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Nordic Society Oikos Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark Author(s): Ismo J. Holopainen and Pétur M. Jónasson Source: Oikos, Vol. 41, Fasc. 1 (Aug., 1983), pp. 99-117 Published by: Wiley on behalf of Nordic Society Oikos Stable URL: http://www.jstor.org/stable/3544352 . Accessed: 04/11/2013 15:14 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. . Wiley and Nordic Society Oikos are collaborating with JSTOR to digitize, preserve and extend access to Oikos. http://www.jstor.org This content downloaded from 150.108.161.71 on Mon, 4 Nov 2013 15:14:13 PM All use subject to JSTOR Terms and Conditions

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Page 1: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

Nordic Society Oikos

Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal ofLake Esrom, DenmarkAuthor(s): Ismo J. Holopainen and Pétur M. JónassonSource: Oikos, Vol. 41, Fasc. 1 (Aug., 1983), pp. 99-117Published by: Wiley on behalf of Nordic Society OikosStable URL: http://www.jstor.org/stable/3544352 .

Accessed: 04/11/2013 15:14

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp

.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].

.

Wiley and Nordic Society Oikos are collaborating with JSTOR to digitize, preserve and extend access to Oikos.

http://www.jstor.org

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Page 2: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

OIKOS 41: 99-117. Copenhagen 1983

Long-term population dynamics and production of Pisidium (Bivalvia) in the profundal of Lake Esrom, Denmark

Ismo J. Holopainen and Petur M. J6nasson

Holopainen, I. J. and J6nasson, P. M. 1983. Long-term population dynamics and production of Pisidium (Bivalvia) in the profundal of Lake Esrom, Denmark. - Oikos 41: 99-117.

During the 21 years (1953-1973, 1976-1977) of routine quantitative sampling re- ported in this paper, three species of Pisidium (P. casertanum, P. subtruncatum and P. henslowanum) have been present in the profundal of the eutrophic Lake Esrom, Denmark. From 1955 to 1962 P. casertanum was numerically dominant (peak den- sity of 3273 ind m2 was attained in 1957), at other times P. subtruncatum dominated (peak 3025 ind m2 in 1955). Since 1957-1958 the densities of both species have been below 1000 ind ml. The peak density of P. henslowanum (370 ind m2) was attained in 1957. All the species laid their eggs in spring (April-May), but the young were not released until the following winter, the exact time depending on the temperature and oxygen conditions. Only some of the eggs laid developed into young, and the size of the brood was dependent on parental size. The young reached maturity at the age of 2 yr, and a maximum life-span of 4-5 yr is suggested. The regularly occurring oxygen deficiency in the hypolimnion in summer caused heavy mortality in the dominant species and halted growth of individuals. Both the standing crop and annual production were lower in the population of P. subtrun- catum, which is a smaller species. The annual P/B-ratios were ca. 1 in both the dominant populations.

L J. Holopainen, Dept of Biology, Univ. of Joensuu, P.O. Box 111, SF-80101 Joen- suu 10, Finland. P. M. J6nasson, Freshwater Biological Lab., Helsing0rsgade 51, DK-3400 Hiller0d, Denmark.

B Teaeme 21 rca (1953-1973, 1976-1977) ripoerme cTaFIapTHb1X KOY4'recT- BeHHEZX yqeToB, UpHBegeHHUX B gaHHOR CTaThe. 3 BKAa Pisidium (P. casertanum, P. subtruncatum, P. henslowanum) BCTpeqaJIHcb B nrpOclyfganI eBTpoHoro 03epa 3cpcM Qa1 ). C 1955 r. no 1962 r. P. casertanum aVCHHHpoBaJ no zlcneH- HOCTH (maxcmari4HaSI rIJIOTHOCT - 3273 3Kc./M2, xCOCTaFHYTa B 1957 r.), B XPY)- rnie riepiH~ox gcwHHpOBYI P. subtruncatum (maKCMrmHaH rmnoTHOCTm 3025 gKc./ M2 B 1955 r.) . C 1957-58 rr mcJIeHHoCTb o60MX BK9OB cHHmiacb HHme 1000 31C. /M2 . MaKCeMsa1ZmHaf X1HCJeHHOCTb P. hens lowanum (370 3KC . /M2) 0ocTH1'rHyTa B 1957 r. Bce BKW oTina~tmam Rtka BecHoal (anperlb-Mak), HO MOnQrjje oCO6H He BbixXHIH 3= 0 cjieoMek 3Hv; TOximie CpOKH 3BZB4CHT OT TemnepaTypu H cQ1e3p- lKaHWff KHICnOpga. JIH 14 H3 HeKOTOpbiX OTJncDKeHEz1 5I= BblXQET Nfl9b. Pa3Mpbi nOTCMCTBa 3cBHCHIT OT pa3MepOB pQrITeJIef. MM0Pqb 3OC0reT 3pJ1CTH B B03- pacTe 2-x neT, a MaKCHMWahHafI Inpo3QmTeiHOCTh )3HH yCTaHOBJIeHag 3o 4-5 neT. PeIryYnapHO Ha6nmae~bg HeroCTaTOK KHCJIOPQ3a B rHTMHHOHe JIeTcm Bblmb- BaeT CWMThHYO CMePTHOCTh AQM4HaH14HOFO BHI3a H rleperbMU B rncecce pOcTa OT- AelHbEX oco6ek. Ypcwaan Ha KOpHK) a roBpaS llpOqyKI4H 6vIu HHDKe y P. subtrun- catum, 6anee wruKoro BHa. OTHcneHae P/B 3a rIg COCTaBJWIO rpHvepHO 1 y nO- YIltJIH O6oHX AIHCM1HpyK~X BIWOB.

Accepted 17 August 1982 ? OIKOS

7* OIKOS 41:1 (1983) 99

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Page 3: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

1. Introduction

Lake Esrom in northern Zealand, Denmark, has a very long tradition of limnological study (Jonasson 1977). It is best known for research on the zoobenthos and the relationships of these organisms with major limnological variables (Berg 1938, Jonasson 1972, 1977, 1978, 1983, J6nasson et al. 1974). The benthic macrofauna at depths below 10 m has a low species diversity and con- sists of species tolerant of low oxygen tensions. Among these are three regularly occurring species of Pisidium: P. casertanum (Poli), P. subtruncatum Malm and P. henslowanum (Sheppard).

The aim of this study is to follow variation in both density and biomass of these species from 1953 up to 1977; to analyze their population dynamics and calcu- late their production. Laboratory studies on growth, re- production and life cycles were carried out coincidently (Holopainen 1980).

The ecology of Pisidium has been recently studied by Alimov (1970, 1981), Meier-Brook (1970, 1977), Johnson and Brinkhurst (1971), Feldmann (1971), J6nasson (1972), Hinz (1975, 1976), Mason (1977), Walter and Kuiper (1978), Holopainen (1979), Holopainen and Hanski (1979), Mackie (1979), Heit- kamp (1980), Vincent et al. (1981), and yet the ecology of Pisidium is still imperfectly known.

Lake Esrom is 22 m deep, temperate and with all the main characters of a eutrophic lake. It is situated in a moraine landscape in northern Zealand, Denmark (560N, 12'E). The lake is 8-9 km long and 2-3 km wide (Fig. 1) with a surface area of 17.3 km2, maximum depth 22 m and mean depth 12.3 m. The bottom at 10-22 m depth (61.3% of total area) is covered with a thick mud layer of high organic content. The drainage area of Lake Esrom, including the lake area is only 76 km2 at the outlet. The lake volume is 213 x 106 m3

(Berg 1938). The area surrounding the lake is calcare- ous moraine with marlpits in the farmland areas on the eastern side of the lake. There are sandy beaches at the north and south ends, and stony beaches are found all around the open lake. These, with the humic ditches in the forest on the western side provide a varied environ- ment. The water supply to the lake is from many small brooks and ditches, of which Fonstrup Balk is the biggest. Sewage inlets occurred earlier, but are now partly diverted to the Sound. Treated and untreated sewage from approximately 3000 people still flow into the lake. An inflow of groundwater is likely. These en- vironmental variables produce a eutrophic calcareous lake of high stability (Berg 1938, J6nasson 1972, J6nasson et al. 1974). Ice cover lasts often for two or three months (J6nasson 1972: Tab. 1). In the period 1954-1963 maximum surface temperature in summer ranged from 18 to 220C. During the same time the temperature at 20 m depth ranged from 8 to 100C, but immediately after the autumn overturn the temperature ranged from 12 to 16'C (J6nasson 1972: Fig 3, 4, 25,

I , . ,1 /

5 5 Slotspark

8 Kongens B0ge 9 Kobceks Vig 10 Tumtingehus

20 11 Skoviund

10~~~~~I \A / N

Fig. 1. Map of Lake Esrom with the 20 m depth curve (broken line), the permanent sampling stations (black dots) as well as the extra stations used in construction of Fig. 3 (circles).

26, 27). Anaerobic conditions developed in the deepest parts of the lake during the later summer stratification period (J6nasson 1972: Figs 5, 29, 30). Mean annual gross phytoplankton production during 1956-1965 averaged 260 g C m2 yr' (Jonasson 1972: Figs 9 to 22), but was reduced to 240 g C m2 yr'1 over the period 1965-1972 (Jonasson et al. 1974: Tab. 5).

2. Material and methods The material analyzed was obtained mainly by J6nasson from the extensive quantitative bottom sampling be- tween the years 1953 and 1973. It consisted of 95 sam- ples taken at more or less regular intervals (Fig. 1) from the Endrup station in the middle of the lake; sampling from the five other profundal stations was of somewhat shorter duration (1953-1963) (Fig. 4). On each occasion, 10 (1953-1957) or 5 (1957-1973) hauls were taken with a 42 cm high Ekman-Birge type grab having a sampling area of 250 cm2. In April-May 1955 an ad-

100 OIKOS 41:1 (1983)

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Page 4: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

ditional set of five-haul samples were taken from 26 stations evenly distributed in the profundal (> 15 m).

Each haul was sieved separately, usually through a 0.20 mm mesh sieve (range 0.15-0.50 mesh), which is considered to be 100% efficient for the Pisidium species present (J6nasson 1955, Holopainen 1979). From September 1976 to August 1977 the Endrup station was sampled at monthly intervals (10 hauls each time) during the open water period; the lake being ice- covered from 19 January to 7 March 1977. These sam- ples were taken with the same grab as above using a sieve with 0.5 mm mesh. The parallel use of a Kajak- type corer with a 55 cm2 tube (for the efficiency see Holopainen and Sarvala 1975) gave similar results to those from the grab (the differences were not statisti- cally significant) and so the larger grab was used routinely.

The sorting of the 1953-1973 material was done by the same person (for details see Jonasson 1955). The material from 1976-1977 was sorted under a stereomicroscope using x 10 magnification which prob- ably gave 100% efficiency since the residue from siev- ing was small.

The material was identified, counted, and the shell lengths of ca. 100 specimens per species per sample were measured by use of ocular micrometer with a pre- cision of 0.03 mm to give a length-frequency distribu- tion. The measured individuals were dissected (after killing in hot water in case of fresh material) and the contained embryos counted and measured.

Since the distribution of both abundant Pisidium species was clumped a log x transformation was used in the calculation of the 95% confidence limits for the numbers (Elliott 1977).

An extra sample of fresh material, taken in May-June 1977, was used to construct the weight-length regres- sions. The shell length was measured, the opened indi- vidual was dried in a preignited and tared aluminium foil cup at 60'C for 24 h, weighed on a Cahn 4600 electrobalance, ignited at 500'C for 12 h and weighed again.

These weight-length regressions, which give the ash- free dry weights (AFDW), were used in all biomass calculations, along with the sample specific length-fre- quency (0.1 mm class intervals) and density values. The production was calculated by the Hynes-Hamilton method (Hynes and Coleman 1968, Hamilton 1969) by using real weights instead of volumes; comparative data show that this method gives reasonably good accuracy and agreement with other methods (Holopainen 1979: Tab. 8).

3. Results and discussion

3.1. Spatial and temporal variation in numbers

3.1.1. Spatial variation The distribution of P. casertanum and P. subtruncatum

W! E

82565 N ~~~~~820fI36 . 8, - -a-

126! 1397 142 137 **i215 3' :24 ,' 153

1162 93.9 " 164

S. 107 */126

~126 / 7.583""- 68" 12 811 97 -

N

Fig. 2. Map of Lake Esrom with the 20 m depth curve (broken line), divisions used to test spatial variation (dotted lines) and the mean densities per 250 cm2 in one sampling (April-May 1955; the figures in the map). N, northern-; M, middle-; S, southern-; E, eastern- and W, western part.

in small areas or between different hauls in one sample, was clearly clumped. This seems to be the usual case in Pisidium especially in profundal areas (Ravera 1966, Ruggiu and Sarageni 1972, Holopainen 1979) and one reason for this could be their very stationary life com- bined with release of the young in the immediate vic- inity of the parent.

The variation in mean density in a larger area around one sampling station was not studied in this lake, but it can be considerable (e.g. Holopainen 1979).

The variation of Pisidium density in the whole regular deep basin of this lake can be seen in Fig. 2. The overall

OIKOS 41:1 (1983) 101

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Page 5: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

Tab. 1. F-statistics for the between samples/between hauls variances in the spatial variation test (analysis of variance; square root transformation). The asterics indicate those areas where the differences between samples (= stations) are statis- tically significant.

Part of lake F

southern part .............................. 1.97 middle part ............................... 1.59 northern part .............................. 8.14*** eastern part ............................... 1.90 western part .............................. 3.09** >20 m .................................. 2.69** 18-20 m ................................. 3.96*** southern + middle part ........ ............ 2.89*** middle + northern part ........ ............ 3.24*** whole lake ................................ 3.39***

mean density based on the means of five-haul samples from 26 stations was 4731 ind m2 (2592-6776). The densities were higher in the deeper part (more than 20 m), on the east side of the lake and in the central part. The densities of P. casertanum were lower than those of P. subtruncatum in the southern part, but the variation within one station was again very high (Fig. 3). The lake was divided into areas (Fig. 2) and the variation in total Pisidium numbers was analyzed by comparing the var- iance between the sampling stations (samples) in each area and that within samples or between different hauls (analysis of variance, square root transformation). In the southern, middle and eastern areas the samples did not differ significantly from each other (Tab. 1) suggesting some degree of homogeneity within those areas. However, there are clear differences in the rela- tive numbers of the species along the south-north axis in the eastern part of the lake (Fig. 3).

Fig. 3. Mean numbers of the 6 -* P.casertanum three Pisidium species in 3 I one sampling (April-May x1O 0 Psubtruncatum 1955) along the south-north 5- 0 P. henslowanum axis of Lake Esrom (for the stations see Fig. 1). White: P. subtruncatum, shaded: P. 4- henslowanum, black: P. casertanum. The vertical C 4 lines show the 95% 3 ?l confidence limits. E

2-

E zi

1 2 3 4 5 6 7 8 11 12 Stat ions

6-

xtl3 R)K?^' -t Skoviund

b\o Kobaeks Vig

4 0 , 6 6'-~~~~~~~~~~1,

2 0 0- 0 0

0-0. \p.'_-_0-. '6 -o -0-----

o I 6-

x103 - 0 - Endrup

0 0-' -- Stotspark

E~~~~~~ ,b / 'o/0' 11 o??/ 6 0 6 ~ ~~~~ -o _O

~~ 2 0 0~~~~~~ 0-

E 0 'X - 6??- D D?b

-2 --0 4 ( 0 ~~~~~~~~~~~~"0

0* I I ~~1551958 11961 Years

Fig. 4. Summed densities of Pisidium species in two northern permanent stations (upper part of the figure, continuous line: Skovlund, broken line: Kobaeks Vig) and in two more southern stations (lower part, continuous line: Endrup, broken line: Slotspark).

102 OIKOS 41:1 (1983)

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Page 6: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

x103

3

P.casertanum - l-P. subtruncatum

.Pelie. henslowanum

2-

E

A~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~A

a) I~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~

I I I I ~ ~ I I %A

1955 1960 1965 1970 1975 Years

Fig. 5. Long-term temporal variation in densities of three Pisidium species in the Endrup station. Continuous line: P. casertanum, broken line: P. subtruncatum, shaded: P. henslowanum.

3.1.2. Temporal variation According to Berg (1938) three species of the genus Pisidium reach a depth of 20 m (P. casertanum, P. henslowanum and P. lilljeborgi) and another two a depth of 14 m (P. subtruncatum, P. hibernicum). The average densities found by him in the years 1932-1933, were very low (100-600 ind m2). These remarkably low densities may be partly explained by the different method used. Berg (1938) used a short Ekman grab, a sieve with 0.67 mm mesh, and, in addition, there were differences in the sorting efficiency.

In any case, the densities of Pisidium in late 1953, twenty years later, were ten times higher and increasing steeply in the profundal of the whole lake (Figs 4-7). Peak numbers were found in 1955-1956 (4000-6000 ind m2), but they had declined sharply by 1957 (south- ern part of the lake) and 1958 (northern part). In mid- lake (Endrup station) P. subtruncatum reached its peak densities in 1955, and P. casertanum in 1957. After their peak both declined until 1963, when P. subtrun- catum seemed to recover and again became dominant until 1977, at least. P. henslowanum has been present since 1953, but in very small numbers from 1962.

The details of seasonal variation are dealt with below in the section on population dynamics.

3.2. Population dynamics

3.2. 1. Reproduction The reproductive system of Pisidium is specialized; the animals are monoecious, ovoviviparous and possess at least the potentiality for autogamy (Odhner 1929, 1951, Heard 1965, Meier-Brook 1970, 1977, Mackie 1978). Fertilization takes place in the spermoviduct, and the eggs pass to the inner demibranches, penetrate into the filaments and are overgrown by the gill tissues (Odhner 1929, Meier-Brook 1970). The brood sac or marsupium thus formed is the place where embryonic growth occurs until the sac ruptures and the big em- bryos lie free in the interlamellar chamber. According to Meier-Brook (1970) the embryos are free in the chamber when they are ca. 0.7 mm to 0.9-1.1 mm long, which are the lengths at birth in most European species. A feature typical of sphaeriids is that the number of eggs laid is much higher than the number of embryos which attain birth size (Meier-Brook 1970, 1977, Mac- kie et al. 1976, Holopainen 1979): about half of the embryos stop growing at a length of about 0.2 mm (Pisidium) and die.

3.2.2. Seasonal cycle of reproduction In these profundal populations of Pisidium a new batch

OIKOS 41:1 (1983) 103

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Page 7: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

6838 5494 Fig. 6. Densities of P. 4- casertanum from 1953 to 103 1P c1sertanum 1977 (arithmetic mean) with

the 95% confidence limits (logarithmic transformation).

3-

2-

Lfl

E :0

z

1953 1956 1959

o A A I

1961 1964 1967

0- 1 1969 1972 1976

Years

of eggs is produced once a year in spring, and the young are born during winter. All observations on eggs con- tained in the filaments of the inner demibranches before the formation of brood sac relate to the period 16 April - 17 May (there are observations for 9 yr on P. caser- tanum, 8 years on P. subtruncatum and one on P. henslowanum: 17 May 1966).

The marsupia are formed in spring and early summer, but the development of embryos, as well as the growth of the parents, ceases from about late June onwards, because of the steeply decreasing amount of oxygen and subsequent anaerobic conditions, which prevail during the rest of the summer stagnation period (J6nasson 1972: Fig. 30). After the autumn overturn the bottom layers become reoxygenated and the prevailing high temperatures provide good conditions for growth.

The embryos of P. casertanum reach birth size ca. 2-2.5 months after overturn. In 1954 the autumn overturn took place 15-22 September, and the sub-

sequent parturition was at the end of November when the profundal bottom temperature was approximately 70C (J6nasson 1972). The year after the onset of overturn was 25 October and again two months later the embryos were of birth size, but probably remained inside the parents until next spring (Figs 6, 8). This might be due to the low and decreasing temperature in midwinter (from 2.80C on 20 December to 1.90C on 10 January and to 3.00C by 13 April 1956). Unfortunately there are no samples available for the 3-4 months be- tween the beginning of January and the end of April, i.e. ice-covered periods of the lake. The rising temper- atures in April-May trigger the parturition if it has not taken place previously. The results for winter 1956- 1957 show a main period of parturition at the end of October, because autumn overturn was as early as 5 September. But gravid individuals with big embryos were also found in March and April, 1957. The same was true in spring 1955 (Fig. 8). This may indicate a

104 OIKOS 41:1 (1983)

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Page 8: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

Fig. 7. Densities of P. 4 subtruncatum from 1953 to x103 1977 with the 95% confidence limits. PuInl I I I ~~~~P. subtruncctum

3

4280

2-

E W0 no

1953 1956 1959 E

= 2 -Q4Y

1961 1964 1967

1969 1972 1976 Years

second reproduction or, more probable, some of the parents laid their eggs so late, perhaps in the autumn instead of spring, that the embryos could not complete their development before the next spring. In any case, a second peak in numbers can be seen in spring 1957 (Fig. 6).

Growth of embryos is regulated by temperature. The earlier the autumn overturn occurs, the higher the temperature. In 1954 the overturn occurred 15-22 September at a temperature of 15'C, in 1955 25 October at a temperature of 12'C, in 1956 5 September at a temperature of 15.50C. The differences in growth

and development time of embryos are clearly partly re- lated to the timing of autumn overturn and partly to bottom temperature. This is shown in Fig. 13, which clearly demonstrated the influence of shortage of oxygen in the bottom layers on the growth of Pisidium as well as the influence of temperature, which is here indicated by the presence or absence of ice-cover. In addition, the ice-cover influences primary production and its distribution from surface to bottom.

In P. subtruncatum the development of embryos is similarly governed by environmental factors but they seem to be liberated from the parents throughout the

OIKOS 41:1 (1983) 105

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Page 9: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

N~~~~~~~~~ 54~~~~~~~~~5

F~~~~~~~~~~~~~~~~~~

~~~~20 0~~~~~~~ C~~~~~~~~~~

a, NP cusertanu m

To~~~~~~~~~~~~~~~~~5

~ 0 1 2 4 0 2A3m

5495

30-

u 20- D

l /o- Pca sertauncum

0 1 2 34 0 1 2 34

Shell length mm

Fig. 8. Example of length-frequency distributions of P. casertanum. The shaded areas represent embryos (inside parents) and the circles indicate the presence of marsupia with small embryos (not measured).

L~~~~~~~~~ N ~ ~ ~ ~ ~ ~ 0~~~~~~~~~~~~~~~~~~

0 1 2 3 0 1 2 3~0 Shl Aeghm

Fig. 9.Eapeo eghfeunydsrbtoso .sbrnau.Frepaain e i.8

whole winter (Fig. 9). The material for P. henslowanum is small but suggests a pattern similar to that of P. sub- truncatum. (Some citations of this work given earlier by Holopainen (1979) concerning the reproduction of Pisidium were unfortunately based on preliminary in- terpretations.)

In Lake Paajarvi, southern Finland, the reproduction of P. henslowanum seems to be non-synchronous in

deeper water (13 m) but no seasonal oxygen deficiency occurs. In the littoral of the same lake P. casertanum gave birth to young synchronously once a year, in the middle of July and the subsequent egg laying did not take place before next spring, ca. 3 months before next parturition (Holopainen 1979). The scattered data on profundal populations of P. casertanum all suggest a similar system to that in Lake Esrom (Thut 1969,

106 OIKOS 41:1 (1983)

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Page 10: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

Fig. 10. Example of length-frequency distributions of P. henslowanum. For 5 explanations see Fig. 8. 9 M

SM

30-

>20-

4 1L

C 95 M

9

Shell length mm

Holopainen 1979), and the pattern is highly dependent on the environment.

3.2.3. Litter size The maximum number of large embryos found in one parent were 20, 12 and 23, mean numbers 5.9, 3.7 and 5.8 in P. casertanum, P. subtruncatum and P. henslowanum, respectively. The number was dependent

on parent length, as was the number of eggs laid or at least those attached to the gill (Fig. 11). On average only ca. 33% of the eggs completed their development to birth size in P. casertanum and the results on P. sub- truncatum also suggest suppression. In the littoral of the oligotrophic Lake Paujarvi the maximum litter sizes were 27 and 28, and mean litter sizes 5.3 and 9.9 for P. casertanum and P. henslowanum, respectively, but the

Fig. 11. Numbers of eggs and embryos per parent. A, P. casertanum: the

40 P.ccas ehrtanum GM-regression (Ricker o0/1 lP.subtruncatum P henslowanum 1973) equation for eggs

I ~~~~~~~~~~~~~(circles) 20- / y = 0.331 x3179 (n = 16, r 0

~ ~ ~ ~/= 0.596) and for embryos (A %o~o j 0 (dots): o do* " vy = 0.015 x5306 (n = 67, r

> 10 gD,6Sl ?l .hw = 0.799). B, P. D / 00> o fi * " subtruncatum;

E

/ ,_ E *0 y = 0.086 x50" (n = 55, r

soO _ = 0.827). C, P. 5 0- 7 henslowanum;

m _ / _ y = 0.170 x3383 (n = 27, r

rs * * / / /,, = 0.879). y = number of o I /,l embryos of size 0.5-0.8 mm. O ,8 I _ / x is parent shell length

' *l O /,' (mm), n = number of E '| /

I observations (parents) and r :3 = I I =correlation coefficient. Z 1 b I . The broken lines refer to

I * I | t - g | rthe corresponding regression 1 2 3 4 1 2 3 4 1 2 3 4 lines for the same species in

Lake Paajarvi (Holopainen Parent shell length mm 1979).

OIKOS 41:1 (1983) 107

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Page 11: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

dependence on parent size was similar in both lakes (Fig. 11). Ladle and Baron (1969) give a mean litter size of 13 (range 3-25) for P. subtruncatum and also report a significant correlation between the number of embryos and parent length. The maximum length reached in this river population (ca. 4.4 mm) was much higher than in profundal of Lake Esrom (3.3 mm). Ac- cording to Meier-Brook (1977) ca. 50% of the embryos in littoral species but 62% in a profundal species (P. conventus) reach birth size. The results of Holopainen (1979) are in total agreement with this in the case of P. conventus and also suggest a suppression of ca. 50% in P. casertanum. If the latter is true, the number of eggs laid per parent could be equal in both P. casertanum populations considered (Lakes Panjarvi and Esrom), but the number reaching birth size is governed by the environment.

3.2.4. Life span and number of litters As stated earlier, both P. casertanum and P. subtrun- catum most probably produce their first clutch at the age of 2 yr. After that they reproduce once a year, and if they reach an age of 4-5 yr, the total number of clutches per parent is 3-4. The mean sizes of successive annual clutches in P. casertanum are estimated to be 2, 5, 11 and 20, or a total of 38 young. In Lake Panjarvi the cumulative figure for the maximal three reproductions is 30 in the same species (Holopainen 1979).

In the lakes of middle and northern Europe Pisidium is reported to live maximum 2-4 yr (Meier-Brook 1970,

Holopainen 1979), but life-spans of one year or shorter are given for various species by Ladle and Baron (1979), Danneel and Hinz (1976), Bass (1979) and Heitkamp (1980).

From North America life-spans of one year or shorter are usually reported (Heard 1965, Burky and Burky 1976, Hamill et al. 1979, Mackie 1979), with the ex- ception of a 2.5 yr life-span for P. casertanum (Burky et al. 1981) and 3 yr for P. amnicum (Vincent et al. 1981).

For P. casertanum only iteroparous populations with a life-span of 3-4 yr have been reported from Europe (Odhner 1929, Holopainen 1979), whereas from North America only semelparous populations with variable life-span (0.5-2.5 yr) have been found in this species (Thut 1969, Mackie 1979, Burky et al. 1981). The number of populations analysed, however, is too small to allow further discussion.

3.2.5. Growth Embryonic growth inside the parent is delayed by the severity of the seasonal environment: after the egg- laying period in spring the growth of embryos is soon slowed down by oxygen deficiency during summer stratification (approximately June-October). This causes the time of embryonic growth from egg to a shell length of ca. 1 mm to be ca. 6 months in P. casertanum - this is twice the time needed under more favourable conditions (Meier-Brook 1970, Holopainen 1979).

The growth after birth was analyzed from length-fre- quency distributions of successive samples (Figs 8, 9)

1. 0 P.Rcasertanum -u

/0 o0~~Q 0 -

,,0o 0,,-" 0 O - 0

< ~ ~ ~ / / - , .0-- 0

cs~~ ~ ~~~~~ - 3o O i.1.Th rwhi

~~~0~~~~~0~ 0~~~

.u 0

/0~~~ C u--u~~0O --

0 0~~~~~~~ 0 0 Fig. 12. The growth in

E -0 weight of successive cohorts S '00. of P. casertanum (circles). o The black squares represent 0 o) 0 the minimum growth

/ -0o o according to the ice /t experimental results of

ice Holopainen (1980). The * Birth arrows on the abscissa J4 4 ^,indicate three main birth

0.01- J Al w J dol II} V AT I S J4 O"V IJW AV IJI IS l 14 I- I I JR 1 I periods and the horizontal Jl9 A54

J '' O ' lJ''A~ ' J O '' t~ '''1956 ~ ''' o '' I J''' A ~ 'J''' O '' broken lines the m inim um 1954 1956 mature and maximum

Years weights.

108 OIKOS 41:1 (1983)

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Page 12: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

12-

10 - v Bottom W 0 _ \ = temperature

a- E

8-

Bottom oxygen

0.5 V1ice1

/Ii no ice a

St rat if icat ion a

Overturn 7 Growth of 0.1 - 0o PRcasertanum

U-

Z Birth

0.01 i A ' O N DI'F'J M'A M J J A' S' O' N' D J F M A M J J A S O N D J F'M A M

1955 1956 1957 Years

Fig. 13. The growth in weight of the 1954 cohort of P. casertanum in relation to bottom temperature and oxygen content. The arrows on the abscissa indicate the three main birth periods.

and the mean lengths of the component groups (consid- ered here as cohorts) were extracted by the graphical method of Cassie (1954), the respective weights calcu- lated and plotted against time, and the points connected subjectively (Figs 12, 13). The annual dynamics of growth is again clearly seen in the figure: the growth stops during the cold winter months as well as during the oxygen-poor summer stagnation period. The number of large individuals is not high enough to give reliable results. The growth of P. casertanum and P. subtruncatum from the profundal of Lake Esrom was studied experimentally by Holopainen (1980), and his data gave clearly faster weight gain for P. casertanum (Fig. 12) even if the annual dynamics was comparable to that in nature.

3.2.6. Mortality and annual changes in numbers The densities of P. casertanum and P. subtruncatum show very wide annual fluctuations as can be seen in Fig. 14. The years of maximum density (1955-57) give

a clear demonstration of the annual pattern: the den- sities increase until all young are born in late spring, reach peak numbers in summer but decline sharply during the three months of summer stratification before the autumn overturn. The minimum numbers are found shortly after the overturn and is soon followed by the production of new young and rising densities. In a period of one year numbers may increase threefold in P. casertanum and P. subtruncatum but the change is less in P. henslowanum. The high mortality in late summer and autumn is most probably due to the anaerobic con- ditions prevailing during summer stratification. The respiratory behaviour of Pisidium in Lake Esrom was described by Berg et al. (1962: Fig. 21), and they showed that Pisidium is affected by low oxygen ten- sions. From current evidence the figure probably de- scribes the respiration of a mixed population of P. casertanum and P. subtruncatum. It shows a 50% de- cline in oxygen consumption from air saturation to the upper critical point at 30% air saturation and a much

OIKOS 41:1 (1983) 109

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Page 13: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

Fig. 14. Annual fluctuations x103 0 in numbers of P. casertanum

Overturn (continuous line) and P. 3- o subtruncatum (broken line). The summer stratification

,"1 o | period and autumn overturn o 1 t\' 1l 1 \o P. casertanu m are indicated as well as the 0 P. casertcInum three main birth periods in 1954-1956 (arrows on

E / / abscissa).

?- 0A'III1I1II I " ''''''II A J I1l- J TT'?,, o J ~

0-0 '0~-0 .f0

~0/0 00 I En C I I .1 0

J# ~ ~ ~ ~ ~ ~ ~ ~ ~ p0

z 0 0 0.01 0*-

B ir th P.subt runcatum

0 'j'J'' j' I

'j'J'c ' I i'...'' O' 'jil W 'J' ' jJ ...A' 'J' 1955 1957

Years

steeper decline between 30 and 5% air saturation. This means that the respiration of these Pisidium species is rather sensitive to oxygen depletion even though they are partly able to survive the summer stratification period. The amount of mortality due to predation is difficult to estimate, but sphaeriids certainly are a food source for fish and the predation pressure may be an important limiting factor in some lakes (e.g. Walter and Kuiper 1978). In Lake Esrom Anguilla anguilla (L.), Abramis brama (L.) and Acerina cernua (L.) are the main predators. The profundal areas are avoided by the predators during summer stratification period due to lack of oxygen.

3.3. Biomass and production

The seasonal and year-to-year variation in standing crop values (Fig. 15) naturally follow the main features of density variation, consequently the peak biomass in P. casertanum was reached in June 1956 (611 mg AFDW m2) and that of P. subtruncatum in May 1955 (180 mg AFDW m2; for annual means see Tab. 2). There are, of course, some seasonal differences in the form of the density and biomass curves caused by the varying proportion of young in the population - e.g. in P. casertanum the variation in the mean weight of free- living individuals in the population (biomass/density) was 80-240 [ig (x = 175 jig, n = 53 sampling dates) in 1954-1962. P. subtruncatum is a smaller species with variation from 29 to 131 jig (x = 71, n = 53) in mean individual weight during the same time interval. The corresponding figures for P. henslowanum were 90-130 jig (x = 116 jig, n = 9) in 1954-1955 (for the weight- length regression equation see Tab. 3 and Holopainen 1979). The annual production was calculated by the

Hynes method in the form described by Hamilton (1969). The real AFDW values were used instead of volumes and the production figures were divided by the maximum life span (assumed to be 4 yr for both species) to get annual production. The use of maximum life-span in years as a divisor in this method in the case of species which live several years (Hamilton 1969) has been shown to give comparable results with other methods (for Pisidium, at least, Holopainen 1979). The produc- tion values for the years of peak density were high (Tab. 2) as a result of the large numbers.

The turnover or P/B-ratio was also comparably high considering the shortness of the annual growing season and the presence of generalist species only. The P/B- ratios under profundal conditions given previously by Johnson and Brinkhurst (1971) and Holopainen (1979) fall between 1-1.5 and are not much higher than those given here (Tab. 4). If the maximum life-span of Pisidium in the profundal of Lake Esrom is 5 yr instead of 4 - which is quite possible - the production figures in Tab. 2 are overestimated by 20% and the P/B-ratios would fall between 0.7-0.8. Although there is not much data available at present (Tab. 4), the majority of results suggest the turnover ratios of Pisidium to be around 1 in Northern Europe. The values given by Gillespie (1969) and Hamill et al. (1979) are much higher (4.3 and 3.8, respectively). Both their species were from running water, and in the first case the river receives water from hot springs. These two river species have a life-span of 1-2 yr or less.

3.4. The role of Pisidium sp. in the profundal macrofauna

In 1933 the share of Pisidium in the total macrofauna was ca. 5% (Berg 1938), in 1955 ca. 20%, and in 1973

110 OIKOS 41:1 (1983)

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Page 14: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

1533 787 Fig. 15. Standring crop A .^ I (biomass) of P. casertanum

l00l (A) and P. subtruncatum 600 ll(B) from the year 1953 to

Rcasertanum 1963 (thick line). The thin lines represent biomass

l l l when numbers in the upper and lower 95% confidence limits (see Figs 6 and 7) are

4, 200- <used in its calculation.

200 E

a ~ ~ ~ ~ ~ ~ ~~~~~~er

0

P. subtruncatum 200

0 1953 1956 1959 1962

Years

ca. 2%. Being small, long-living animals, they form an even smaller part of the annual mean biomass and pro- duction (Tab. 6). Yet the density of Pisidium in the profundal (ca. 1000 ind m-2) is high in these cir- cumstances (depth, low oxygen) and - in contrast to the other groups - consisted of two equally strong species (for discussion see below). The population dynamics as well as life habits of Pisidium and Potamothrix ham- moniensis have many features in common, the main

differences arising from the details of feeding and re- production (J6nasson 1972: Fig. 60, Jonasson and Thorhauge 1972, 1976a and b, Thorhauge 1975, 1976).

The long-term variation in numbers of these profun- dal detritivores are compared in Fig. 18.

The reasons for the increase in Pisidium numbers in 1953-1956 and the decline in 1957-1958 are not clear. A logical explanation would be the eutrophication pro- cess or the increase in nutrient content and decrease in

Tab. 2. Mean annual biomass and production figures for Pisidium in the profundal of Lake Esrom. The annual P/B ratio in P. henslowanum was assumed to be 1.

P. casertanum P. subtruncatum P. henslowanum SUM year B P P P/B B P P P/B B P P

mg m-2 mg m-2 kJ m-2 mg M2 mg M2 kJ m2 mg m2 kJ m-2 kJ mn2

1954 ..... 186.1 174.1 3.88 0.94 85.6 82.1 1.83 0.96 23.1 0.51 6.22 1955 ..... 261.3 243.3 5.42 0.93 128.7 117.7 2.62 0.91 19.9 0.44 8.48 1956 ..... 438.1 369.2 8.22 0.84 85.1 83.0 1.85 0.98 18.0 0.40 10.47 1957 ..... 356.0 360.7 8.03 1.01 71.6 69.9 1.56 0.98 20.6 0.46 10.05 1958 ..... 247.0 224.1 4.99 0.91 39.7 45.8 1.02 1.15 - - 6.01 1959 ..... 122.8 121.2 2.70 0.99 22.4 17.2 0.38 0.77 - - 3.08 1960 ..... 135.4 106.8 2.38 0.79 21.7 19.2 0.43 0.89 - - 2.81 1961 ..... 108.1 95.5 2.13 0.88 23.8 26.4 0.59 1.11 - - 2.72 1962 ..... 78.2 84.1 1.87 1.08 33.3 36.2 0.81 1.09 - - 2.68 1963 ..... 60.8 65.1 1.45 1.07 61.2 55.4 1.23 0.91 - - 2.68 1964 ..... 39.4 40.4 0.90 1.02 48.4 45.4 1.01 0.94 - - 1.91 1965 ..... 78.9 66.5 1.48 0.84 66.4 71.9 1.60 1.08 - - 3.08

OIKOS 41:1 (1983) 111

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Page 15: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

Tab. 3. The weight-length regression equations for Pisidium in the form w = alb, where w is AFDW in ig and 1 is length in mm. A linear, B functional (Ricker 1973) regression after ln transformation and C Marquardt's algorithm method (Conway et al. 1970). The non-linear confidence limits are given for C. The values in boxes were used in biomass calculations.

A B C

P. casertanum May 1977 (n=36) .......................... a=18.914 18.769 19.279 (18.328-20.230)

b= 3.039 3.050 3.015 ( 2.974- 3.052) July 1977 (n=39) .a=14.392 14.223 20.910 (19.655-22.166)

b= 3.286 3.301 2.942 ( 2.882- 2.993) P. subtruncatum

May 1977 (n=34) .a=20.782 20.682 22.518 (21.392-23.644) b= 3.005 3.022 2.890 ( 2.836- 2.940)

June 1977 (n=77) .a=16.956 16.774 19.824 (18.833-20.814) b= 3.326 3.365 3.098 ( 3.039- 3.153)

Tab. 4. Production (P) and annual production-biomass (P/B) ratio of Sphaeriidae.

Species P kJ m-2 yr1 P/B depth m water body and locality author

P. virginicum .342.26 0.2 Root Spring, USA Teal 1957 P. compressum .50.17 4.3 1 Madison River, USA Gillespie 1969 P. crassum .0.88 1.3 0-4 Lake Krugloe, USSR Alimov 1970 S. suecicum .61.59 1.5 0- - Sphaeriidae

(several species) 5.0-10.0 1.2-1.5 5-30 Great Lakes, Canada Johnson and Brinkhurst 1971

P. casertanum .1.4-1.8 1.4 Upton Broad, England Mason 1977 - ................... 3.93 1.3 2 Lake P55jarvi, Finland Holopainen 1979 P. conventus .1.0 1.0 25 - P. casertanum .0.4-3.7 3.8 2-8 Ottawa River, Canada Hamill et al. 1979 - ................... 0.9-8.2 0.8-1.1 20 Lake Esrom, Denmark this study P. subtruncatum 0.4-2.6 0.8-1.2 20 P. amnicum .2.4 1.4 1 St. Lawrence River, Vincent et al. 1981

Canada

Tab. 5. Some characteristics of Pisidium populations in the profundal (20 m) of Lake Esrom.

Characteristic P. casertanum P. subtruncatum P. henslowanum

max. shell length (mm) ............. .................... 4.3 3.3 4.4 minimum length of gravid individuals (mm) ...... ......... 2.4 1.7 2.1 length at birth (mm)

a) minimum free ................... .................. 0.9 0.8 0.9 b) maximum embryo ............. .................... 1.1 1.0 1.1

number of embryos per parent mean ............................................. 5.9 3.7 5.8 maximum ........................................... 20 12 23

length of pre-reproductive age (yr) ....... ................ 2 2 maximum lifetime (yr) .............. .................... 4-5 4-5 ? birth period ........................................... winter winter winter

oxygen content, which are both well documented (e.g. J6nasson et al. 1974, J6nasson 1983). Nothing drastic can, however, be seen in the nutrient load until 1961, when the town of Fredensborg began to discharge un- treated sewage through a pipeline into the southern part of the lake. Before that, the regular long-term sewage-

and manure flow from the human settlements to the southern part of the lake raised the nutrient content of the lake, because the brooks were converted into pipelines, leaving the decay of organic matter to the lake ecosystem itself. The detritivore populations were influenced first by increasing microbial production in

112 OIKOS 41:1 (1983)

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Page 16: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

Tab. 6. Bivalves as part of profundal macrofauna.

Years Average Mean annual Mean annual Annual Author no m 2 biomass g DW m-2 production P/B

(AFDW for Pisidium) Kcal mr2 yr-1

Chironomus anthracinus .... 1958-60 9000 10.16 75.3 3.8 (4.0) J6nasson 1972 Potamothrix hammoniensis . 1956-60 5500 1.22 6.0 0.8 J6nasson and Thor-

hauge 1972, 1976a, b Pisidium (3 species) ....... 1955-57 4000 0.47 2.4 1.0 This study Chaoborusflavicans ....... 1953-54 1750 1.69 14.4 1.7 J6nasson 1972 Procladius pectinatus ....... 1954-55 300 0.27 2.9 1.9 J6nasson 1972

Total ..... 20550 13.81 101.0 Pisidium % of total ........ 19.5 3.8 2.4

the sediment, thus causing the clear increase in numbers of the two subsurface feeding populations (Potamothrix hammoniensis and Pisidium spp.) which can be seen clearly in 1953 to 1956. In 1971 the untreated sewage was converted to another watershed.

Reasons for the fluctuations of Potamothrix ham- moniensis and the surface feeding Chironomus an-

thracinus have earlier been discussed by J6nasson (1972) and J6nasson and Thorhauge (1976a).

In the case of Pisidium the coincident prolongation of lack of oxygen probably caused the heavy mortality in autumn (Fig. 14) and the consequent high seasonal fluctuation in numbers, and finally a clear decrease in population sizes, first at the south end near the nutrient

100- 100-

Fig. 16. Ash content of P. C50 0

casertanum (A) and P. C: subtruncatum (B). The a,

- circles are for embryos -C - P.casertanum P.subtruncatum removed from the brood sac and the vertical broken lines

a______________________________________ ,____,____,____,____,________,_ indicate mature size. 0 1 2 3 4 5 0 1 2 3 4 Shell length mm

0~~~~~~~~

CL 0.9

88 /S o So" /, 0-- - 0.7~~~~~~~~

300- / E 0~~~~-

200- P.casertanum C *

0~~~~~~~~~~

300-

o \ -

Fig. 17. Production (dots) ?. _--* t and production/biomass LFP.subtruncatum* -~ (P/B) ratio (circles) in the - populations of P. casertanum 0- 95 a15r6196 (continuous line) and P. 95 Xrl8 subtruncatum (broken line). Yea rs

8 OIKOS 41:1 (1983) 113

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Page 17: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

Potamothrix hammoniensis 30

x103

20

10

40 - \ IUntreated Chironomus anthracinus

Sewage 'sewage Jconverted 30E

20 E

10 :Z

0 South |North Pisidium spp.

2

1

1955 1960 Years 1965 1970

Fig. 18. Long-term fluctuation in numbers of the main detritivorous profundal species in Lake Esrom.

source, and then at the north near the outlet of the lake (Fig. 4).

Generally, Pisidium species are considered to be more vulnerable to eutrophication and lack of oxygen than Tubificidae and some Chironomidae. The results of Berg et al. (1962) indicate that the critical oxygen level for P. casertanum (ca. 30% of air saturation) is higher than for Potamothrix hammoniensis (9%), the other subsurface feeder, or Chironomus anthracinus (25%), the surface feeder. The apparent capacity of profundal detritivores for anaerobic metabolism and the questions of its ecological effects are still mostly un- answered (see discussion). The respiratory adaptation of these and some other benthic animals to different oxygen levels has recently been discussed by J6nasson (1978).

In contrast to Pisidium the Tubificidae show two other peaks in 1966 and 1973 (Fig. 18) and an almost identical trend is followed by Ch. anthracinus. The var- iation between successive years in the numbers of Tubificidae has been explained with competition and perhaps predation by Ch. anthracinus (J6nasson and Thorhauge 1972, 1976a, Jonasson 1978) which does

not completely explain, however, the three peaks at 7-10 yr intervals. Unfortunately, we are not very familiar with this kind of long-term cyclic fluctuations in benthic animals, and even less so with the reasons for them.

4. General discussion

4.1. Coexistence of two species with high numbers

Both P. casertanum and P. subtruncatum are known as euryoecious generalist species capable of inhabiting a great variety of water bodies (Valle 1927, Odhner 1929, Meier-Brook 1963, 1975, Feldmann 1971, Holopainen 1979, Holopainen and Hanski 1979). This apparent high tolerance to environmental variation and even deterioration is obviously an important trait in the profundal of Lake Esrom where the oxygen deficiency in summer is a regular phenomenon (J6nasson 1972). The environmental severity is a plausible explanation for the absence of the profundal specialists, P. conven- tus and P. personatum (see Meier-Brook 1975, Holopainen and Hanski 1979). The stable coexistence

114 OIKOS 41:1 (1983)

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Page 18: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

of the two generalist species at fairly high numbers obviously needs some explanation. In this possibly competitive situation, the basic question would be: what permits P. subtruncatum to co-exist when it is a smaller species, grows slower, achieves maturity later and pro- duces lower number of young (maximum 12 per parent as compared to 20 in P. casertanum, Tab. 5), even if the young are more advanced at birth (12% of minimum mature weight as compared to 7% in P. casertanum).

The length ratio of the two species is 1.3 and weight ratio 1.8 for maximum sized animals, but the respective figures are 1.4 and 2.7 when minimum sizes are com- pared. According to general experience (e.g. Hutchin- son 1959, Fenchel 1975) this is enough to explain the coexistence of two ecologically similar species. How- ever, the mechanism involved is not easily understood with detritivorous animals unless they take their food from different sized sediment particles or flocci etc. This possibility is supported by the fact that the gut contents of Pisidium usually looks like brown sediment despite these being regarded as filter-feeders. However, a more likely answer to their coexistence here is an absence of competition due to the severity of the abiotic environ- ment or predation pressure. Consequently, the densities are much lower than the carrying capacity of the envi- ronment as judged by the food availability.

4.2. Anaerobiosis

The obvious high tolerance of these three Pisidium species to lack of oxygen and their consequent ability to survive several weeks in totally anaerobic conditions is a problem in itself. According to J6nasson (1972) the period of total oxygen lack at the depth of 20 m in Lake Esrom may be more than 8 wk (e.g. in 1958, 1959) during the summer stagnation period - with bottom temperatures as high as 8-10TC. In these conditions the bivalves, as homotopic animals, are confined to the bottom and must be physiologically adapted to anaerobiosis. This kind of facultative anaerobiosis is not uncommon in aquatic bivalves as recently reviewed by Newell (1972), de Zwaan and Wijsman (1976), de Zwaan et al. (1976) and de Zwaan (1977). The ample literature on this subject is generally directed towards marine species, but the metabolic responses in freshwater are probably similar in main features (e.g. Goddard and Martin 1966). An interesting ecological point concerns the effects of anaerobiosis on the energy flow and energy allocation in these populations. Obviously the energy demands of individuals and of the whole population can be considerably depressed when necessary as suggested by the cessation of growth in both adults and embryos (see above) and by the de- crease in oxygen consumption as a result of decreasing oxygen content of the environment (Berg et al. 1962). The oxygen consumption of P. casertanum from Lake Esrom was shown to decline fairly regularly with de- creasing oxygen content of the water, until a value of ca.

3 mg 1` or 30% of saturation had been reached, when the consumption was ca. 50% of the initial value. The decrease then became steeper, and at 0.5 mg 17' the consumption was only 10% of the initial. The critical point according to Berg et al. (1962) was an oxygen content of ca. 1.5-3 mg 17' or 15-30% of saturation at a temperature of 1 1C. This could be the main or at least one physiologically critical point with a decrease in energy expenditure and subsequent switch to a greater use of anaerobic metabolism. Typical features of anaerobiosis seem to be, in addition to reduced metabolic rate, a higher relative and sometimes abso- lute use of carbohydrates as the energy source (Pasteur effect) and the accumulation and/or excretion of organic acids.

Studies on aquatic snails (Mehlman and von Brand 1951, McMahon and Russel-Hunter 1978) have shown that those tolerant of anaerobic conditions excreted organic acids continuously as end products of anaerobic metabolism instead of accumulating lactid acid, as in those species with a low resistance to anoxia. The latter species build up an oxygen debt, which has to be repaid by higher oxygen uptake in subsequent aerobic condi- tions. The obvious resistance of the Pisidium popula- tions in question to long anoxic periods suggests that they are able to decrease the metabolic rate extensively and to excrete the end products of anaerobic metabolism. So they are not likely to have any oxygen debt or elevated oxygen consumption after the autumn overturn - even if high amounts of oxygen are readily available at that time. Yet the anaerobiosis must reduce the carbohydrate reserves of the bivalves and their re- building is likely to further slow down the growth of adults and/or embryos.

Acknowledgements - This study was made at the Freshwater Biological Laboratory, Univ. of Copenhagen. The authors ex- press their most sincere thanks to Mr E. Frederiksen and Mr F. Pedersen for valuable help in laboratory and field work and also to H. Heegaard, K. Therkildsen and H. M0ller. The au- thors are much obliged to C. Meier-Brook, who confirmed the identifications of the two dominant species, to E. Ranta, who programmed the computer and finally to Professors T. B. Reynoldson and K. H. Mann who criticized the manuscript. The financial support from the Nordic Council of Ecology and Danish Ministry of Education to I.J.H. is also gratefully acknowledged.

References Alimov, A. F. 1970. Potok energii cherez populyatsiyu mol-

lyuskov (Na primere Sphaeriidae). - Gidrobiol. Zhurnal 6: 63-71.

- 1981. Funktsionalnaja ekologiya presnovodnykh dvustvor- chatykh mollyuskov. - Trud. Zool. Inst. AN SSSR 96: 1-248.

Bass, J. A. B. 1979. Growth and fecundity of Pisidium am- nicum (Muller) (Bivalvia: Sphaeriidae) in the Tadnoll Brook, Dorset, England. - J. Conch. 30: 129-134.

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Page 19: Long-Term Population Dynamics and Production of Pisidium (Bivalvia) in the Profundal of Lake Esrom, Denmark

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