Limnology (2003) 4:101–107 DOI 10.1007/s10201-003-0097-y
© The Japanese Society of Limnology 2003
RESEARCH PAPER
Narumi Tsugeki · Hirotaka Oda · Jotaro Urabe
Fluctuation of the zooplankton community in Lake Biwa during the 20th century: a paleolimnological analysis
Received: December 24, 2002 / Accepted: March 25, 2003
Abstract Detailed zooplankton records from a 26-cm sediment core with a time resolution of approximately 3–10 years were obtained from Lake Biwa, Japan, to examine the historical variations in the zooplankton community during the 20th century. In the sediments, selected zooplankton remains have fluctuated over the years. Daphnia – large zooplankton herbivores – did not occur from 1900 to 1920, and formed a very minor component of the zooplankton community in the following 30 years, while Bosmina – small zooplankton herbivores – were common during this period. In the mid-1960s, however, when eutrophication was noticeable in this lake, Daphnia numbers increased dramatically and became the dominant zooplankton thereafter. In contrast, Difflugia brevicolla and D. biwae, two amoeboid protozoans that live in connection with the lake bottom environment, occurred abundantly until the late 1950s, but gradually decreased after the mid-1960s. In particular, D. biwae, a species peculiar to this lake, was not found in sediment dated after 1980, suggesting its extinction. These results indicate that the zooplankton community structure changed greatly in the 1960s, and suggest that the eutrophication occurring at this time altered the relative strength of top-down and bottom-up forces on the zooplankton community in Lake Biwa. Key words Daphnia · Difflugia · Lake Biwa · Long-term changes · Zooplankton
N. Tsugeki (*) · J. Urabe Center for Ecological Research, Kyoto University, 509-3 Kamitanakami Hirano-cho, Otsu 520-2113, Japan Tel. ⫹81-77-549-8018; Fax ⫹81-77-549-8201 e-mail:
[email protected] H. Oda Center for Chronological Research, Nagoya University, Nagoya, Japan
Introduction To understand how human activities have affected given ecosystems, it is necessary to trace long-term biological trends up to the present with sufficient time resolution. Indeed, to conserve and manage lake ecosystems, quantitative information on the biological community before anthropogenic impacts become apparent is essential. However, at time scales of decades or longer, direct biological monitoring of ecosystems is rare. In general, such a monitoring program starts after symptom of something changes are recognized, and so quantitative information on the biological community before an anthropogenic impact becomes apparent is not available. One method to overcome such a situation in lake ecosystems is paleolimnological analysis of plankton remains (Anderson 1993; Jeppesen et al. 2001). Paleolimnology is the study of lake ecosystem structure and function based on the historical record in sediments (Leavitt et al. 1993). A number of limnological and ecological studies have clarified functions of, species interactions among, and preferred environmental conditions of plankton. Using such information, it is possible to reconstruct the food web structure (Kerfoot 1974) and trophic interactions that dominated in the past (Kitchell and Kitchell 1980; Leavitt et al. 1989) from the absolute and relative abundance of sedimentary remains of plankton. In the present study, such an approach was applied to Lake Biwa, the largest lake in Japan. Lake Biwa is one of the ancient lakes of the world and is the most species-rich freshwater habitat in Japan. It provides water resources for 14 million people living in the Kansai region. Thus, Lake Biwa is both biologically and economically important. Although anthropogenicallyinduced eutrophication has been recognized since the early 1960s (Ogawa et al. 2001), intensive plankton monitoring was not started until 1965 (Mori et al. 1967). Before 1960, several studies described the planktonic fauna and flora in this lake but did not examine the plankton community quantitatively (Kawamura 1918; Ueno 1934; Negoro 1954). In Lake Biwa, paleolimnological studies were conducted by
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Horie (1984), but that study examined microfossils of plankton in the sediment obtained from 200-m cores dated at about 400 000 years BP (Kadota 1976, 1984). Thus, little is known of the structure of the plankton community just before the eutrophication began. Therefore, we tried to quantitatively trace changes in the plankton community over the past 100 years in the lake. We focused mainly on cladocerans, because their remains are well preserved in lake sediments (Leavitt et al. 1993; Jeppesen et al. 2001). In addition, they play important roles in lake ecosystems as dominant herbivores and the prey of planktivorous fish. The biomass of herbivorous plankton increases with increasing algal biomass (McCauley and Kalff 1980), and the species composition of cladocerans is profoundly affected by fish (Brooks and Dodson 1965; Leavitt et al. 1989) and invertebrate predators (Kitchell and Kitchell 1980). Thus, by examining the composition and absolute abundance of cladoceran remains in sediments, we can infer past changes in algal abundance and strength of predation pressure by planktivorous fish (Leavitt et al. 1993; Jeppesen et al. 2001). Beside cladoceran remains, we also examined rhizopod remains and algal pigments in the sediments to assess historical changes in the trophic and physicochemical conditions of Lake Biwa. These results will provide an insight into how and why the plankton community in Lake Biwa has changed over the 20th century.
Material and methods Fig. 1. Location of the sampling sites
Sediment core A 26-cm-long sediment core was collected from the north basin of Lake Biwa at a pelagic site (water depth of 75 m; 35°15⬘N, 136°04⬘E) with a 10.9-cm-inside-diameter gravity corer on 16 April 2001 (Fig. 1). The core was carefully cut in 1-cm increments from the surface to a depth of 26 cm. Each increment was sealed in a shield bag and stored at 4°C until analysis. Dating We used 210Pb and 137Cs to determine the age of the lake sediments, because both are effective measures for dating sediments deposited during the past 100–150 years (Roberts 1998). 210Pb and 137Cs activities were measured by gammaray spectrometry. Dried samples for 210Pb and 137Cs were sealed in standard holders to allow 222Rn and its short-lived daughters to equilibrate. After achieving equilibrium for at least two weeks, concentrations of radioisotope were determined with a high-purity Ge-detector (GWL-120230-S, EG&G Ortec, Oak Ridge, TN, USA). The activity is expressed as excess of 210Pb (termed 210Pbexcess hereafter), which is defined as total 210Pb concentration minus 210Pb that is produced within soils (termed the supported fraction), assuming the supported 210Pb to be in equilibrium with 214Pb. A geochronology was established according to the constant initial concentration (CIC) 210Pb dating model (Robbins and Edgington 1975). The average mass accumulation rate
(g cm⫺2 year⫺1) was determined from 210Pb activity for the part of the sediment core above 22 cm (see Table 1) and applied to determine the age of the lake sediments from 26 cm below the lake bottom to the lake bottom itself. The validity of the dating was checked by the peak of the 137Cs impulse, which was traced in the early 1960s (Roberts 1998). The sedimentation rate (cm year⫺1) was calculated from the estimated calendar year (AD) and the thickness of the sediment sample. Pigments and microfossil analyses Algal pigments in sediment samples (1.5 g wet weight) were extracted in 20 ml of 90% acetone for 24 h at room temperature in the dark. The samples were then centrifuged, and the concentration of chlorophyll-a ⫹ phaeopigments in the supernatant was analyzed fluorometrically according to the method of Lorenzen (1967). The concentration was used to roughly evaluate changes in the abundance of planktonic algae. Zooplankton remains were analyzed according to a simplified method of Frey (1986). At each depth, a known amount of wet sediment, generally 3 g, was dispersed in 100 ml of distilled water. After the suspension was homogenized by shaking by hand, 1 ml was subsampled and observed under 100⫻ and 400⫻ magnification in a Sedgewick–Rafter cell. For the identification of cladoceran
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remains, headshields, shells, postabdomens, and postabdominal claws were used. In each sample, at least 100 fragments of these skeletal components were counted. Then, for each taxon, we adopted the most abundant skeletal component as a measure of remains per unit of sediment (Hofmann 1978; Frey 1986). We also enumerated rhizopods, which are small amoeboid protozoa with protective structures made of chitinous membranes or cemented minute sand grains. We counted two Difflugia species, Difflugia biwae Kawamura and D. brevicolla, because they were easily identified and abundant. Because we counted them in the same samples as the cladoceran remains, the total counts of rhizopod tests per sample varied from 4 to 575, depending on the depth of sediment. The flux of zooplankton remains (FZ: individuals cm⫺2 year⫺1) and algal pigments (FA: µg cm⫺2 year⫺1) were calculated as follows (Brugam 1978), FZ ⫽ number of remains per cm3 of sediment ⫻ sedimentation rate (cm year⫺1) FA ⫽ amount of pigments per cm3 of sediment ⫻ sedimentation rate (cm year⫺1)
Results Dating The profiles of 210Pbexcess in the sediment core clearly showed a linear reduction with depth, suggesting that the sediment was not disturbed vertically (Table 1). The 210Pbexcess activities decreased systematically from 0.63 Bq g⫺1 in the surface layer to 0.051 Bq g⫺1 at a core depth of 22 cm. From these data, the average mass accumulation rate of the lake sediment was estimated as 0.0857 g cm⫺2 year⫺1 and the calendar year ranged from 1901 at a core depth of 26 cm to 2001 at the surface of the lake bottom. The 137Cs activities increased linearly from 0.016 Bq g⫺1 at the bottom surface to 0.082 Bq g⫺1 at core depths of 13–14 and 15–16 cm and then decreased below these layers. This vertical profile indicates that a peak of 137Cs exists at a core depth of 14–15 cm. From this result, we assigned this layer to the early 1960s, in close agreement with the age estimated by 210Pb dating. Sedimentation rates estimated from calendar years based on the 210Pbexcess activity and the thickness of the lake sediment varied between 0.18 and 1.1 cm year⫺1 in the top 22 cm of sediment and decreased gradually with depth. Before 1950, the flux of chlorophyll (chlorophyll-a ⫹ phaeopigments), estimated from the sedimentation rate and chlorophyll concentration in the sediment, was less than 1.6 µg cm⫺2 year⫺1 (Fig. 2). However, it increased by five times from 1960 to 1980. Thereafter, the flux was stable at a high level except for the most recent years, when the highest flux was recorded because of the precipitation of fresh algae. Microfossil analyses Cladoceran remains were found in all samples. In particular, Daphnia, Bosmina, and Chydorus were abundant, de-
Table 1. 210Pb and 137Cs analytical results of a sediment core collected from the north basin of Lake Biwa Sample no.
Depth (cm)
210 Pbexcess (Bq g⫺1 ⫾ s.d.)
137 Cs (Bq g⫺1 ⫾ s.d.)
210 Pb age (year, AD)
I0 I1 I2 I3 I4 I5 I6 I7 I8 I9 I10 I11 I12 I13 I14 I15 I16 I17 I18 I19 I20 I21 I22 I23 I24 I25
0–1 1–2 2–3 3–4 4–5 5–6 6–7 7–8 8–9 9–10 10–11 11–12 12–13 13–14 14–15 15–16 16–17 17–18 18–19 19–20 20–21 21–22 22–23 23–24 24–25 25–26
0.632 ⫾ 0.026 0.590 ⫾ 0.030 0.609 ⫾ 0.030 0.475 ⫾ 0.029 0.415 ⫾ 0.028 0.344 ⫾ 0.028 0.444 ⫾ 0.028 0.363 ⫾ 0.028 0.251 ⫾ 0.028 0.207 ⫾ 0.028 0.254 ⫾ 0.028 0.235 ⫾ 0.027 n.d. 0.145 ⫾ 0.028 n.d. 0.112 ⫾ 0.027 n.d. 0.133 ⫾ 0.028 n.d. 0.0778 ⫾ 0.027 n.d. 0.0513 ⫾ 0.027 n.d. n.d. n.d. n.d.
0.0158 ⫾ 0.0023 0.0188 ⫾ 0.0027 0.0253 ⫾ 0.0027 0.0265 ⫾ 0.0027 0.0316 ⫾ 0.0027 0.0331 ⫾ 0.0027 0.0351 ⫾ 0.0028 0.0348 ⫾ 0.0028 0.0453 ⫾ 0.0028 0.0520 ⫾ 0.0029 0.0582 ⫾ 0.0029 0.0635 ⫾ 0.0030 n.d. 0.0823 ⫾ 0.0032 n.d. 0.0823 ⫾ 0.0031 n.d. 0.0417 ⫾ 0.0029 n.d. 0.0166 ⫾ 0.0026 n.d. 0.00564 ⫾ 0.0025 n.d. n.d. n.d. n.d.
2000 1999 1997 1994 1991 1989 1986 1983 1980 1977 1974 1971 1967 1963 1959 1955 1950 1945 1939 1933 1928 1922 1917 1912 1906 1901
s.d., standard deviation; n.d., no data
Fig. 2. Depth and time profiles of chlorophyll flux (chlorophyll-a ⫹ phaeopigments) in the north basin of Lake Biwa
pending on the depth of sediment (Fig. 3). Leptodora and Diaphanosoma were also found, but their abundance was very low. In the sediment sample collected at a depth of 1–2 cm, several postabdominal claws of the Daphnia pulex group were found. These probably come from D. pulicaria,
104 Fig. 3. Depth and time profiles of flux for remains of (a) Daphnia, (b) Bosmina, and (c) Chydorus; and (d) percentage contribution of these taxa to total cladoceran remains
which has been abundant in recent years (Urabe et al., in preparation). Judging from the morphology, other Daphnia remains belonged to the subgenus Hyalodaphnia. According to morphological features, the Hyalodaphnia in Lake Biwa were identified as D. galeata (Tanaka 1992). However, genetic analysis suggests that the Hyalodaphnia in this lake include two genetically distinct species of the D. galeata group and their hybrids (Ishida and Urabe, in preparation). Since we could not distinguish these species and hybrids on the basis of the morphology of the remains, we treated them as one taxon. From the morphology of Bosmina remains, we identified B. longirostris and B. fatalis. However, we recorded these species as one taxon. The relative abundance of these Bosmina species will be presented in another report. Daphnia remains were not found in the sediment dated before 1920 and were rare in the subsequent 30 years. However, in sediments dated after 1960, their remains were abundant. The flux of Daphnia remains increased dramatically from 1960 to 1980, as did the flux of chlorophyll. The flux of Daphnia decreased in the mid-1980s but recovered to higher levels in recent years. The Bosmina results were similar to the Daphnia results. However, unlike Daphnia, Bosmina were commonly found before 1950, and no substantial increase in the flux occurred until 1970. Chydorus remains were also commonly found in the sediments dated after 1990, but the flux was much lower than those of Daphnia and Bosmina remains. We also found resting eggs of Daphnia species in several samples but the number was in general less than one thousandth of Daphnia remains in total. Stratigraphic data of the Daphnia resting eggs will be shown with genetic analyses elsewhere (Ishida and Urabe, in preparation). In contrast to the cladocerans, the remains of the two rhizopod species were abundant before 1960 and decreased dramatically thereafter (Fig. 4). In particular, Difflugia biwae remains were not found at all in the sediment dated after 1980. Throughout the study period, the flux of D. brevicolla remains was at least four times higher than that of D. biwae.
Fig. 4. Depth and time profiles of flux for remains of (a) Difflugia biwae and (b) Difflugia brevicolla
Discussion In the present study, the calendar year of sediment samples as calculated from 210Pb dating ranged from 1901 at a depth of 26 cm to 2001 at the surface of the lake bottom. The reliability of this chronology was confirmed by 137Cs activity. However, the sedimentation rate in our study was much higher than that of Ogawa et al. (2001), who dated sediments collected at 8.5 cm depth at 1901. They collected sediment core samples at a site 8 km north from our sampling site. According to them, the nitrogen isotope ratio (δ15N) increased dramatically in the sediments dated to the 1960s. They ascribed this increase to eutrophication caused by urbanization in the catchment of Lake Biwa. In accord with their finding, the flux of chlorophyll dramatically increased in the sediments dated to the 1960s in our study. If pigments were degraded with time at a constant rate, such
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changes in the flux would be unlikely. The concordance of temporal changes between the nitrogen isotope ratio and the flux of chlorophyll indicates that eutrophication progressed rapidly in the 1960s. It should be noted that, since the sedimentation rate in the present study is higher than that of Ogawa et al. (2001), our sampling site is more suitable for chronological analyses, with a greater time resolution over the 20th century. In parallel with the flux of chlorophyll, that of cladoceran remains increased from 1960 to 1980, suggesting that not only primary production but also secondary production increased during this period. In addition, animal remains suggest that before 1960, Difflugia and Bosmina were relatively abundant but Daphnia were minor components of the zooplankton community. In fact, Kawamura (1918) reported the appearance of Bosmina, Difflugia biwae, and D. brevicolla in Lake Biwa but did not mention the Daphniidae. Ueno (1934), who intensively studied the taxonomy of the Daphniidae in East Asia, did not report any species of the subgenus Hyalodaphnia from Lake Biwa, although he collected individuals of the Daphnia pulex group (D. biwaensis) in 1924 and 1934 at offshore sites. Negoro (1954) examined zooplankton samples collected in 1952 and commonly found Bosmina, Difflugia biwae, and D. brevicolla. Again, however, he did not mention Hyalodaphnia species, although he recorded a few individuals of Daphnia biwaensis. In the present study, we found no remains of the D. pulex group except at a depth of 1–2 cm. Thus, even if species of the D. pulex group were present before 1960 in Lake Biwa, their abundance would have been very limited. In contrast, Miura and Cai (1990) commonly found both Hyalodaphnia (D. galeata) and Bosmina (B. longirostris) in zooplankton samples collected monthly from 1965 to 1979. They indicated that Daphnia abundance increased in the 1970s. Although Hyalodaphnia had relatively low abundance in the mid-1980s (Kawabata 1989), they have been among the dominant zooplankton in recent years (Yoshida et al. 2001). In 1999, D. pulicaria, a species of the D. pulex group, appeared abundantly in Lake Biwa (Urabe et al., in preparation). Almost coinciding with the calendar year of their appearance, we found remains of the D. pulex group in sediment at a depth of 1–2 cm. Thus, the chronological records of the remains in the sediments accord well with the sporadic records of zooplankton from direct samplings in this lake. Unfortunately, we could not examine historical changes in abundance of copepods, which are one of the major components in the zooplankton community in Lake Biwa (Yoshida et al. 2001), because their remains are not well preserved in the lake sediments. However, the chronological records of cladoceran remains indicate that the zooplankton composition in Lake Biwa changed greatly in the mid-1960s. Why were Daphnia minor components of the zooplankton community before the 1960s? One may suspect that algal food was not sufficient to support their population growth, because the lake was then oligotrophic. However, the threshold food concentration sustaining body growth and reproduction of D. galeata is almost the same level as that of B. longirostris (Urabe and Watanabe 1991). In ex-
ploitative competition, although Daphnia can outcompete, or coexist with, Bosmina, the latter can never exclude the former (Kerfoot and Pastorok 1978; DeMott and Kerfoot 1982; Goulden et al. 1982; Urabe 1990). Furthermore, since Daphnia can store more energy reserves, they can resist starvation longer than Bosmina can (Threlkeld 1976; Goulden et al. 1982). Thus, the low abundance of Daphnia before the 1960s cannot be explained by food shortage. Leptodora kindtii and cyclopoid copepods are known to prey on cladocerans and sometimes occurred abundantly in Lake Biwa (Yoshida et al. 2001). We do not have quantitative data of these invertebrate predators in the past. However, again, low abundance of Daphnia before the 1960s cannot be attributable to predation by L. kindtii and cyclopoid copepods because they preferentially prey on small zooplankton such as Bosmina (Brandl and Fernando 1975; Branstrator and Lehman 1991), which were more abundant than Daphnia before the 1960s. Leavitt et al. (1993) demonstrated that in several lakes in North America, Daphnia remains increased relative to Bosmina remains when the abundance of planktivorous fish declined. It is well known that most planktivorous fish prey selectively on Daphnia species because of their large body size (e.g., Brooks and Dodson 1965; Gliwicz and Pijanowska 1989). Planktivorous fish inhabiting the offshore areas in Lake Biwa, such as hon-moroko (Gnathopogon caerulescens), ayu (Plecoglossus altivelis altivelis), and isaza (Chaenogobius isaza), also preferentially prey on Daphnia but not on Bosmina (Sunaga 1964; Nakanishi and Nagoshi 1984; Urabe and Maruyama 1986; Kawabata et al. 2002). Thus, before the eutrophication occurred, the rate of loss of Daphnia due to predation by fish might have been high relative to their reproduction rate. This explanation can be also be applied to the reason why Daphnia increased after the 1960s. According to Yuma et al. (1998), the annual fishery catch of planktivorous fish in Lake Biwa did not change greatly before and after the 1960s, although some planktivorous fish such as isaza have decreased in recent years. Thus, the strength of predation pressure on Daphnia by fish would not have changed greatly during the period of eutrophication. The increase in primary production due to eutrophication, however, should increase the algal food supply to herbivore zooplankton to some extent. Thus, the increase in Daphnia abundance after the 1960s seems to reflect an increase in their reproduction rate. Alternatively, the quality of algae as food for herbivorous zooplankton might have been low before the 1960s. In Lake Biwa, algal growth is limited mainly by phosphorus supply in the previous few years (e.g., Urabe et al. 1999). Thus, nutrient limitation should have been more severe when this lake was oligotrophic. Under low nutrient conditions, the nutrient content of algae relative to carbon is generally lower (Healey and Hendzel 1979; Urabe et al. 2002). Recent studies have shown that the relative phosphorus content in algal food affects the growth rate of Daphnia (Urabe et al. 1997), but less so that of Bosmina (Schulz and Sterner 1999). Therefore, Bosmina but not Daphnia could maintain their population before the 1960s on a low-foodquality diet. This argument implies that the increase in
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Daphnia abundance after the 1960s was mainly due to changes in food conditions rather than to changes in their loss rate. Eutrophication in Lake Biwa, however, disadvantaged rhizopod species. According to Ichise et al. (1996), Difflugia biwae, an endemic species in Lake Biwa, has not been seen since 1987. Our results showed that it decreased in the early 1960s and was not found after 1980. Thus, D. biwae seems to be extinct in Lake Biwa, as suggested by Ichise et al. (1996). D. brevicolla also decreased dramatically in the early 1960s and has become rare in recent years. These rhizopod species live at the lake bottom (Negoro 1954), though they have appeared as plankton in some seasons (Negoro 1954; Fenchel 1987). In the 1960s, the yearly minimum oxygen concentration at the lake bottom decreased from 6 to 3 mg l⫺1 at an offshore site (Ishikawa et al., in preparation), probably because of an increase in the sinking flux of organic matter due to increased primary production. Thus, eutrophication may have interfered with their life histories by altering environmental conditions at the lake bottom. In conclusion, our results clearly show that the zooplankton community composition in Lake Biwa changed in the mid-1960s, when eutrophication was greatest. The prominent changes in the zooplankton community after the 1960s were an increase in Daphnia abundance and a decrease in rhizopod abundance. An increase in Daphnia abundance suggests that algal food supply for zooplankton increased relative to predation pressure by fish after the mid-1960s. This implies that in Lake Biwa, the increase in primary production due to eutrophication promoted secondary production but not production of planktivorous fish. Acknowledgments We are grateful to C. Yoshimizu, M. Kagami, S. Ishida, and J. Togari for their help with laboratory and field sampling. We particularly appreciate the invaluable suggestions made by T. Ishikawa and W. Makino. Thanks are also due to T. Koitabashi and T. Miyano for shipboard assistance. This work was supported by a Grant-in-Aid for Scientific Research B (No. 12440218) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan.
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