Freshwater Biology (2002) 47, 2313–2324

Life history of Daphnia galeata in a hypertrophic reservoir and consequences of non-consumptive mortality for the initiation of a midsummer decline

S. HU¨ LSMANN and H. VOIGT Institute of Hydrobiology, Dresden Technical University, Dresden, Germany

SUMMARY 1. Field and laboratory investigations were combined in a 2-year study on the initiation of a midsummer decline of Daphnia galeata Sars in a hypertrophic reservoir. Quantitative field samples were taken twice a week, and, adult and juvenile mortality rates were calculated. Patterns of reproduction and survival of daphnids born during spring and early summer under fluctuating food conditions were determined in life-table experi- ments. 2. The abundance of Daphnia increased strongly in early May and declined in June 1998 (midsummer decline). In 1999, Daphnia density increased only slowly in spring and remained constantly high throughout the summer.

3. Food conditions (concentrations of POC<30 lm) for daphnids deteriorated in both years in response to increasing Daphnia densities, resulting in a clear-water phase of about 4

weeks. When Daphnia abundance declined in 1998, POC<30 lm concentrations increased greatly, whereas in 1999 food conditions improved only slightly and Secchi depth remained high. 4. Survival of daphnids in life-table experiments decreased greatly after food became rare and was strongly reduced in those animals born during the clear-water phase compared with those born later. In addition, age at first reproduction was retarded during the clear- water phase, resulting in very low population growth rates. Survivorship patterns in life- table experiments suggest a strong impact of non-consumptive mortality on Daphnia population dynamics. 5. Field data of mortality point to differences in mortality patterns between years, probably resulting from different predation impacts of juvenile fish. In both years, however, adult mortality contributed substantially to overall mortality at the end of the clear-water phase. As bottom-up effects on D. galeata were very similar in both years, the significance of non-consumptive mortality on the initiation of midsummer declines appears to depend largely on recruitment patterns before the clear-water phase. A high impact can be expected when Daphnia populations are dominated by a peak cohort of nearly identical age during the clear-water phase.

Keywords: clear-water phase, Daphnia galeata, life history, midsummer decline, mortality

Introduction

The relative importance of bottom-up and top-down Correspondence: Stephan Huulsmann,€ Netherlands Institute of influences on Daphnia population dynamics and the Ecology, Centre for Limnology, PO Box 1299, 3600 BG Maarssen, induction of midsummer declines of Daphnia abun- the Netherlands. E-mail: [email protected] dance has been the focus of numerous studies (e.g.

2002 Blackwell Science Ltd 2313 2314 S. Huulsmann€ and H. Voigt Luecke et al., 1990; De Stasio et al., 1995; Mehner ment patterns of D. galeata Sars observed in a year et al., 1998a). Predation has been suggested to be the with a midsummer decline (Huulsmann€ & Weiler, main driving force by some investigators (Mills & 2000). Forney, 1983; Cryer, Peirson & Townsend, 1986); Meaningful extrapolation of age-specific mortality others have stressed on the importance of bottom-up patterns from laboratory populations to field situa- effects (Lampert et al., 1986; Boersma, van Tongeren tions is impracticable. Conversely, death rates calcu- & Mooij, 1996). However, only in a few cases could lated from field data encompass all sources of the predominant role of predation be demonstrated mortality and are confounded by large uncertainties by detailed comparisons of consumption and mor- (George & Edwards, 1974; Taylor, 1988). An approach tality patterns (Mills & Forney, 1983; Vijverberg simulating in situ conditions while precluding preda- et al., 1990). Consequently, many investigators con- tion hence would be preferable for estimating the cluded that the combined effects of food limitation importance of non-consumptive mortality in field and predation drive Daphnia populations to decline populations. Most studies that have analysed Daphnia in summer (Luecke et al., 1990; Wu & Culver, 1994; life-history patterns under in situ conditions focused Mehner et al., 1998a). It remains largely speculative, on growth or reproduction (Weglenska, 1971; however, as to how exactly these interactions work, Threlkeld, 1979, 1980, 1985; Langeland, Koksvik & although effects of size-selection and timing of top- Olsen, 1985; Larsson et al., 1985; Muuller-Navarra€ & down and bottom-up factors might be especially Lampert, 1996) and neglected mortality. In situ experi- important (Post et al., 1997; Mehner et al., 1998b; ments related to midsummer declines (Threlkeld, Benndorf et al., 2001). 1979, 1985; Larsson et al., 1985) focused only on the Bottom-up effects influence Daphnia dynamics in actual decline phase. If, however, non-consumptive different ways. Starvation-induced mortality may be mortality of adults and preadults is important for the expected especially in juvenile stages (Threlkeld, 1976; decline, the life history of the daphnids born during Tessier et al., 1983) and has been suggested as the the build-up of the population or during the period of main cause of midsummer declines in several lakes high Daphnia abundance would be most critical. (e.g. Boersma et al., 1996), although this mechanism Gries & Guude€ (1999) recently gave evidence of the might not hold for every species and situation significance of non-consumptive mortality for the (Matveev & Gabriel, 1994). Reduced fecundity owing dynamics of D. galeata in Lake Constance. High to food limitation during the spring clear-water phase population losses resulting from sedimentation were is commonly regarded as key mechanism (Lampert attributed to an unidentified infection. However, size– et al., 1986; Sommer et al., 1986). This mechanism is frequency distributions of D. galeata in that study difficult to demonstrate, however, because birth and point to ageing effects as a partially alternative death rates must be considered simultaneously and explanation. That is, it is possible that the infection both parameters are related in a complex way invol- ‘only’ influenced reproduction, whereas mortality ving time lags (e.g. George & Edwards, 1974). The resulted simply from senescence. question remains therefore: Which part of the popula- The exact mechanism leading to midsummer tion dies during a decline and why? Although declines of Daphnia remains speculative as long as mortality of older and larger specimens of Daphnia is the life history under natural conditions is not commonly attributed to selective predation (Gliwicz known. Therefore, the main goal of this study was & Pijanowska, 1989), the synchronous die-off of a to elucidate the life-history pattern of D. galeata peak-cohort might also be an important source of during spring and early summer in a reservoir. Data adult mortality and contribute to the induction of a from life-table experiments approximating field con- midsummer decline (Huulsmann€ & Weiler, 2000; ditions were related to population dynamics and Benndorf et al., 2001). The proposed mechanism demography of D. galeata between May and July in involves a reduced mean life span of a peak cohort two successive years, one with a midsummer decline caused by interactions between starvation-induced and one without. The mortality of juveniles and and age-specific mortality (Threlkeld, 1976). Evidence adults was calculated from both field data and for this idea came from the analysis of long-term data estimates of juvenile growth, and compared with (Benndorf et al., 2001), and the mortality and recruit- Daphnia survival in life-table experiments to get

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2313–2324 Life history of Daphnia galeata Sars 2315 insight into the relative importance of non-con- where Nti+1,obs., Nti,obs. is observed abundance at ti+1 sumptive and consumptive mortality for the initi- and ti, respectively and Nti+1,calc., the calculated )1 ation of a midsummer decline. abundance at ti+1. Mortality rates (m) (day )of juvenile and adult daphnids were calculated by subtracting r from r¢, which results in:

Methods À 1 m ¼ðln Nti þ 1;calc: À ln Ntiþ1;obs:ÞDt ðday Þð3Þ Field sampling and determination of population parameters Life-table experiments Daphnia galeata and particulate organic carbon A total of nine life-table experiments were per- (POC l ) were sampled twice a week from May <30 m formed in 1998 and 1999. Large, fecund individuals to July 1998 and 1999 in the pelagic zone of Bautzen of D. galeata from Bautzen Reservoir were obtained Reservoir, Germany. Samples were taken with a tube by net tows (780 lm) and kept in filtered reservoir sampler (diameter 95 mm, 2 L; Limnos, Finland) at water for 12 h. Six to ten neonates were then placed 1-m intervals over the whole water column. Samples individually in glass vessels (15 mL) filled with from three stations with a similar water depth reservoir water. Water was changed daily (1998) or (10–12 m) were pooled. Secchi depth was recorded every other day (1999), but gently stirred everyday. and water temperature was measured in depth At least three additional neonates were taken to intervals of 1 m. Daphnids from zooplankton samples estimate the initial length of the experimental were enumerated in at least three subsamples. About animals. All experiments were run at 18 ± 0.5 C 100 individuals were measured and the number of and a 16 : 8 h light–dark cycle. eggs in the brood pouch, as well as their develop- Depth-integrated water samples from the reservoir mental stage (Threlkeld, 1979) was recorded. The were collected twice a week and stored in the dark proportion of adult daphnids was calculated after at 4 C. In 1998, the water was passed over a 30-lm determination of the size at maturity (SAM) according screen to remove non-edible size fractions of the to Stibor & Lampert (1993). seston. In 1999, a 250-lm screen was used to mimic Juvenile growth was estimated once per week in more closely the food situation experienced by flow-through chambers at 18 C. Neonates born Daphnia in the field, because inedible particles may within 12 h after collection of adults in the field were influence Daphnia feeding behaviour (Burns, 1968). placed in prefiltered (250 lm) reservoir water, which The POC in the stored reservoir water had was collected twice a week, and the length increase <30 lm moderately increased after 3 days during the clear- recorded after 6 days. water phase (mean increase of 34%). Survival and Mortality was calculated by comparing computed number of offspring were recorded daily. Age at densities of juveniles and adults with the actual first reproduction was estimated by subtracting the abundance estimated in field samples. Briefly, the egg-development time at 18 C [i.e. 3 days; calcula- hypothetical proportion of juvenile and adult daph- ted according to Bottrell et al. (1976)] from the birth nids at sampling date t was calculated by applying i+1 date of the first offspring. The animals of each single weekly obtained juvenile growth rates to all juveniles experiment were treated as a cohort for which age- at t and estimating the potential recruitment of i specific survival (l ) and mean age-specific fecundity daphnids during this time interval (Johnsen, 1983; x (offspring per female, m ) was calculated. The Dorazio, 1986). Field densities of juvenile and adult x intrinsic rate of population growth, r, for each Daphnia at successive sampling dates were used cohort was calculated iteratively from the Euler together with calculated potential densities to esti- equation: mate the population growth rate (r) and the ‘potential’ population growth rate (r¢)(Huulsmann€ & Weiler, Xx¼x ¼ À rx ð Þ 2000): 1 e lx mx 4 x¼a À 1 r ¼ðln Nti þ 1;obs: À ln Nti;obs:Þ=Dt ðday Þð1Þ where x is the age and, a and x are age at first and last 0 À 1 r ¼ðln Nti þ 1;calc: À ln Nti;obs:Þ=Dt ðday Þð2Þ reproduction, respectively.

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2313–2324 2316 S. Huulsmann€ and H. Voigt Results of adults increased. Juvenile and adult mortality rates varied in a similar way (Fig. 1c), increasing greatly Population dynamics and food conditions during the decline of the population and tending to ) The abundance of D. galeata rose from 46 ind. L 1 at remain high thereafter. Because of the very low ) the end of April 1998 to about 140 ind. L 1 within abundance after the decline, strong fluctuations of 1 week (Fig. 1a). After a strong decline in mid-May mortality rates seen in Fig. 1c are likely to result from and a subsequent increase, the population crashed in sampling errors. early June, went almost extinct, and did not recover The POC<30 lm concentrations decreased slightly ) until the end of July (<1 ind. L 1). The SAM was high after the increase in Daphnia abundance in early May (1.4–1.6 mm) and the population was dominated by (Fig. 1d), and strongly increased again at the begin- juvenile stages until mid-June (Fig. 1b). After the ning of June when Daphnia densities decreased. Secchi decline, SAM decreased to 0.8 mm and the proportion depth was closely related to POC<30 lm concentra- tions. A distinct clear-water phase (defined as the period with Secchi depths >2.5 m) developed in May )1 (a) when POC<30 lm concentrations were £ 0.8 mg L ,

) 150

–1 whereas low water transparency in summer corres- ponded to low Daphnia abundance and high 100 POC<30 lm concentrations. 50 In 1999, the population density of D. galeata ) gradually increased from 8 to 70 ind. L 1 between Abundance (ind. L 0 the beginning and end of May (Fig. 2a), and ) (b) never fell below 20 ind. L 1 thereafter. Densities ) 1.5 0.8 >100 ind. L 1 were only recorded twice at the end

1.0 0.6 of July and August. As in 1998, SAM was high (1.3– SAM Proportion of adults 0.4 1.6 mm) during the period of high Daphnia abun-

SAM (mm) 0.5 0.2 dance in May and early June (Fig. 2b), and gradually Proportion of adults 0.0 0.0 decreased to an average of 1.1 mm during the rest of (c) the study. Juvenile size classes dominated the pop-

–1 0.8 Juvenile ulation except for two short periods in July. Mortal- Adult ity rates of adults were generally higher than those 0.4 of juveniles. A consistent trend was not apparent 0.0 (Fig. 2c).

Mortality rate (day ) The POC concentrations decreased and –0.4 <30 lm Secchi depth increased in the second half of May (d) 0.0 1999 when Daphnia densities increased, as was the 2.0 case in 1998 (Fig. 2d). In contrast to 1998, however, –1 1.5 2.5 Secchi POC<30 lm concentration did not recover in June and ) 1.0 5.0 July (values always <0.9 mg L 1), in accordance with POC

POC (mg L0.5 ) the different population dynamics of Daphnia in both

7.5 Secchi depth (m) 0.0 years. 1 May 15 May 1 Jun 15 Jun 1 Jul 15 Jul 1 Aug 1998 Life-table experiments Fig. 1 Changes in the abundance of Daphnia galeata (a), their size at maturity (SAM) and proportion of adults in the population The reproduction of animals born in life-table experi- (b), mortality rates (c), and the concentration of POC<30 lm and ments during the clear-water phase in May 1998 was Secchi depth (d) in Bautzen Reservoir between May and July very low (Fig. 3). About 50% of the individuals failed 1998. The vertical arrows in panel (a) indicate the dates when to reproduce and among those that did, only one life-table experiments were started. The horizontal arrow in panel (d) indicates the clear- water phase with a Secchi depth produced more than two broods. Moreover, the age >2.5 m. at first reproduction was greatly retarded: median

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2313–2324 Life history of Daphnia galeata Sars 2317

(a) 1998 1999 )

1 150 – 14 n = 7 n = 6 n = 6 n = 9 n = 8 n = 10/7n = 10 n = 10 12 100 10

50 8 6 Abundance (ind. L 0 4 (b) Number of broods 2 0 1.5 0.8

1.0 0.6 n = 4 n = 6 SAM 80 n = 3 n = 9 n = 6 n = 4/3 n = 6 n = 7 Proportion of adults 0.4

SAM (mm) 0.5 0.2 60

0.0 0.0 Proportion of adults 40 (c)

1 0.8 20

– Juvenile Adult Age at first brood (days) 0.4 0

0.0 80

Mortality rate– (day0.4 ) 60 (d) 0.0 2.0 40

1 Secchi – 2.5 1.5 20 Age at death (days) 1.0 POC 5.0 0

POC (mg L0.5 ) 1 May 1 Jun 1 May 1 Jun 1 Jul 7.5 Secchi depth (m) 0.0 Date of birth 1 May 15 May 1 Jun 15 Jun 1 Jul 15 Jul 1 Aug 1999 Fig. 3 Life-history characteristics of Daphnia galeata from Baut- zen Reservoir in 1998 (left panels) and 1999 (right panels). Box Fig. 2 Changes in the abundance of Daphnia galeata (a), their size plots display the median and the 10th, 25th, 75th and 90th at maturity (SAM) and proportion of adults in the population percentiles as vertical boxes with error bars. The total numbers (b), mortality rates (c), and the concentration of POC<30 lm and of experimental animals are given in the top panels. The num- Secchi depth (d) in Bautzen Reservoir between May and July bers of experimental daphnids that reproduced are provided in 1999. The vertical arrows in panel (a) indicate the dates when the middle panels. Experiments started during the clear-water life-table experiments were started. The horizontal arrow in phase are shown as hatched bars. panel (d) indicates the clear- water phase with a Secchi depth >2.5 m. low later in the summer to start additional experi- ments. values were about 28 days (minimum 23 days) and In 1999, the first experiment was started before 20 days (minimum 13 days) for animals born in the the clear-water phase (Fig. 3). All individuals of this first and second half of the clear-water phase, cohort reproduced after 5–6 days, that is, before the respectively. Median values of the age at death were POC<30 lm concentration reached a minimum. Six of almost identical to the age at first reproduction during nine animals had only one brood, and animals of this period. In June 1998, after the population had this cohort only survived for 21 days on average declined and the food concentration increased, all (median value). Most daphnids born during the animals reproduced (median value of about eight clear-water phase (27 May and 10 June) produced broods) and had nearly the same age at first repro- only a few broods or did not reproduce at all. The duction (12–14 days). These daphnids also grew much age at first reproduction was delayed, but, in older than did those born during the clear-water contrast to 1998, animals born in the first half of phase. The abundance of daphnids in the field was too the clear-water phase reproduced earlier (median of

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2313–2324 2318 S. Huulsmann€ and H. Voigt 15 days) than those born later (range of 18–47 days). 3 1999 Longevity of experimental animals varied consider- 11 May 2 m ably during the clear-water phase, but the median x values were low. The reproduction and survival of 1 POC daphnids born in late June and July 1999 also 0 differed greatly within single experiments, but in 3 ) 27 May 1 general these animals produced more broods, – 2 day

reproduced earlier and lived longer than those born 1 – during the clear-water phase. 1

Mean age-specific fecundity (mx) was related to 0 Daphnia 4 3 food quantity (Figs 4 and 5). Mean brood sizes were 7/10 Jun generally low; exceptions were always because of 2 mx on 7 Jun

single surviving daphnids. In 1998, animals born at (neonates mx on 10 Jun x 1 the beginning of the clear-water phase (11 May) only m

)or 0 started reproducing when food conditions improved 1 – 3 (Fig. 4). High mx values were recorded after 21 Jun )1 POC<30 lm concentrations exceeded 1 mg L ; they 2

represent three successive broods of a single survi- POC (mg L 1 ving animal. This also holds true for the high fecundity of animals born on 25 May 1998. Both 0 3 brood size and frequency of hatching were higher for 5 Jul animals born in June after the clear-water phase. 2 Reproduction decreased when this cohort was about 1 45 days old. 0 Most of the animals that were born before the clear- 0 1020304050607080 water phase in 1999 (11 May) reproduced only once Days since birth and with only one to three eggs (Fig. 5). Reproduction Fig. 5 Mean age-specific fecundity (mx)ofDaphnia galeata from Bautzen Reservoir in life-table experiments started at five

6 77 dates in 1999 and development of food conditions (POC<30 lm) 3 m 1998 11 May x plotted against days since birth of the experimental animals. )

1 POC

– 2 day

1 1 – ceased almost completely after the POC<30 lm concen- 0 tration reached a minimum. Daphnids born during 3 7 5 Daphnia 25 May the clear-water phase (27 May and 7 ⁄10 June) had a 2 very low fecundity (mx mostly <0.5). Higher values 1 were only found for animals born in early June after a (neonates

x

m very slight increase in the concentration of POC l 0 <30 m

)or 6 about 50 days after birth (i.e. in mid-July). At that 1 3

– 8 June time, only a few individuals were still alive; all mx 2 values >1 were only because of one reproducing 1 daphnid. For those animals that were born later (21 POC (mg L 0 June and 5 July), the slightly improved food supply 0 1020304050607080 occurred earlier in their lives. They responded with Days since birth increasing fecundity. Survivorship also appeared to depend on food Fig. 4 Mean age-specific fecundity (m )ofDaphnia galeata x conditions (Fig. 6). In 1998, daphnids born at different from Bautzen Reservoir in life-table experiments started at three dates during the clear-water phase died simulta- dates in 1998 and development of food conditions (POC<30 lm) plotted against days since birth of the experimental animals. neously at the end of this phase, although there was

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2313–2324 Life history of Daphnia galeata Sars 2319

0.15 2.0 1.0 11 May 1998 25 May 1.5 0.10 0.8 8 Jun 1.0 0.6 0.05 r 0.5 POC ) 1 – ) 1 0.4 – 0.00 0.0 (day ) 0.15 x 2.0 r l 0.2 1999

1998 POC (mg L 1.5 0.0 0.10 11 May 1.0 1.0 27 May 0.05 0.5 7 Jun 0.8 10 Jun 0.00 0.0

Proportion surviving ( 21 Jun 1 May 15 May 1 Jun 15 Jun 1 Jul 15 Jul 0.6 5 Jul

0.4 Fig. 7 Population growth rate (r)ofDaphnia galeata in life-table experiments started in 1998 and 1999 plotted against the date of 0.2 birth of the experimental animals. Experiments started during 1999 the clear-water phase are shown as hatched bars. The POC<30 lm 0.0 concentrations from Figs 1 and 2 are also shown for ease of y n n ul ul g g p p a Ju Ju J J u u e e M 1 5 1 5 A A S S comparison. 15 1 1 1 15 1 15

Fig. 6 Mean age-specific survival (lx)ofDaphnia galeata from Bautzen Reservoir in life-table experiments started at different and longevity of D. galeata, suggesting that non- dates in 1998 (upper panel) and 1999 (lower panel). Each line consumptive mortality may be highly significant for represents one life-table experiment, starting on the date of birth Daphnia population dynamics. of the experimental animals. Experiments started during the clear- water phase are displayed by open symbols. Life-history pattern a 2-week difference in age. Daphnids born in Based on data from 1999, life-history pattern of June 1998 lived longer. Daphnids born before the D. galeata during spring and early summer in Bautzen clear-water phase in 1999 (11 May) had a low Reservoir can be generalised in the following way: mortality until most animals suddenly died about animals born during the build-up of the population 20 days after their birth. Some individuals survived because of excellent food conditions reproduce early, for another 30 days, but the majority of this cohort but have low survival rates when food conditions had vanished at the end of the clear-water phase. deteriorate. Reproduction almost completely ceases in Although more variable than in 1998, timing of the this situation and maximum longevity is about death of daphnids born at different dates during the 50 days. Virtually all individuals of this cohort die clear-water phase in 1999 was broadly similar during the clear-water phase. Although Daphnia can between mid-June and early July. Some specimens adapt their feeding apparatus to food conditions (e.g. survived until the age of about 90 days. As in 1998, Voigt & Benndorf, 2000), the response to decreasing average survivorship was highest for daphnids born food concentrations is slow in adult individuals, after the clear-water phase. because the number of setae is determined at birth The population growth rate (r) was lowest during and the filtering area can only be changed during the clear-water phase in both years (Fig. 7), with rates molting (cf. Voigt & Huulsmann,€ 2001). Animals 1.5–9-fold higher both before and after the clear-water spending their juvenile stages under good food phase. conditions are therefore highly vulnerable to starva- tion. This is the case during the early stages of the clear-water phase when changes in food supply are Discussion both severe and sudden. In contrast, the animals born The results of this study indicate that food limitation at the beginning of the clear-water phase would be during the clear-water phase affects the reproduction expected to enlarge their filter screens, thus better

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2313–2324 2320 S. Huulsmann€ and H. Voigt cope with poor food conditions, and be able to mature created different food conditions. However, the and reproduce under these conditions even when presence of particles >30 lm has been shown not to they last for several weeks. Unfortunately, the lack of decrease adult survival or reproduction of D. galeata life-table data during the period when POC<30 lm (Voigt & Huulsmann,€ 2001). Secondly, changes in the concentrations declined did not allow us to test this reservoir water during storage (3 days) may have hypothesis. altered the food conditions for the experimental Animals born later during the clear-water phase animals compared with the field situation. An live shorter and reproduce later, resulting in very increase in POC<30 lm concentrations was indeed low population growth rates. In general, they only observed during the clear-water phase, probably reproduce once the food supply increases, that is, at resulting from growing bacteria and other heterotro- the end of the clear-water phase. Survival to maturity phic microorganisms. However, given the exponen- is only about 50%. The later the neonates are born tial growth of these microorganisms, the average during the clear-water phase, the greater the negative condition during a sampling interval was probably effects of starvation. Therefore, daphnids born either rather close to the initial situation. Finally, the shortly after the decline in food availability, or relatively small volume of experimental vessels towards the end of this period, die almost simulta- (15 mL) may have reinforced food limitation com- neously. Daphnids born after the clear-water phase, pared with the field situation, although a similar set- when food supply improves, live longer, reproduce up had been used with the even larger D. pulicaria earlier and produce more offspring than those born (Epp, 1996). More importantly, life-history data are during the clear-water phase. consistent with results from field samples. The mean clutch size of adult daphnids always dropped to values £ 1 during the clear-water phase in different Significance of life-history data years, while SAM remained high during this period The relatively short life span of D. galeata found in the or even increased (Huulsmann,€ 2001). This suggests present study was similar to the results of the few that one cohort of adults dominated the population other life-table experiments that attempted to mimic during the clear-water phase and that animals born in situ conditions with different Daphnia species (Lei & during periods of low food supply postpone repro- Armitage, 1980; Threlkeld, 1980). These life spans are duction until conditions improve. generally much shorter than those found in laboratory experiments (Vijverberg, 1976; Lei & Armitage, 1980; Daphnia mortality Orcutt & Porter, 1984), probably because of lower food quality and fluctuating environmental conditions The results of our life-table experiments suggest the in the field (Lei & Armitage, 1980). Age at first following (non-consumptive) mortality pattern: after reproduction as a key factor for Daphnia fitness (Vanni the onset of food limitation, adult mortality is high, & Lampert, 1992) increases in response to decreasing then declines and increases again towards the end of food levels and low temperature (Weglenska, 1971; the clear-water phase. At that time, ‘old’ adults, – Hrba´ckova´ & Hrba´cek, 1978; Orcutt & Porter, 1984). which have survived throughout the clear-water However, as there seems to be a physiological phase – and ‘young’ adults – which were born during constraint to the acceleration of development with this period and are just about to become mature – die temperature, the very high values of age at first simultaneously. Juvenile mortality would first be low reproduction found in the present study may have or moderate, but would increase during the clear- resulted from a combination of low food and water phase because of the death of animals that are relatively high temperature (Neill, 1981; Giebelhausen about to become adults. & Lampert, 2001). Mortality in the field was estimated based on the The general trends in life-table experiments were abundance of eggs, juveniles and adults. Because consistent in both years, although the experiments these estimates encompass all sources of mortality suffered from a number of limitations. First, reservoir and are subject to greater errors, they cannot be water was passed over a 30-lm and 250-lm screen in directly compared with the life-table data. Differ- 1998 and 1999, respectively, which could have ences in mortality patterns between years may be

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2313–2324 Life history of Daphnia galeata Sars 2321 explained by specific conditions in single years. For reduced recruitment. A strong ageing effect on the example, there may be differences in the biomass of initiation of midsummer decline can be expected if the juvenile zooplanktivorous fish (Mehner et al., 1998a), members of the peak cohort have a similar life history in the duration of the clear-water phase and high and thus die more or less simultaneously. The mean predation pressure, and in the population structure life span of daphnids born during the build-up of the of the Daphnia (absolute and relative density of population was indeed low, suggesting that these juveniles). With regard to the last point, uncertain- animals would have vanished by the end of the clear- ties in determining SAM (Stibor & Lampert, 1993) water phase. The life history of animals born during and the significance of prereproductive mortality periods of low food supply points to a strong effect of found in life-table experiments are important. To low longevity on overall mortality in this situation some extent, ‘adult mortality’ estimated from field (Dorazio, 1984). samples may thus actually be mortality of late Recruitment prior to the clear-water phase is a juvenile instars (Huulsmann€ & Weiler, 2000). Juvenile major determinant for the initiation of the midsum- fish are the main vertebrate predators in May and mer decline. In 1998, the population increased three- June in Bautzen Reservoir (Mehner et al., 1998a; fold during 1 week in early May. The strong decline in A. Wagner, personal communication); because of June (end of the clear-water phase) can partly be gape-limitation, they forage mainly on juvenile attributed to the die-off of this peak cohort. This daphnids (Mehner et al., 1998b). It is likely therefore interpretation is also supported by laboratory experi- that adult mortality during the clear-water phase ments on adult survival at different food regimens in resulted primarily from a combination of age-speci- 1998 (Voigt & Huulsmann,€ 2001). In 1999, in contrast, fic and starvation-induced mortality. Juvenile daph- the population increased slowly and continuously. No nid mortality may be caused by both starvation and dominant cohort developed. Although adult mortality predation by juvenile fish and invertebrate preda- increased about 4 weeks after the onset of the clear- tors. It should be kept in mind, however, that apart water phase, similar to the situation in 1998, the from food quantity and quality, further bottom-up consequences were minor because only a small part of related factors may influence survival, especially the population was affected. Thus, non-consumptive maternal effects (Lynch & Ennis, 1983; Cowgill, mortality of adult daphnids may actually occur in Williams & Equivel, 1984) and effects of dissolved every year, especially at the end of the clear-water cyanobacterial toxins (Lampert, 1981; Jungmann, phase, but its significance for the population dynam- 1992). Whereas maternal effects were largely inclu- ics depends on the strength of the peak cohort and ded in our life-table approach, cyanobacterial toxins consequently on recruitment in early spring. This do not appear to have had a large impact on conclusion is corroborated by a comparative analysis Daphnia fitness in our study, because r was relat- of reported cases of midsummer declines (Huulsmann,€ ively high in summer. in press). Despite uncertainties related to the mortality pat- The formation of peak cohorts has been shown to be terns as determined from field samples in the present a distinguishing feature of cycling populations study, adult mortality clearly contributed substan- (McCauley & Murdoch, 1987). Assuming that Daphnia tially to overall mortality during Daphnia declines at exhibits a ‘single-generation’ cycle during the clear- the end of the clear-water phases, regardless of the water phase, without interference of additional mor- magnitude of the decline. tality factors, the formation of a new cohort should be expected. However, the population is likely to be highly vulnerable to predation at the time when it Conclusions declines to its nadir before the new cohort is pro- Results of this study suggest that non-consumptive duced. The extent of the decline thus depends on the mortality may be significant for Daphnia population timing of all mortality factors and recruitment pat- dynamics. The proposed mechanism relies on two terns. A full explanation of midsummer declines of prerequisites: the formation of a strong peak cohort of daphnids will only be possible if all these factors are about the same age and, subsequently, strongly taken into account.

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