAKAYUKI HANAZATO2

1Lake Biwa Environmental Research Institute/5－34 Yanagasaki, Otsu, Shiga 520－0022, Japan 2Institute of Mountain Science Shinshu University, Division of Science for Inland Water Environment /5－2－4 Kogandori, Suwa, Nagano 392－0027, Japan

Abstract We assessed the combined impacts on the community of small-sized herbivorous zooplankton using mesocosms, in which their populations were exposed to copepod Mesocyclops pehpeiensis predation and/or food shortage. The densities of the small-sized zooplankton were depressed in the tanks with M. pehpeiensis and a low algal density, probably because the prey populations were unable to compensate for the population loss by copepod predation. In contrast, most of the herbivorous zooplankton, especially rotifers, established large populations, despite their exposure to predation in the tanks with high algal density. This might be due to their high reproductivity under the conditions. In addition, the release from competitive pressure by cladocerans, whose populations were suppressed by intensive predation by M. pehpeiensis, would be favorable for the rotifers. Our experimental findings may explain the herbivorous zooplankton community structure in the shallow eutrophic lakes inhabited by abundant copepods. The results may become valuable information for reducing biological interference with rotifers within zooplankton assemblages, leading to effective use of the animals for water treatment systems.

Keywords: community structure, copepod predation, food abundance, small sized zooplankton

( ) INRODUCTION algal, bacterial and detrital resources , which governs the reproduction of zoo­ Predacious copepods often appear abun­ plankton populations5)－8). Herbivorous zoo­ dantly in lakes, and impose high predation plankters compete with one another for food pressure on small-sized herbivorous zoo­ resources because most of them utilize plankton such as rotifers1). Copepods prey particles within a common size range of up effectively on small-sized, soft-bodied, and to 25 µm (4－17 µm for rotifers8)－11); 1－25 µm non-spined prey zooplankton species2),3). This for cladocerans7),12),13). Many studies have is probably the main factor accounting for shown that population densities of the small the phenomenon that, in the field, copepods zooplankters, such as rotifers, decline in the exert different degrees of predation pressure presence of large cladocerans such as on each of herbivorous zooplankton popu­ Daphnia9),11). Cladocerans generally have lations, and that they alter species composition large body and food competition advantage of the prey community1),4). over rotifers. This advantage is attributed A factor other than predation that controls mainly to the fact that large zooplankters population dynamics of small-sized her­ have a high clearance rate and tolerance to bivorous zooplankton is food abundance starvation9). In addition, the wider size range ＊ Corresponding author Phone number: +81 77 526 4800 E-mail: [email protected] 120 Japanese J. Wat. Treat. Biol. Vol.53 No.4 of food particles available to cladocerans, in 100 L, diameter 40 cm, height 73 cm) were comparison with rotifers, may contribute to used for the experiment. To establish a the better food competitiveness. zooplankton community in each tank, the The community structures of herbivorous bottom sediments of the eutrophic Lake zooplankton would be controlled in a complex Suwa, Japan, including resting eggs of manner by food resources and invertebrate various zooplankton species, was collected at predation. It is expected that the populations the center of the lake (6 m depth; 36°2’N, of small-sized zooplankton species, especially 138°5’E) with an Ekman grab sampler. About rotifers, which dominate zooplankton com­ 1.5 kg of sediment was placed in each tank, munities in eutrophic lakes (generally fish- which was then filled with 80 L of tap water, abundant lakes) are imposed strong effect by and the experiment was started (day 0). All the combined effects. Predaceous copepods of the tanks were kept in the laboratory in a play significant role in determining com­ controlled environment (temperature 20℃, munity structures of herbivorous zooplankton photoperiod 16－h light/8－h dark). On day 10, even in such lakes1),14) because they are able the mesocosm tanks were divided into two to maintain its populations by their escape groups of six tanks each: low-food tanks and response, diel vertical migration which is high-food tanks (Fig. 1). On the same day, to effective to reduce predation pressure by create different food levels for the herbivorous fish15). Chang and Hanazato16) have performed zooplankton in the tanks, we added the a community-level laboratory experiment to green alga Chlorella vulgaris (purchased evaluate the combined impacts of food from Chlorella Industry Co. Ltd., Fukuoka, abundance and copepod predation on zoo­ Japan) to the low-food and high-food tanks to plankton assemblage. However, they were create algal densities of approximately 1×103 unable to evaluate the combined impact on cells/mL and 1×105 cells/mL, respectively. planktonic rotifer species since the densities Algae were added repeatedly at 1－ or 2－day of such species were low, but the benthic intervals, thereafter. On day 19, 120 adults species Lepadella sp. was abundant during of Mesocyclops pehpeiensis (body length, > the experiment. Thus, we tried to assess the 1000 µm) were introduced into each of three combined impacts of algal concentration and low-food tanks and three high-food tanks copepod predation on small-sized herbivorous (low-food Mesocyclops tanks, high-food zooplankton, particularly planktonic rotifer Mesocyclops tanks, respectively). The pred­ populations in a community-level experiment. ators were obtained from Lake Suwa one month before the start of the experiment and MATERIALS AND METHODS maintained in the laboratory with a Twelve cylindrical plastic tanks (volume zooplankton assemblage collected from the

Figure 1 The experimental protocol. Combined Impacts of Algal Density and Copepod Predation on the Community of Small-Sized Zooplankton 121 lake. No invertebrate predators were early and late copepodite stages are generally introduced into the remaining three low-food known to be herbivorous and omnivorous, tanks and three high-food tanks, which respectively, and therefore the latter stage is served as controls (low-food control tanks, considered to be when M. pehpeiensis feeds high-food control tanks, respectively). The mainly on herbivorous crustaceans and experiment was terminated on day 27. rotifers. Water temperature and phytoplankton The data sets were analyzed using 2 × 2 biomass indicated by chlorophyll a (chl. a) in factorial ANOVA with the difference in algal the tanks were measured at 1－ or 2－day density and the introduction of M. pehpeiensis intervals. Water temperature was measured as the main factors, and day as repeated with a thermister (YSI 55 dissolved oxygen measures. The differences in density of meter; YSI Co., Ohio, USA). For measurement zooplankton species among tanks subjected of chl. a, 100 mL of water was collected from to different treatments were analyzed each tank and filtered through a Whatman statistically with two-way repeated-measures GF/C filter, and then chl. a in the particles ANOVA using StatView ver.5 (SAS Institute that remained on the filter was measured Inc., Cary, NC, USA). using methyl alcohol and fluorescence 17) RESULTS according to Marker et al . Zooplankton were sampled from all the Water temperature did not differ markedly tanks on day 16 and at 1－ or 2－day intervals between the control and the Mesocyclops thereafter. To collect zooplankton samples, tanks under the respective food conditions the water column (3.0 L in volume) from the (Fig. 2). Under the high-food conditions, the surface to 32 cm depth (approximately 20 cm values of chl. a tended to be lower in the above the bottom sediment) in the tanks was control tanks than those in the Mesocyclops collected using a column sampler (diameter 5 tanks, but the difference was not significant cm, length 50 cm) with a hydraulically (repeated-measures ANOVA, treatment: F = operated bottom flap. Since some zooplankters 1.211, P = 0.2820). The values of chl. a in the might have been distributed unequally in the low-food tanks were very low and were tanks, the water was gently mixed with a therefore hardly determined during most of wooden rod before sampling to make their the experimental period. distribution uniform. Zooplankton were then It was impossible to completely exclude M. collected by filtering the sampled water pehpeiensis from the control tanks, because through a 40－µm mesh net, and preserved in their resting stages were contained in the sugar-formalin containing a final concen­ bottom sediment, and hence some copepods tration of 4% formalin18). The mesh size (40 appeared in the tanks (Fig. 3). However, the µm) of the net was sufficiently smaller than densities of their early and late copepodite the body width of small species such as the stages were higher in the Mesocyclops tanks rotifers Filinia and Polyarthra8),19). Therefore, than in the control tanks during the all the crustacean and rotifer individuals experiment (Table 1). In the experiment, (except eggs) should have been collected with unexpected invertebrate predators such as the net. The water that had filtered through Leptodora kindtii (except for M. pehpeiensis) the net was returned to the tank to reduce did not appeared in the mesocosm tanks. water loss. Zooplankton in the samples were Three cladoceran (Bosmina longirostris, B. identified to species or genus level and fatalis and Bosminopsis deitersi) and four counted with a microscope at ×100 magnifi­ rotifer species (Brachionus angularis, Filinia cation. For the predator M. pehpeiensis, the longiseta, Hexarthra mira, and Keratella body lengths of individuals were measured valga) appeared commonly in the mesocosm and divided into two life stages according to tanks (Figs. 4 and 5). Their densities were Chang and Hanazato14): early copepodite higher under high-food conditions than under stages (body length < 800 µm) and late low-food conditions. The results of two-way copepodite stages including adults (body repeated measures ANOVA showed that the length ≥ 800 µm). The feeding habits of the effects of food treatment were significant for 122 Japanese J. Wat. Treat. Biol. Vol.53 No.4

Low food High food 26 26 24 Water temperature 24 Water temperature

22 22 C C o o 20 20 18 18 16 16 14 14

2.0 30 Chl. a 25 Chl. a 1 1 - 1.5 - L 20 g L g 1.0 µ µ 15 10 0.5 5 0.0 0 14 16 18 20 22 24 26 28 14 16 18 20 22 24 26 28 days days Figure 2 Changes in water temperature and chl. a (average ± SE) in the mesocosm tanks with low food density (left panel) and high food density (right panel) during the experiment. Clear circles, control tanks; Solid circles, Mesocyclops tanks.

Low food High food 3.0 20 1 1

- Mesocyclops pehpeiensis - Mesocyclops pehpeiensis 2.5 (early copepodite stages) 15 (early copepodite stages) 2.0 1.5 10 1.0 indiv. L indiv. L 5 0.5 0.0 0 14 16 18 20 22 24 26 28 14 16 18 20 22 24 26 28 days days

0.8 1.2 1 1 - - Mesocyclops pehpeiensis Mesocyclops pehpeiensis 1.0 0.6 (late copepodite stages) (late copepodite stages) 0.8 0.4 0.6 0.4 indiv. L indiv. L 0.2 0.2 0.0 0.0 14 16 18 20 22 24 26 28 14 16 18 20 22 24 26 28 days days Figure 3 Changes in density (average ± SE) of M. pehpeiensis in the mesocosm tanks with low food density (left panel) and high food density (right panel) during the experiment. Clear circles, control tanks; Solid circles, Mesocyclops tanks. Note that the scales of density (vertical axes) in the panels are different from one another. Combined Impacts of Algal Density and Copepod Predation on the Community of Small-Sized Zooplankton 123 P 0.527 0.879 0.423 0.597 0.549 0.349 0.260 0.809 0.003 F 0.718 0.756 5.793 1.138 1.401 0.322 0.636 0.224 0.960 FoodPredator× Day × P 0.760 0.875 0.520 0.630 0.333 0.466 0.898 0.807 0.004 F 1.178 0.769 0.196 0.872 0.326 5.422 0.392 0.583 0.230 PredatorDay × P 0.119 0.518 0.051 0.129 0.526 0.435 0.406 0.001 <0.001 F FoodDay × 0.773 0.758 2.103 7.354 2.031 8.637 0.934 1.000 2.885 p 0.113 0.519 0.413 0.138 0.014 0.487 0.465 <0.001 <0.001 Day F 0.770 4.152 2.154 1.971 0.873 8.421 0.983 0.830 15.461 M. pehpeiensis , M. respectively. Day was the repeated measure. Significant level in bold. P 0.175 0.188 0.059 0.446 0.240 1.000 0.001 0.002 0.006 1.810 8.722 F 1.435 1.924 0.595 3.826 0.000 14.382 11.996 FoodPredator× P 0.183 0.010 0.018 0.065 0.305 0.001 0.033 0.006 <0.001 Predator F 7.538 1.087 4.978 1.855 6.227 8.595 3.666 16.964 12.840 P 0.180 0.014 0.248 0.034 (days 21 － 27) (days <0.001 <0.001 <0.001 <0.001 <0.001 Food F 6.725 1.877 1.385 4.920 27.814 16.095 64.324 22.346 115.197 M. pehpeiensis Results of two-way repeated-measures ANOVA used to estimate the differences in the densities of each zooplankton species among treatments after used to estimate the differences ANOVA Results of two-way repeated-measures introduction of introduction early copepodite early stages latecopepodite stages F. longiseta Rotifers B.angularis K. valga B.deitersi H. mira H. Cyclopoidcopepods M.pehpeiensis B.fatalis Cladocerans B.longirostris Table 1 Table The treatment food and predator show difference in food density and with- or without or with- density and food in difference show predator and food treatment The 124 Japanese J. Wat. Treat. Biol. Vol.53 No.4

Low food High food 3.0 6 1 -1 - Bosmina 2.5 Bosmina 5 longirostris longirostris 2.0 . L 4 v 1.5 i 3 1.0 2 in d indiv. L 0.5 1 0.0 0

1.4 3.0 1 -1 - 1.2 Bosmina fatalis 2.5 Bosmina fatalis

1.0 . L 2.0

0.8 v i 1.5 0.6 1.0 in d indiv. L 0.4 0.2 0.5 0.0 0.0 0.6 60 1 -1 - Bosminopsis deitersi 0.5 Bosminopsis deitersi 50

0.4 . L 40 v 0.3 i 30 0.2 20 in d indiv. L 0.1 10 0.0 0 14 16 18 20 22 24 26 28 14 16 18 20 22 24 26 28 days days Figure 4 Changes in density (average ± SE) of cladocerans in the mesocosm tanks with low food density (left panel) and high food density (right panel) during the experiment. Clear circles, control tanks; Solid circles, Mesocyclops tanks. Note that the scales of density (vertical axes) in the panels are different from one another. the abundances of most zooplankters, except tanks during the experiment. Two-way for late copepotide stages of M. pehpeiensis repeated measures ANOVA represented that and B. deitersi (Table 1). the effects of food × predator interactions The introduction of M. pehpeiensis signifi­ were not significantly for the densities of cantly affected the zooplankton densities cladocerans (Table 1). (except for B. deitersi) in the mesocosm tanks The densities of rotifers were also (Table 1). The densities of B. longirostris and significantly affected by the predator B. fatalis were lower in the Mesocyclops treatment (Table 1). Under low-food condi­ tanks than in the control tanks, especially tions, like the cladocerans, the rotifer under low food-conditions (Fig. 4). Although abundances were lower in the Mesocyclops the abundances of two cladoceran species tanks than in the control tanks (Fig. 5). In were significantly influenced by the predator contrast to the cladocerans and the rotifer treatment, their abundances under high-food populations under low-food conditions, the conditions were not different between the densities of rotifers in the high-food control Mesocyclops tanks and the control tanks tanks were lower than those in the high-food (repeated measures ANOVA: B. longirostris, Mesocyclops tanks (Fig. 5), although signifi­ F = 0.2, P = 0.63; B. fatalis, F = 4.5, P = cant differences in the densities between the 0.05). On the other hand, the effects of control and the Mesocyclops tanks were predator (introduction of M. pehpeiensis) were observed only for B. angularis and H. mira not significant for B. deitersi, but the density (Table 1, food × predator interaction: B. of the cladoceran in the Mesocyclops tanks angularis, F = 14.38, P = 0.0001; H. mira, F was low as compared with in the control = 8.72, P = 0.006). Combined Impacts of Algal Density and Copepod Predation on the Community of Small-Sized Zooplankton 125

Low food High food 10 400 1 1

- Brachionus angularis - Brachionus angularis 8 300 L 6 200 4 indiv. L indiv . 2 100 0 0 50 1600 1 1

- Filinia longiseta - Filinia longiseta 40 1200 30 800 20 indiv. L indiv. L 10 400 0 0 50 400 1 1

- Hexarthra mira - Hexarthra mira 40 300 L 30 200 20 indiv. L indiv . 10 100 0 0

3.0 160 1 1

- Keratella valga - Keratella valga 2.5 120 2.0 1.5 80 1.0 indiv. L indiv. L 40 0.5 0.0 0 14 16 18 20 22 24 26 28 14 16 18 20 22 24 26 28 days days Figure 5 Changes in density (average ± SE) of rotifers in the mesocosm tanks with low food density (left panel) and high food density (right panel) during the experiment. Clear circles, control tanks; Solid circles, Mesocyclops tanks. Note that the scales of density (vertical axes) in the panels are different from one another.

of algal density and copepod predation on DISCUSSION planktonic species before the dominance of In contrast to Chang and Hanazato16), most periphytic and/or benthic species. The rotifers in the present study were planktonic combined impacts played important roles in species. This might be due to the difference structuring the community of small-sized of lapsed days from the addition of lake herbivorous zooplankton. The results suggest sediments to the end of the experiment. that the responses against the effects differ Because mesocosm tanks have walls, among zooplankton populations. periphytic and/or benthic species often domi­ All of the herbivorous zooplankton species nate zooplankton community when many without Mesocyclops tanks established larger days elapse after the addition of lake populations under high-food conditions than sediments to the tanks. However, we under low-food conditions. This might be succeeded in examining the combined impacts because the zooplankters attained high 126 Japanese J. Wat. Treat. Biol. Vol.53 No.4 reproductivity under plenty food conditions. rotifers in the control tanks might have been These results can be expected by huge due to competitive pressure by cladocerans. previous literatures. On the other hand, most On the other hand, the early copepodite herbivorous zooplankton populations were stages of cyclopoid copepods including the negatively affected by M. pehpeiensis under genus Mesocyclops are regarded as feeding low-food conditions, in agreement with the on algae although few studies have shown results of Chang and Hanazato16). The values feeding rate of the animals on algae. Thus, of chl. a under low-food conditions were close perhaps the early copepodite stages of M. to zero during the experiment (Fig. 2). pehpeiensis might also exert competitive Therefore, zooplankton would have been pressure on rotifers. exposed to both food shortage and M. With a mesocosm experiment, Chang and pehpeiensis predation in the Mesocyclops Hanazato16) reported that most herbivorous tanks. The food shortage would have reduced cladoceran populations were subjected to their reproductivity and probably made it high predation pressure by M. pehpeiensis difficult for their populations to compensate irrespective of algal density. In contrast to for the population loss due to predation, thus the cladocerans, the rotifer populations in increasing the impact of predation. This their experiment were not affected negatively might explain why the zooplankton popu­ by the copepod, irrespective of food abun­ lations were strongly suppressed by M. dance. In the study of Chang and Hanazato16), pehpeiensis predation under low-food con­ periphytic animals (the cladoceran Chydorus ditions. sp. and the rotifer Lepadella sp.) appeared In contrast, it seemed that the prey abundantly in the mesocosm tanks. Because populations under high-food conditions were copepods possess mechanoreceptors that hardly affected by copepod predation. detect vibrations and water displacements Interestingly, rotifers established larger pop­ created by swimming prey22), and periphytic u­lations in the Mesocyclops tanks than in the animals are generally more sessile than control tanks (Fig. 5, Table 1). However, this planktonic ones, it is difficult to assess the did not mean that the preys were not eaten relationships between food abundance and by copepods, because many studies have prey-predator interactions (planktonic zoo­ shown that they are greatly susceptible to plankton prey-invertebrate predators) in copepod predation1). In general, rotifers are pelagic food web by their study. In the present considered to have much higher population experiment, any periphytic species were growth rates than cladocerans when food is hardly observed. Therefore, we have plentiful5). Thus, rotifers might be able to succeeded in demonstrating the predation compensate for any population loss due to impact of a cyclopoid copepod on a pelagic copepod predation by their high reproductivity. zooplankton community in the presence of However, a high population growth rate different phytoplankton biomasses, and the alone cannot explain the higher rotifer den­ results indicate that zooplankton community sities that were observed in the Mesocyclops structures are shifted in a complex manner tanks than in the control tanks. Presumably, by the combined impacts of invertebrate the lower densities in the control tanks predation and food abundance. resulted from competition with cladocerans. The differences were also evident between Rotifers and cladocerans feed on particles the present study and Chang and Hanazato16) (algae, bacteria, and detritus) within similar with regard to the densities of the early and size ranges (4－17 µm for rotifers9)－11); 1－25 µm late copepodite stages of M. pehpeiensis in for cladocerans7),12),13)). In the present experi­ the low-food tanks. The early copepodite ment, we used the green alga Chlorella stages maintained low densities in the low- vulgaris as food source for zooplankton. Since food tanks (0.22－0.89 indiv./L) in the former the clearance rate of cladocerans on the alga study whereas they hardly appeared in the is higher than that of rotifers20), 21), then the latter. On the other hand, the late copepodite former animals are competitively superior to density in the low-food tanks was lower in the latter. Therefore, the low densities of the former experiment (max. density: 0.33 Combined Impacts of Algal Density and Copepod Predation on the Community of Small-Sized Zooplankton 127 indiv./L) than in the latter (max. density: an experimental analysis with mesocosms. approx. 2.0 indiv./L). In case of the genus Hydrobiologia, 556, 233－242 (2006) Mesocyclops, the early copepodite stages feed 2 ） Gilbert, J. J., and Williamson, C. E.: Predator- on rotifers in addition to algae23). Thus, it is prey behavior and its effect on rotifer possible that the early copepodite stages of urvival in associations of Mesocyclops M. pehpeiensis have imposed competitive and edax, Asplanchna girodi, Polyarthra vulgaris, predation pressure on rotifers in our and Keratella cochlearis. Oecologia, 37, 13 experiment. This might explain why the －22 (1978) rotifer populations were suppressed by 3 ） Diéguez, M. C., and Gilbert, J. J.: Suppres­ copepods in the present study than in the sion of the rotifer Polyarthra remata by study by Chang and Hanazato under low-food the omnivorous copepod Tropocyclops conditions. extensus: predation or competition. J. In eutrophic lakes, small zooplankters Plankton Res., 24, 359－369 (2002) especially rotifers are principal grazers, and 4 ） Lair, N.: Effects of invertebrate predation consume a lots of organic particles such on the seasonal succession of a zooplankton as phytoplankton and bacteria, inducing community: a two year study in Lake increase in water transparency7),8), 21),24). Due Aydat, France. Hydrobiologia, 198, 1－12 to their sharp appetite, they are used (1990) generally for water treatment systems. Our 5 ） Stemberger, R. S., and Gilbert, J. J.: Body results have shown that the community size, food concentration and population structures of small-sized zooplankton depend growth in planktonic rotifers. 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