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Article

How Daphnia magna Defends Itself against Predators: Mechanisms and Adaptations in a Freshwater Microcosm

by
Goran Kovačević
1,*,
Petra Tramontana Ljubičić
2,
Daniela Petrinec
3,
Damir Sirovina
1,
Maja Novosel
1 and
Davor Želježić
4
1
Department of Biology, Faculty of Science, University of Zagreb, Horvatovac 102a, HR-10000 Zagreb, Croatia
2
IV. Gimnazija, Ul. Žarka Dolinara 9, HR-10000 Zagreb, Croatia
3
Croatian Institute for Brain Research, University of Zagreb School of Medicine, Šalata 12, HR-10000 Zagreb, Croatia
4
Unit for Mutagenesis, Institute for Medical Research and Occupational Health, HR-10000 Zagreb, Croatia
*
Author to whom correspondence should be addressed.
Water 2024, 16(3), 398; https://doi.org/10.3390/w16030398
Submission received: 7 November 2023 / Revised: 2 January 2024 / Accepted: 19 January 2024 / Published: 25 January 2024
(This article belongs to the Special Issue Biodiversity and Functionality of Plankton Communities)
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Abstract

:
The freshwater water flea (Daphnia magna Straus, 1820) is prey for numerous predators. Yet it possesses a wide range of strategies to defend itself against predation. The aim of this work is to investigate the defensive mechanisms employed by D. magna to reduce predation by the coelenterate Hydra viridissima, and two planarians, Polycelis felina and Dugesia gonocephala. To do this, we used a freshwater microcosm. An additional aim is to investigate interactions with the presence of the isolated endosymbiotic algae from green hydra, thus combining and observing the interaction of the zooplankton and microalgal component. Each experiment included five replicates (13.5 °C, 25 °C), in crystallizing glass containers (60 mL volume, 60 mm diameter, 35 mm height), including satiated (fed with larvae of Artemia salina) and starved predators, respectively (one or five individuals of a particular predator species in one microcosm). As the isolated microalgae are unique, we tracked the following three mechanisms of Daphnia defense for the first time including precisely this microalgal component: (i) grouping (visual magnification), i.e., two or more Daphnia holding together; (ii) the phenomenon of overproduction, i.e., any number of Daphnia in one container above the 10 initially added individuals; and (iii) accelerated movement (“bullet movement”), i.e., high-speed movements in particular microcosms. The results provide new information for a better understanding of the interspecific relationships in systems that include both zooplankton and microalgal components.

1. Introduction

The large water flea (Daphnia magna Straus, 1820) (Branchiopoda, Cladocera) is a zooplankton species widespread in the Northern Hemisphere, up to 5 mm in size. Due to its abundance, it represents an important source of food for numerous invertebrates and fish [1]. D. magna feeds on bacteria and planktonic algae [2] by filtering the surrounding water. The consumption of bacteria in D. magna is the same or even greater in the presence of algae in suspension, and algae consumption is lower in the presence of bacteria compared to its absence [3]. In nature, water fleas frequently occupy the role of prey, and predation is thought to be the most common cause of their mortality [4].
D. magna can reproduce parthenogenetically or sexually, depending on environmental conditions. Eggs are produced by stem cells in the ovary. The embryogenesis of parthenogenetic eggs occurs in the dorsal brood pouch from which the young water fleas emerge as smaller versions of adult individuals [5]. The number of juveniles produced by the adult D. magna depends on the amount of food available and on environmental impacts. The length of time between moltings depends on the water temperature. In adults, it can vary from >15 days at 5 °C to approximately two days at 25 °C. The period between moltings also depends on the age of the individuals. Juveniles molt every day for the first five days of life at a temperature of 25 °C [6]. Algae nutrition also affects the reproduction of D. magna: male individuals are more active in mating behavior and more successfully fertilize resting eggs after eating the algae Stephanodiscus hantzschii Grunow in Cleve and Grunow, 1880 [7].
D. magna is a commonly used organism in biological research. It is suitable for testing because of its appropriate body size, easy maintenance and manipulation in laboratory conditions, short life cycle, and great reproductive ability. A large number of individuals can become available in a very short time [8]. Although D. magna is widespread in aquatic ecosystems, it does not inhabit those that are polluted [9], and therefore, it is used for ecotoxicological research [10,11,12].
Green hydra (Hydra viridissima Pallas, 1766) and the planarians Dugesia gonocephala (Duges, 1830) and Polycelis felina (Dalyell, 1814) are small freshwater invertebrates. H. viridissima (Cnidaria, Hydrozoa) has a radially symmetrical body, up to 10 mm in size and, as a predator, feeds mostly on insect larvae, bacteria, and small crustaceans. Hydra catch prey with tentacles. Stinging cells in the tentacles play a key role in defense and in capturing the prey [13]. In its gastrodermal myoepithelial cells, it harbors endosymbiotic microalgae. It is a commonly used model organism. Planarians belong to the Platyhelminthes, they are predators and detritivores and feed on small annelids, mollusks, insect larvae, and planktonic crustaceans. Planarians have an important ecological role in food chains. Because of their simple and inexpensive breeding, easy collection, and low tolerance to various chemical substances, they are often used in various ecotoxicological studies [14,15,16,17]. P. felina inhabits clean and cold streams and lakes in Europe and Asia and tolerates rapid currents well [18]. D. gonocephala is a common inhabitant of the lentic and lotic ecosystems of continental Europe [19].
A microcosm represents a simplified ecosystem in controlled conditions, which is used to simulate and predict the behavior of organisms within natural ecosystems. Research based on the concept of the microcosm is of great importance in determining the roles of certain organisms in the ecosystem. Qualities of the microcosm include reproducibility and the possibility of controlled conditions [20]. The microcosm as a link between theory and nature itself increases understanding of natural processes and enables research into natural processes and ecosystems in controlled conditions [21].
The purpose of our study is to investigate the mechanisms of defense used by D. magna to defend itself against three macrozoobenthic organisms, one hydra and two planarian species. We wanted to observe interspecific reactions in a multispecies ecosystem/freshwater microcosm. To do this, we used freshwater microcosms in which we monitored the population dynamics of D. magna when in the presence of these three predatory species. Our study investigated and determined the defense mechanisms and adaptations of D. magna in freshwater microcosms within a system including water fleas, the macrozoobenthic hydras, and planarians as well as the isolated endosymbiotic microalgae, thus combining and observing the interaction of zooplankton and microalgal components. We wanted to see what difference isolated microalgae make and what effect they have in a freshwater microcosm. Evidence on isolation/cultures of endosymbiotic algae from green hydra, and on the presence of microalgae in the microcosms is limited. Furthermore, to the best of our knowledge, the isolates of microalgae Desmodesmus subspicatus from green hydra we used in this work are unique, i.e., they present the only permanently maintained culture in the world. We expected to observe the effect of this very specific microalgal component in the microcosm systems. As the used isolated microalgae are unique, we tracked the three mechanisms of Daphnia defense for the first time including precisely this microalgal component. Focusing on the population dynamics, we monitored the reactions of D. magna regarding the relationships between the constituents in the set of freshwater microcosms.

2. Materials and Methods

2.1. Organisms

The following freshwater organisms were used in this study: the large water flea (Daphnia magna Straus, 1820), green hydra (Hydra viridissima Pallas, 1766), isolated endosymbiotic microalgae from green hydra, Desmodesmus subspicatus (Chodat) Hegewald et Schmidt 2000 (Chlorophyceae), and the planarians Polycelis felina (Dalyell, 1814) and Dugesia gonocephala (Duges, 1830). Most of the organisms were cultivated at the Division of Zoology, University of Zagreb, but P. felina was collected from Gračanski potok (Zagreb, Croatia). D. magna was cultivated in a 60 L breeding aquarium with aerated water with a temperature range from 17 °C to 21 °C. Once to twice per week, D. magna was fed with yeast (dry or fresh) and every day with fresh Chlorella sp. and fish food (the smallest granulation). Maintenance was performed under halogen light (T8, 35 W) with a photoperiod of a 10 h night and 14 h day.
The culture of H. viridissima was maintained in glass containers (volume 2 L) in aerated aquarium water at room temperature of 21 °C and under diffused daylight of a photoperiod of 10 h light and 14 h darkness. H. viridissima were fed two times per week with the planktonic crustacean Artemia salina (Linnaeus, 1758) (larvae), and after each feeding, they were transferred into fresh aerated aquarium water. D. gonocephala was maintained in glass containers and in the same manner. P. felina was kept in a laboratory in glass containers (volume 1 L) in aerated aquarium water. They were kept in a refrigerator at a temperature of 13.5 °C and fed once a week with larvae of A. salina. One hour after each feeding, they were transferred into fresh aerated aquarium water in order to remove any remains of digested food.
The isolated microalgae were maintained by a standardized method in test tubes 16 cm long and 15 mm in diameter on sterile deep stock agar (2 g of agar, 100 mg KNO3, 1 mL MgSO4·7 H2O, 1 mL K2HPO4, 0.1 mL FeCl3 and 100 mL of distilled water) [22,23]. The algae were isolated in a standard way [24]. They grew in sterile conditions in an air chamber at 24 °C and under constant illumination of an intensity of 80 μmol/m2; each tube contained 5 mL of nutrient substrate.

2.2. Experimental Setup of the Microcosms

Experiments were performed in crystallizing glass containers of 60 mL volume, 60 mm in dimeter and 35 mm in height with 50 mL of aerated water. Each experiment was set up in two temperature regimes: 25 °C with a photoperiod of an 8 h day and 16 h night, and 13.5 °C in the dark. Both satiated and starved predators (hydras, planarians) were used, respectively. Satiated animals were those fed just before the experiment, and starved animals had last been fed at least three days before the experiment. Each experiment setup was performed in five replicates and the results were recorded one hour and 24 h after the experimental setup. Combinations of the experimental organisms are presented in Table 1.
In each microcosm setup, either one or five individuals of a particular hydra or planarian species were added with a dropper. In microcosms with more than one hydra/planarian species, hydras and planarians were added in ratios of 1:1 and 5:5 individuals (one or five predatory individuals of a particular predator species per one microcosm), respectively. Ten individuals of the prey D. magna were added per microcosm. In the case of the experimental setups that included the addition of the microalgae, one quarter of the algae content from one test tube in 10 mL of aerated water was added with a metal spatula and homogenized by stirring with a spatula without changing the direction of mixing. After mixing, the suspension of algae was added to a 60 mL container previously filled with 40 mL of aerated water, and then the other constituents of the microcosms were put into these containers.
Changes in Daphnia were registered by visual observation. The grouping of D. magna was considered any holding together of two or more living individuals, two or more individuals some of which were alive, and some dead, and two or more dead individuals that had once been alive during the experiment. Overproduction of D. magna was considered any number of D. magna in one container above the ten initially added individuals, during the experiment. Alive and dead animals were counted. Accelerated movement or “bullet movement” describes high-speed movements of living D. magna in particular microcosms, compared to movements of living D. magna in the control setup with D. magna present only.

2.3. Statistical Analysis

For the statistical processing of data, the Statistica 13.0 software package was used. The potential difference between the groups was determined by variance analysis and the Tukey test. The statistical significance in all the methods used was p < 0.05. For the statistical analysis of the grouping, both live and dead individuals of D. magna were included. For the statistical analysis of overproduction, the number of Daphnia individuals over ten in one container was included, where both live and dead individuals were counted.

3. Results

In this paper, we present three mechanisms of defense and adaptations of D. magna in the freshwater microcosm within the system of water fleas—the macrozoobenthic organisms hydras and planarians—the isolated endosymbiotic microalgae. These mechanisms are: the grouping (Figure 1 and Figure 2), overproduction (Figure 3), and accelerated movement (“bullet movement”) (Table 2) of D. magna. The results enabled us to gain a clearer picture of the importance and mode of the predator–prey relationship and the role of the large water flea in maintaining the natural balance of freshwater ecosystems.
In the control setup with D. magna, no grouping, overproduction, or accelerated movement was noticed.
In the control setup with D. magna and the microalgae, overproduction of D. magna was observed only after an exposure of 24 h at 13.5 °C and 25 °C. Accelerated movement (“bullet movement”) of D. magna was present only after 24 h at the higher temperature (Table 2).
The setup with Daphnia, with added green hydra as a starved predator, showed a grouping of D. magna after one hour with five hydras at 25 °C, as well as after 24 h with one hydra at 13.5 °C, and with one hydra and five hydras at 25 °C (Figure 2).
In the setup with D. magna and P. felina as a satiated predator, a grouping of Daphnia was present after one hour with one planarian at the lower temperature and with five planarians at both temperatures (Figure 1). After 24 h, the grouping phenomenon of D. magna was observed with five planarians at both temperatures and with one P. felina at 25 °C. When P. felina was introduced starved in the experiment, the grouping of D. magna was observed after one hour and 24 h with one planarian and five planarians at 13.5 °C and 25 °C (Figure 2).
In the setup with D. magna and satiated D. gonocephala, the grouping of D. magna was observed after 24 h with one planarian at the lower temperature and with one planarian and five planarians at 25 °C. When D. gonocephala individuals were starved, the grouping of D. magna was present after one hour with one planarian and five planarians at both temperatures. After 24 h, the grouping of D. magna was present with one planarian at both temperatures and also with five D. gonocephala at 13.5 °C (Figure 2).
In the setup with D. magna, and green hydra and P. felina as satiated predators, the grouping of D. magna was observed after one hour with one hydra and one planarian at both temperatures and after one hour with five hydras and five planarians at the higher temperature. After 24 h, the grouping of D. magna was present with one hydra and one planarian and with five hydras and five planarians at both temperatures. With the presence of starved predators, the grouping of D. magna was present after one hour with one hydra and one planarian at the lower temperature and with five hydras and five planarians at both temperatures. After 24 h, the grouping was observed with one hydra and one planarian at 25 °C and with five hydras and five planarians at 13.5 °C and 25 °C (Figure 2). Overproduction of D. magna when the predators were satiated was observed after one hour with five hydras and five planarians at both temperatures. In the case of 24 h exposure, overproduction was observed with one hydra and one planarian at 25 °C and with five hydras and five planarians at both temperatures. When predators were introduced into the experiment starved, overproduction of D. magna was observed after one hour with five hydras and five planarians at the higher temperature. In the case of 24 h exposure, overproduction of D. magna was observed with one hydra and one planarian and with five hydras and five planarians at both temperatures (Figure 3).
In the setup with D. magna, and green hydra and D. gonocephala as satiated predators after one hour the grouping of D. magna was present with one hydra and one D. gonocephala and five hydras and five D. gonocephala at both temperatures. In the case of 24 h exposure, the grouping of D. magna individuals was observed with one hydra and one planarian at both temperatures and with five hydras and five planarians at 13.5 °C. In the case of starved predators, after one hour, there was a grouping of D. magna with one hydra and one D. gonocephala and with five hydras and five D. gonocephala at 13.5 °C and 25 °C. Grouping after 24 h was observed with one hydra and one D. gonocephala at 13.5 °C and 25 °C (Figure 2). Overproduction of D. magna when the predators were satiated was observed after one hour with one hydra and one D. gonocephala at 25 °C. When predators were introduced into the experiment starved, overproduction of D. magna was observed after one hour with one hydra and one D. gonocephala at both temperatures. With 24 h exposure, overproduction of D. magna was observed with one hydra and one D. gonocephala at 13.5 °C and 25 °C (Figure 3).
In the setup with D. magna, and P. felina and D. gonocephala as satiated predators, the grouping of Daphnia was noted after one hour with one individual of each planarian species and five individuals of each planarian species at both temperatures. After 24 h, this grouping phenomenon was observed with one P. felina and one D. gonocephala at both temperatures and with five P. felina and five D. gonocephala at 25 °C. When predators were introduced into the experiment starved, the grouping of D. magna was present after one hour with one individual of each planarian species, and five P. felina and five D. gonocephala at both temperatures. After 24 h, the grouping of D. magna was present with one P. felina and one D. gonocephala at 13.5 °C (Figure 2). Overproduction of D. magna was observed only in the case when predators were satiated, after one hour with one P. felina and one D. gonocephala, and with five P. felina and five D. gonocephala at 25 °C. After 24 h, overproduction of D. magna was observed with one individual of each planarian species at both temperatures and also with five individuals of each planarian species at 13.5 °C (Figure 3).
In the setup with D. magna and P. felina and the microalgae, the grouping of Daphnia was noted after one hour with one satiated planarian at the lower temperature and with five satiated planarians at 25 °C. After 24 h, the grouping phenomenon occurred with one satiated planarian at the lower temperature and with five satiated P. felina at 25 °C. When predators were introduced into the experiment starved, the grouping of D. magna was noted after one hour with one planarian and five planarians at 13.5 °C. After 24 h grouping of D. magna was noted with five planarians at the lower temperature (Figure 2). Overproduction of D. magna when predators were satiated was noted in the case of 24 h exposure with one planarian and five planarians at both temperatures. When predators were introduced into the experiment starved, overproduction of Daphnia was observed after one hour with one planarian at the lower temperature. After 24 h, overproduction was observed with one planarian and five planarians at 13.5 °C and 25 °C (Figure 3). Accelerated movement (“bullet movement”) of D. magna individuals was observed after 24 h with one satiated planarian and five satiated planarians at the higher temperature (Table 2).
The overall statistically significant difference in the grouping of D. magna in the experiment is shown in Figure 2.
No grouping of Daphnia was observed in our experimental setup with D. magna and satiated hydras, and in the case of starved hydras, the occurrence of D. magna grouping was lower than in the case of starved planarians. The influence of two species of predators on the occurrence of D. magna grouping in relation to the influence of one species of predator in the system was greater and was observed to a greater extent when only one predator individual was present in the microcosm. The incidence of D. magna grouping in the presence of the microalgae was lower than in the setup without the microalgae, showing their influence on the stability of the ecosystem. When one individual of a predator was present in the system, altogether the occurrence of overproduction was higher in the case of starved predators. Overall, a statistically significant difference in the overproduction of D. magna in the experiment is shown in Figure 3.

4. Discussion

At the level of aquatic ecosystems, freshwater zooplankton is a very common prey for other larger invertebrates and vertebrates. Daphnia demonstrates a wide range of defense strategies against both tactile and visual predators. In the presence of predators that prefer large water fleas, a higher rate of reproduction whereby water fleas produce smaller-sized individuals to avoid predatory attacks is observed [25]. The reverse situation is seen in the presence of predators that prefer individuals of smaller size. The swimming speed of D. magna in the presence of the cyanobacterial toxin microcystin increases significantly, which can be used as an indicator to detect lower concentrations of this toxin [26]. Furthermore, the speed of D. magna depends on different outer impacts such as light and predators [27].
In this research, we used well-known organisms from freshwater ecosystems: H. viridissima, P. felina, D. gonocephala, D. magna, and the isolated endosymbiotic microalga D. subspicatus. These and related species are used in microcosm research [27,28,29,30,31,32,33,34]. The results of our study point to the defense mechanisms and adaptation of D. magna in freshwater microcosms: grouping, overproduction, and accelerated movement. We tracked the three mechanisms of Daphnia defense for the first time in the microcosms that contain exactly this unique microalgal component. Due to its role as a key food source for secondary consumers, D. magna is an important link in food chains [1]. Predator and prey often find themselves in nature in a development cycle of adaptations to hunting and defense strategies against predators. Therefore, predation has a strong selection pressure and effect on the shaping of the ecosystem. Body size, length of the abdomen, and strength of the carapace of the species D. middendorffiana Fischer, 1851, are defense strategies against the copepod Heterocope septentrionalis Juday and Muttkowski, 1915, whereby the size of Daphnia often changes from generation to generation in response to the annual life cycle of predators [35]. The effectiveness of Cladocera in avoiding predatory attacks may also be influenced by environmental factors (light intensity, water temperature, availability of nutrients, and oxygen concentration) [36].
Predators constantly stalk their prey; therefore, predation has a strong selective effect on prey. As a result, the prey adapts to more efficiently avoid predators, including structural and behavioral changes such as speed [37]. Although it might be stated that predation is harmful (both for the individual prey that is eaten, and for the entire prey population), predation is not necessarily negative for the surviving prey population. The prey that are eaten are not always random individuals that are caught first but are often those that are the weakest links in their population, for example, slow individuals. In contrast, prey individuals that are not eaten feel less mutual competitive pressure for limited resources and produce more offspring. As a result, predation has a positive effect on the prey individuals that are not eaten [38].
Until recently, biological drivers of plankton aggregation were underappreciated [39]. Our results show that the large grouping of D. magna individuals was present as a defense mechanism against predatory attacks. Although in the setup with D. magna and P. felina, and with D. magna and D. gonocephala, the grouping of D. magna was recorded both in the case of satiated and starved planarians, this was seen in a much larger, statistically significant extent in the case of starved predators. They had a much greater tendency to catch their prey. In this case, the frequency of the attacks of P. felina and D. gonocephala increased. Such a grouping of prey individuals was very likely one of the defense strategies against predatory attacks, in which D. magna camouflage themselves among dead individuals in order to avoid death or simply by grouping to achieve an apparently larger size with which D. magna might attempt to intimidate the predator and make it abandon the attack.
Similarly, the grouping of D. magna is visible in the middle of the experimental dish in the presence of a larger number of the flatworm Mesostoma [40]. The grouping of prey individuals as a strategy for thwarting predator attacks has been observed in other species. In microcosm research, the grouping of P. felina is observed as a protective mechanism against predation from other predators [41]. In fish, individuals of Pacific salmon in larger groups have lower predation risk [42]. In addition, the microalgae form aggregations and nets to protect themselves from predation attacks [30]. One of the important drivers of grouping is the detection of predators, so exposure to the chemical cues released by fish and by invertebrate predators (and a substance released from homogenized Daphnia) induces a tendency to form aggregations in Daphnia [43].
Herein, in the case of starved planarians, after 24 h, there was a lower incidence of grouping of D. magna compared to after one hour because there was a smaller number of living individuals. A similar situation was observed in the experimental setups in which one individual of two species of predators was present in the system. In the setup with D. magna and green hydra, the grouping of D. magna individuals was recorded to a small extent and only in the case of starved animals. A possible reason for this is that green hydras move to a lesser extent and at a lower speed than P. felina and D. gonocephala. Therefore D. magna could more easily avoid being caught by green hydra, by retreating to parts of the experimental dish without hydras. The difference in the influence of two species of predators on the occurrence of D. magna grouping in relation to the influence of one predator species was more noticeable when only one predator individual was present in the microcosm, and this difference was reduced when there were five predator individuals. When there was a large number of predator individuals, D. magna grouped to a lesser extent due to more frequent predatory attacks. A lower incidence of grouping was observed when the microalgae were present in the system along with predators, in comparison to other microalgae-free setups. It is possible that grouping is hindered by the aggregation of microalgae and the formation of the microalgal net, with water fleas trapped in the microalgal hunting net [30]. In conclusion, with the presence of predators in the microcosm, individuals of D. magna defended themselves by grouping in such a way that two or more living or dead individuals were grouped together.
The functional diversity of Daphnia zooplankton was also demonstrated in the overproduction mechanism. The regularity of overproduction was observed, especially in the setups with Daphnia, Polycelis and algae, and Daphnia and algae. After one hour, there was no or low overproduction when predators were introduced into the system either satiated or starved, at both temperatures. Overproduction was observed to a greater extent after 24 h with satiated and starved predators, at both temperatures. This is probably because one hour of contact between D. magna and other constituents of the microcosm was too short for possible overproduction. A significantly higher incidence of overproduction was observed when the microalgae were present. Therefore, the microalgae had a great influence on overproduction, in addition to predators [44].
An example of functional diversity is also displayed by D. pulex Leydig, 1860. If it is exposed to chemical stimuli that signal the presence of predatory larvae of the dipteran Chaoborus, embryos of D. pulex will develop into individuals with defensive spines that will reduce their risk of being eaten by a predator [37,45]. Adaptations of Cladocera, such as body size, fast swimming when escaping, the development of protruding structures on the body, and resting when attacked by predators make them less vulnerable to predation attacks by the copepod Mesocyclops leuckarti Claus, 1857 [36]. In our research, it is possible that the microalgae stimulated the reproduction of D. magna, unlike the research [25] where Scenedesmus obliquus (Turpin) Kützing, 1833, becomes toxic to Daphnia. In general, in our research, there was a greater incidence of overproduction when predators were starved. Then, individuals of D. magna were under greater pressure from predatory attacks and resorted to overproduction. Furthermore, it was observed that in some cases D. magna individuals were smaller than the initial individuals added in the experiment [44]. In the presence of predators that prefer larger individuals of D. magna, there is a higher rate of reproduction whereby D. magna produce individuals of smaller size to avoid predatory attacks [25]. The presence of predators can lead to a reduction in the body size of the prey, which serves as a defense against visual predators [46]. Certain invertebrate predators have strict restrictions regarding the shape and size of their prey [47,48,49,50].
As for the concept of overproduction in our research, it is not entirely clear whether the individuals of D. magna really multiplied, some of them being sucked out by planarians during predation, or whether these “sucked individuals” of D. magna were actually molts of the individuals initially added. If it was a case of multiplication, D. magna was capable of fast reproduction within 24 h under the given predatory pressure. It is possible that the overproduction of Daphnia is a consequence of possible feeding on the microalgae. Since the period between moltings depends on environmental factors and may vary in adult individuals of D. magna [6], it is, in any case, clear that the individuals of D. magna under predation pressure reacted rapidly—either by reproduction or by molting. The microalgae had a great influence on the overproduction of Daphnia, and it is possible that they affected the reproduction of D. magna. Since overproduction was also present in the setups without the microalgae, but with two different predator species, overproduction of Daphnia was possibly stimulated by the “fear” of predation by a larger number of present predators. Finally, if it was a case of molting, this would serve as a camouflage mechanism for the water fleas that survived.
The accelerated movement of D. magna as a high-speed movement is a good escape mechanism from slow predators. During this experiment, we observed an accelerated movement, a description of which we did not find in the literature. D. magna moved at high speed, similar to a bullet heading towards its target, with constant changes of direction. We observed this kind of movement also when there were no predators in the microcosm, but with the presence of the microalgae in the system. In the setup of D. magna with the microalgae, the greatest accelerated movement (“bullet movement”) of D. magna was observed after 24 h at the higher temperature. The swimming rate of D. magna in the presence of the cyanobacterial toxin microcystin is known to increase significantly [26], and the D. magna movement can be affected by certain substances released by predators [43]. In addition, D. magna individuals start to spin around their body axes in the presence of the flatworm Mesostoma, and at a high speed in the presence of a toxin released by the flatworm Mesostoma [40]. Therefore, the observed accelerated movement of D. magna in our experiment could have been stimulated by chemical substances secreted by a member of the microcosm or simply by feeding on the microalgae. It would be useful to determine whether the microalgae caused such a reaction by secreting a kind of toxin or other substance.
We have clearly demonstrated three mechanisms of defense and adaptation of D. magna in the freshwater microcosm, showing the functional diversity of D. magna. Further research could comprise: (i) the variation or change of different environmental conditions (light, temperature, and the introduction of xenobiotics into the system); (ii) different lengths of observation times; or (iii) new combinations of organisms in the microcosms. Furthermore, it could be useful to: (i) increase the volume and depth of the experimental containers; (ii) increase the used number of individuals of a particular species; and (iii) investigate microcosms by introducing or using other freshwater organisms, such as brown hydra or other species of microalgae. This would allow us to extend our knowledge of a variety of responses to environmental factors and ecological modeling.
Networks of dependencies among species or a detailed analysis of multispecies ecosystems with multiple bidirectional interactions have not been performed, but it would be useful to see them in the future, including some other relationships/phenomena/mechanisms that we are currently processing. Introducing more parameters would provide a better insight into the complexity of the relationships in the microcosm/ecosystem. Finally, the use of Convergent Cross Mapping (CCM), Sensitivity Analysis (SA), global sensitivity and uncertainty analysis (GSUA), and other analysis and modeling tools [51,52,53] could be considered for further work on ecological dynamics in the freshwater microcosm.

Author Contributions

Conceptualization, G.K., P.T.L. and D.P.; methodology, G.K., P.T.L., D.P. and D.S.; validation, G.K., P.T.L., D.P. and D.S.; formal analysis, G.K., P.T.L., D.P., D.S., M.N. and D.Ž.; investigation, G.K., P.T.L. and D.P.; resources, G.K., P.T.L., D.P., D.S., M.N. and D.Ž.; writing—original draft preparation, G.K., P.T.L., D.P., D.S., M.N. and D.Ž.; writing—review and editing, G.K., P.T.L. and D.P.; visualization, G.K., P.T.L., D.P., D.S., M.N. and D.Ž.; supervision, G.K. and D.S.; project administration, G.K.; funding acquisition, G.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the University of Zagreb, institutional project number 106-F19-00056/20284116, and support number 20286544.

Data Availability Statement

The data presented in this study are available in this article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Water 16 00398 g001
Figure 1. Microcosm with D. magna and P. felina. Grouped individuals of D. magna are circled.
Figure 1. Microcosm with D. magna and P. felina. Grouped individuals of D. magna are circled.
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Water 16 00398 g002
Figure 2. Mean values and standard deviations of grouped individuals of D. magna with statistical significance for satiated (F) and starved (H) conditions after one hour and 24 h at both temperatures in the experimental setup with: D. magna and one (A1) or five (A5) individuals of D. gonocephala; D. magna and one (B1) or five (B5) individuals of P. felina; D. magna and one (C1) or five (C5) individuals of green hydra; D. magna and one (D1) or five (D5) individuals of D. gonocephala and P. felina; D. magna and one (E1) or five (E5) individuals of P. felina and green hydra; D. magna and one (F1) or five (F5) individuals of D. gonocephala and green hydra; D. magna and one (G1) or five (G5) individuals of P. felina, and the microalgae. The symbols indicate statistically significant differences between the experimental setups: C1 and D1 in satiated conditions at 25 °C after 1 h (Δ); C1 and D1 in starved conditions at 25 °C after 1 h (#); C5 and F5 in satiated conditions at 25 °C after 1 h (◊); C5 and F5 in starved conditions at 13.5 °C after 1 h (*); D1 and G1 in satiated conditions at 25 °C after 1 h (¤); D1 and G1 in starved conditions at 25 °C after 1 h (§); A1 and C1 in starved conditions at 25 °C after 1 h (β); A1 and C1 in starved conditions at 13.5 °C after 1 h (δ); A1 and G1 in starved conditions at 25 °C after 1 h (Φ); F1 and G1 in starved conditions at 13.5 °C after 1 h (ϰ); F5 and G5 in satiated conditions at 25 °C after 1 h (Ж); A5 and F5 in satiated conditions at 25 °C after 1 h (ω); B5 and F5 in satiated conditions at 25 °C after 1 h (Θ); A1 and D1 in satiated conditions at 25 °C after 1 h (Ϩ); B1 and D1 in satiated conditions at 25 °C after 1 h (Ω); B1 and F1 in starved conditions at 25 °C after 1 h (æ); and C1 and F1 in starved conditions at the higher temperature after one hour (Ξ).
Figure 2. Mean values and standard deviations of grouped individuals of D. magna with statistical significance for satiated (F) and starved (H) conditions after one hour and 24 h at both temperatures in the experimental setup with: D. magna and one (A1) or five (A5) individuals of D. gonocephala; D. magna and one (B1) or five (B5) individuals of P. felina; D. magna and one (C1) or five (C5) individuals of green hydra; D. magna and one (D1) or five (D5) individuals of D. gonocephala and P. felina; D. magna and one (E1) or five (E5) individuals of P. felina and green hydra; D. magna and one (F1) or five (F5) individuals of D. gonocephala and green hydra; D. magna and one (G1) or five (G5) individuals of P. felina, and the microalgae. The symbols indicate statistically significant differences between the experimental setups: C1 and D1 in satiated conditions at 25 °C after 1 h (Δ); C1 and D1 in starved conditions at 25 °C after 1 h (#); C5 and F5 in satiated conditions at 25 °C after 1 h (◊); C5 and F5 in starved conditions at 13.5 °C after 1 h (*); D1 and G1 in satiated conditions at 25 °C after 1 h (¤); D1 and G1 in starved conditions at 25 °C after 1 h (§); A1 and C1 in starved conditions at 25 °C after 1 h (β); A1 and C1 in starved conditions at 13.5 °C after 1 h (δ); A1 and G1 in starved conditions at 25 °C after 1 h (Φ); F1 and G1 in starved conditions at 13.5 °C after 1 h (ϰ); F5 and G5 in satiated conditions at 25 °C after 1 h (Ж); A5 and F5 in satiated conditions at 25 °C after 1 h (ω); B5 and F5 in satiated conditions at 25 °C after 1 h (Θ); A1 and D1 in satiated conditions at 25 °C after 1 h (Ϩ); B1 and D1 in satiated conditions at 25 °C after 1 h (Ω); B1 and F1 in starved conditions at 25 °C after 1 h (æ); and C1 and F1 in starved conditions at the higher temperature after one hour (Ξ).
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Water 16 00398 g003
Figure 3. Mean values and standard deviations of overproduction of D. magna with statistical significance for satiated (F) and starved (H) conditions after one hour and 24 h at both temperatures in experimental setups with: D. magna and one (D1) or five (D5) individuals of D. gonocephala and P. felina; D. magna and one (E1) or five (E5) individuals of P. felina and green hydra; D. magna and one (F1) or five (F5) individuals of D. gonocephala and green hydra; D. magna and one (G1) or five (G5) individuals of P. felina, and the microalgae; D. magna and the microalgae (L). The symbols indicate statistically significant differences between the experimental setups: D5 and G5 in satiated conditions at 25 °C after 24 h (Δ); D5 and G5 in starved conditions at 25 °C after 24 h (#); F5 and G5 in starved conditions at 25 °C after 24 h (◊); F5 and G5 in satiated conditions at 25 °C after 24 h (¤); D1 and G1 in starved conditions at 25 °C after 24 h (*); E1 and G1 in starved conditions at 25 °C after 24 h (§); E5 and G5 in starved conditions at 25 °C after 24 h (Θ); F1 and G1 in starved conditions at 25 °C after 24 h (Σ); F5 and G5 in starved conditions at 25 °C after 24 h (β), and within the same experimental setup; E1, satiated conditions at 13.5 °C and starved conditions at the lower temperature after 24 h (◦); G1, satiated and starved conditions at the higher temperature after 24 h (Φ); and G1, in starved conditions at the higher temperature after one hour and 24 h (Ж).
Figure 3. Mean values and standard deviations of overproduction of D. magna with statistical significance for satiated (F) and starved (H) conditions after one hour and 24 h at both temperatures in experimental setups with: D. magna and one (D1) or five (D5) individuals of D. gonocephala and P. felina; D. magna and one (E1) or five (E5) individuals of P. felina and green hydra; D. magna and one (F1) or five (F5) individuals of D. gonocephala and green hydra; D. magna and one (G1) or five (G5) individuals of P. felina, and the microalgae; D. magna and the microalgae (L). The symbols indicate statistically significant differences between the experimental setups: D5 and G5 in satiated conditions at 25 °C after 24 h (Δ); D5 and G5 in starved conditions at 25 °C after 24 h (#); F5 and G5 in starved conditions at 25 °C after 24 h (◊); F5 and G5 in satiated conditions at 25 °C after 24 h (¤); D1 and G1 in starved conditions at 25 °C after 24 h (*); E1 and G1 in starved conditions at 25 °C after 24 h (§); E5 and G5 in starved conditions at 25 °C after 24 h (Θ); F1 and G1 in starved conditions at 25 °C after 24 h (Σ); F5 and G5 in starved conditions at 25 °C after 24 h (β), and within the same experimental setup; E1, satiated conditions at 13.5 °C and starved conditions at the lower temperature after 24 h (◦); G1, satiated and starved conditions at the higher temperature after 24 h (Φ); and G1, in starved conditions at the higher temperature after one hour and 24 h (Ж).
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Table 1. Combinations of experimental organisms in the microcosms.
Table 1. Combinations of experimental organisms in the microcosms.
Daphnia magna + Hydra MicrocosmD. magna + Planarians (+ Microalgae) MicrocosmD. magna + Hydra + Planarians Microcosm
Hydra viridissima + D. magnaPolycelis felina
+ D. magna		Dugesia gonocephala
+ D. magna		H. viridissima + P. felina
+ D. magna
P. felina + D. magna + microalgaeP. felina + D. gonocephala
+ D. magna		H. viridissima
+ D. gonocephala + D. magna
controls
D. magnaD. magna + microalgae
Table 2. The occurrence of accelerated movement (“bullet movement”) of D. magna in the experimental setup with D. magna and P. felina and the microalgae, and in the experimental setup with D. magna and the microalgae.
Table 2. The occurrence of accelerated movement (“bullet movement”) of D. magna in the experimental setup with D. magna and P. felina and the microalgae, and in the experimental setup with D. magna and the microalgae.
Polycelis felina + Daphnia magna + Microalgae D. magna + Microalgae
P. felina (1)P. felina (5)
Satiated (25 °C)1 h−−25 °C−
24 h+++
Satiated (13.5 °C)1 h−−13.5 °C−
24 h−−−
Starved (25 °C)1 h−−
24 h−−
Starved (13.5 °C)1 h−−
24 h−−
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Kovačević, G.; Tramontana Ljubičić, P.; Petrinec, D.; Sirovina, D.; Novosel, M.; Želježić, D. How Daphnia magna Defends Itself against Predators: Mechanisms and Adaptations in a Freshwater Microcosm. Water 2024, 16, 398. https://doi.org/10.3390/w16030398

AMA Style

Kovačević G, Tramontana Ljubičić P, Petrinec D, Sirovina D, Novosel M, Želježić D. How Daphnia magna Defends Itself against Predators: Mechanisms and Adaptations in a Freshwater Microcosm. Water. 2024; 16(3):398. https://doi.org/10.3390/w16030398

Chicago/Turabian Style

Kovačević, Goran, Petra Tramontana Ljubičić, Daniela Petrinec, Damir Sirovina, Maja Novosel, and Davor Želježić. 2024. "How Daphnia magna Defends Itself against Predators: Mechanisms and Adaptations in a Freshwater Microcosm" Water 16, no. 3: 398. https://doi.org/10.3390/w16030398

APA Style

Kovačević, G., Tramontana Ljubičić, P., Petrinec, D., Sirovina, D., Novosel, M., & Želježić, D. (2024). How Daphnia magna Defends Itself against Predators: Mechanisms and Adaptations in a Freshwater Microcosm. Water, 16(3), 398. https://doi.org/10.3390/w16030398

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