Introduction

Diel vertical migrations (DVM) of planktonic animals are the example of rhythmic changes of habitat preferences (De Meester et al., 1999) related to light avoidance which rely on synchronic displacements to abundant in food and warm surface waters (epilimnion) after the sunset and descending to colder deep waters with food scarcity before the sunrise. The migration amplitude of freshwater planktonic animals can exceed 60 m (Hutchinson, 1967). Vertical migrations are one of the most efficient mechanism of defense of planktonic prey against visual predators that require light to detect their prey. Migrating planktonic animals, such as Daphnia, are relatively safe during the day in deep waters, but they bear the costs related to limited food availability and lower metabolic rate under low temperature of hypolimnion. Migratory mode of life is, therefore, related with fitness costs—temporary occurrence in suboptimal habitats with food scarcity and low temperature affects the individual growth rate and population growth rate (Loose & Dawidowicz, 1994). In addition, overcoming a steep temperature gradient in a short period of time can also be costly (Mikulski et al., 2017). According to Dawidowicz & Loose (1994), the reduction in population growth of migrating Daphnia (as compared to non-migrating ones) related to vertical thermal gradients can reach over 70% whereas costs related to the food scarcity in deep waters do not exceed 10%. The difference between temperatures in the strata occupied by planktonic animals during the day and night seem to constitute the essential source of fitness costs of DVM.

All models presenting the effects of global warming on stratification in lakes predict the increase of water temperature. It is so far predicted that epilimnetic temperature will tend to increase twice as fast as the temperature of hypolimnetic strata (de Stasio et al., 1996; Niedrist et al., 2018; Stetler et al., 2021). Mean increase of temperature of the epilimnion of Zurich lake equaled in the second half of XX century to 0.24 °C per decade, while hypolimnetic temperature increased only by 0.13 °C per decade (Livingstone, 2003). If fitness costs related to migratory behavior result from the differences in temperature, one may predict that with this difference growing, the costs of DVM will also increase.

The essential aim of our study was to test the hypothesis that changes in vertical temperature gradients in the reservoirs of temperate zone as predicted by the models of global warming (de Stasio et al., 1996), will increase the fitness costs of diel vertical migrations as the mechanism of predator avoidance. To achieve this goal, we compared the juvenile growth rate as the appropriate measure of cladocrean fitness (Lampert & Trubetskowa, 1966) and fecundity in two clones (genotypes) of Daphnia magna. The Daphnia were cultured in the conditions of diel changes in summer temperature typically experienced by planktonic animals, vertically migrating between the epilimnion and hypolimnion in stratified lakes nowadays and under the conditions which, most probably, will reign in the lakes at the end of the century under the conditions of climate warming.

Methods

Two clones of Daphnia magna have been used in the experiment—clone VE from Binnensee (Germany) and clone N from large pond Vrebensky Rybnik (Czech Republic). In both of them, plankitovorous fish either occur permanently (Binnensee) or seasonally (Vrebensky Rybnik).

For the experiment, we used a cohort of Daphnia magna, grown in 250 ml beakers in filtered (0.45 μm) water from Lake Szczęśliwickie in Warsaw. Lake water was stored in a large underground tank with a capacity of 10 m3 and intensively aerated for at least 3 months before the experiment. Animals were fed a suspension of single-celled green algae Acutodesmus obliquus in a density corresponding to 1 mg Corg l−1. Animals were daily transferred to beakers with fresh medium.

The cultures were maintained in a thermostatic chamber (Constant Climate Chamber HPP, Memmert, Germany), which allowed programming the daily changes in temperature and light conditions in four thermal regimes. Cultures were maintained in conditions of summer photoperiod (16L:8D), at temperatures experienced by non-migratory animals, constantly staying in a warm, surface layer of water (epilimnion) and by animals migrating vertically, spending days in cool strata (hypolimnion), and nights in epilimnion. The animals placed in the beakers did not migrate, but were exposed either to conditions that reflect the circadian rhythm of changes in environmental temperature experienced by migrating animals, or to the constant high temperature conditions experienced by animals that remain in the epilimnion for a day. Such life table approach to study fitness and demographic costs of diel vertical migration was first proposed by Orcutt and Porter (1983). Spatial “immobilization” of animals in the beakers excludes the potential costs of locomotion, associated with traversing vertical distances in the lake water column by migrating Daphnia. These, however, were shown to be neglectfully low in relation to the costs associated with the low temperature prevailing in the hypolimnion visited for daytime (Dawidowicz & Loose, 1992).

In the treatment reflecting the present-day thermal conditions experienced by the migrants, the “epilimnion” temperature of 20 °C and the “hypolimnion” temperature of 8 °C were set, while in the treatment simulating the forecasted thermal conditions according to de Stasio (1996)—28 °C and 12 °C, respectively. The cyclic temperature changes from “hypolimnetic” to “epilimnetic” were synchronized with the photoperiod (16L:8D hours, respectively). The change in temperature from “day” to “night” (and vice versa) in cultures simulating migrations occurred linearly, within 1 h, and began 30 min before the “sunset” (turning off the light in the chamber) or the “sunrise” (turning the light on) (Fig. 1).

Fig. 1
figure 1

Pattern of temperature changes in the experimental treatments simulating thermal conditions experienced by migratory Daphnia contemporarily (solid line) and in predicted temperature conditions (broken line). Shaded horizontal bars indicate the night time

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Cultures of each clone were exposed to four different thermal regimes (28 °C; 28–12 °C; 20 °C; 20–8 °C). In each of the thermal treatments, 60 juvenile (12 ± 6 h of development) D. magna from both clones, originating from the second egg clutch of their mothers, were randomly distributed in 6 beakers (10 specimens in each) containing 250 ml of medium. In total, 480 individuals of D. magna (240 from each of the clones) were used during the experiment. The experiment lasted until Daphnia reached the age of first reproduction (AFR) i.e., until the eggs appeared in the brood chambers, then their body length was measured under a stereoscopic microscope, and eggs were counted in each of the individuals.

The dry mass of animals was calculated using the relationship between the body size of D. magna and their mass, from the formula given by Bottrell et al. (1976), modified on the basis of unpublished data of P. Dawidowicz for the clones used, according to the formula:

$$M = 0.00{34}e^{{{1}.{5}0{28}L}}$$

where M—dry mass of the individual (μg), e—Euler number, basis of natural logarithms, L—length of the individual (mm)

The mass thus obtained was used to calculate the individual growth rate of Daphnia, according to the formula:

$$W = \left( {{\text{ln}}M_{{t_{0} }} - {\text{ln}}M_{t} } \right)/\left( {t{-}t_{0} } \right)$$

where t final dry mass of the individual (at time t). Mt0—initial dry mass (taken as the average mass of juvenile D. magna aged 12 ± 6 h at the beginning of the experiment, at time t0), (t − t0)—the duration of the experiment in days (equal to the age of first reproduction).

The birth rate of Daphnia was calculated according to Paloheimo (1974) formula:

$$b = {\text{ln}}\left( {E + {1}} \right)/D$$

where b—birth rate, E—egg number per individual at time t, D—time (in days) from neonate instar till the release of the first clutch offspring

The values of the life history parameters measured (or calculated) for individuals from one beaker were averaged and these averages were treated as a starting point for a 2-way analysis of variance (2-way ANOVA), testing the significance of clone effects (genotype) and thermal regime on the studied parameters (i.e., dry weight, growth rate, fecundity and birth rate of individuals in each clone). The significance of the differences in the tested parameters between individual variants of the experiment was checked by the Tukey post-hoc test of multiple comparisons (at P = 0.05). The statistical calculations were made using STATISTIX v. 9.0 (Analytical Software, 2105 Miller Landing Rd, Tallahassee, FL 32312).

Results

The effect of temperature was evident across all the life-history attributes measured, i.e., age, mass and fecundity at the first reproduction, as well as somatic growth rate and birth rate (two-way ANOVA, P < 0.0001 in all cases, Table 1).

Table 1 Two-way ANOVA testing for the effects of genotype (Clone) and thermal regimes (Temp., 28 °C; 28–12 °C; 20 °C; 20–8 °C) on Daphnia life-history parameters.
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The age at first reproduction of Daphnia varied with increasing average temperature in each thermal variant of the experiment, ranging from 4 days in Daphnia exposed constantly in the “warmed epilimnion” (28 °C) to 12 days in Daphnia experiencing daily temperature changes ranging from 20 to 8 °C (Fig. 2a). Due to the low time resolution (all the animals started reproduction within less then 24 h, and they were were inspected for egg presence only once a day) it was not possible to obtain a measure of variation in AFR within a treatment and no statistical analysis was performed here.

Fig. 2
figure 2

Life-history parameters of D. magna (clone N—open bars, and clone VE—shaded bars) reared at various thermal regimes (means ± 1 SD): a age at first reproduction (AFR); b body mass; c fecundity (number of eggs per individual); d somatic growth rate; e birth rate

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The thermal regime significantly affected the body mass of Daphnia at first reproduction (P = 0.05, Tukey test), which was largest in the coolest variant of the experiment i.e., in Daphnia “migrating” in the temperature range 20–8 °C, and the smallest in Daphnia residing at 28 °C (Fig. 2b). A similar pattern was observed for Daphnia fecundity, but here the difference between the 28–12 °C and 20 °C thermal variants was not significant (P = 0.05, Tukey test; Fig. 2c).

Although the mass at maturity of Daphnia exposed at a constant temperature of 28 °C was the lowest, they achieved the highest rate of somatic growth, as a result of the short time required to reach maturity (Fig. 2d). The lowest rate of somatic growth characterized animals exposed to both variable temperature conditions (28–12 °C and 20–8 °C), between which there were no significant differences (P = 0.05, Tukey test). The birth rates calculated for the different thermal variants of the experiment differed in a very similar way (Fig. 2e).

Discussion

Diel vertical migrations of zooplankton are considered as a trade-off behavior aimed at minimizing the risk of predation, but at the expense of reduced growth rate, resulting from the conditions prevailing in the daily refugium in the depths of lakes (Dawidowicz & Pijanowska, 2018). The most important factor determining the slowdown in the growth of migrating Daphnia is reduced metabolic rate at low temperature they experience during their daily stay in a cold hypolimnion (Dawidowicz & Loose, 1992), while the costs related to food scarcity in the deep water refuge (see a re-analysis of field data on Daphnia DVM against the vertical distribution of food and temperature by Gliwicz & Pijanowska, 1988, presented by Dawidowicz, 1994), locomotion (swimming) costs during DVM (Dawidowicz & Loose, 1992), and costs of physiological stress while passing through the steep thermal gradients in metalimnion (Mikulski et al., 2017) are relatively minor.

We attempted to assess the impact of expected climate change, and resulting changes in the thermal stratification of lakes in temperate zone, on the relative adjustment costs incurred by Daphnia migrating in temperature gradients, expressed by the ratio of the growth rate of individual “migrants” to non-migratory individuals permanently dwelling in surface waters. The experiments confirmed the significant influence of the thermal regime on all studied parameters of the life history of D. magna. “Migratory” animals (experiencing on average a lower average daily temperature) had larger size and body mass at the first reproduction than the “permanent residents” of warm epilimnion, which is consistent with literature data (Weetman & Atkinson, 2004). However, at low temperatures the time taken by the “migrants” to reach the age of first reproduction increased significantly, as a result of which their growth rate was significantly lower than the growth rate of animals exposed to conditions of lack of vertical migration (i.e., at a constant, high temperature). The relative adaptive costs of migration, i.e., the costs expressed by the percentage ratio of the growth rate of migrants to this achieved by “non-migrants”, were thus lower in animals exposed to thermal gradients observed in modern lakes compared to the same lakes subjected to climate change according to the scenarios given by De Stasio (1996). The relative reduction in the growth rate of “migrants” will change from the current 40% to over 55% expected under global warming conditions at the end of the twenty-first century.

The fecundity of Daphnia raised at low temperatures was generally higher than that of animals kept at high temperatures. This seems surprising in the light of earlier results (e.g., of Orcutt & Porter, 1983) who demonstrated that fecundity increases with growing temperature, to decrease at high temperature being, however, consistent with the observations of McKee and Ebert (1996), who reported a negative relationship of mean clutch size in D. magna with temperature. Moreover, the decrease in fertility with increasing temperature may have been due to unintended differences in food availability. The level of food, as important factor determining the reproductive effort in cladocerans (Węgleńska, 1971; Pijanowska et al., 2006), was assumed to be the same in all of the experimental variants. However, the animals were transferred to a fresh medium with a suspension of algal food, once a day. It is likely that some of the algae during the 24-h exposure fell to the bottom of the beakers, and the rate of sedimentation of particles in the water increases with increasing temperature, since the density and viscosity of water is inversely correlated with temperature. This would mean that the food losses caused by algal sedimentation were greater in beakers with (on average) warmer water, and therefore the effect of temperature on animal fertility would only be indirect and result from the varying availability of food. Despite the likely differences in food supply, Daphnia grown in thermal conditions of warm epilimnion, more prone to food shortage in this experiment, nevertheless had a higher rate of somatic growth, as well as birth rate, than “migratory” Daphnia. This is consistent with the empirical data of Loose and Dawidowicz (1994), who showed that the effect of temperature on the growth and birth rates of Daphnia far outweighs the impact of food abundance (except in situations of extreme food shortage).

The increase in the cost of vertical migration will be particularly severe for planktonic animals due to the fact that the pressure of planktivorous fish will also increase with the warming of the surface waters of lakes (Jeppesen et al., 2010). Thus, the intensification of predator pressure will occur in parallel with the increase in the costs of defense against these predators. As a consequence, this may lead to changes in zooplankton communities and the disappearance of large plankton species, e.g., of the genus Daphnia, in favor of competitively weaker species of smaller body size, e.g., Cerodaphnia or Bosmina, which are less sensitive to the pressure of fish. They remain during the day in the epilimnion of lakes and do not bear the costs of vertical migration. This would be consistent with the mechanism described by Dawidowicz and Wielanier (2004).

Summary

Our results demonstrated that forecasted changes in the thermal stratification of lakes of temperate zone, namely the increase in the difference between the temperature of epilimnion and hypolimnion, will result in an increase in Daphnia fitness costs associated with vertical migrations. We suggest that these increased costs may mitigate the competitive advantage of large-bodied cladocerans, such as Daphnia, over small-sized cladoceran species that permanently dwell in warm and food-rich surface waters, relying on their low size-dependent susceptibility to visual predators rather than DVM as their primary defense against fish predation.