The prevalence of diapause response to risk of size-selective predation in small- and large-bodied prey species

The prevalence of diapause response to the simulated threat of fish predation was compared in three species of planktonic crustaceans of the genus Daphnia (D. magna, D. pulicaria and D. longispina), which due to their different body size vary in vulnerability to fish predation pressure in natural conditions. Higher incidence of diapause response was presumed in the larger-bodied species, which due to their higher conspicuousness and higher energetic content experience the greatest size-selective pressure from visually foraging fish. Small-bodied species were expected to utilize less costly yet less effective active defences, e.g. lower conspicuousness achieved due to slower body growth when facing risk of size-selective predation. Proportions of females forming diapausing structures as well as females body size at the maturation period were compared in experimental beakers containing or not containing fish kairomones (chemical cues of fish predation) in a few clonal lineages of 3 species of Daphnia derived from a single lake inhabited by fish. The highest incidence of diapause response to fish kairomones was observed in D. magna (when measured both as proportion of sensitive individuals and as proportion of inductive clones), the largest of the tested Daphnia species. The lowest proportion of individuals and clones that employed diapause was reported in the smallest tested species, D. longispina. In addition, the large-bodied Daphnia (D. magna) showed a greater reduction in body size in response to fish kairomones than the small-bodied species (D. longispina). The results of the present study support the assumption of higher prevalence of diapause response to the threat of selective predation in larger and more vulnerable prey species.     

Predator-induced diapause in Daphnia magna may require two chemical cues

The production of diapausing eggs by Daphnia magna stimulated by fish exudates can be explained as an anti-predator defence ensuring genome protection in periods of high risk from fish predation. The combined effects on the induction of D. magna diapause of an “alarm” chemical originating from injured conspecific prey and fish kairomones were tested. The results of the experiment showed that the cues when present together promote both the production of ephippial eggs and male formation, indicating their role in the synchronization of the entire mode of Daphnia sexual reproduction. Ephippial eggs were only produced in the presence of both fish kairomone and conspecific alarm chemicals, while male offspring occurred in the treatments where both, one or none of the cues were present. However, production of males was the highest when both cues were provided. D. magna responded similarly to the tested cues whether or not the hypothetical alarm substance associated with predator odour came from Daphnia specimens actually eaten by fish or from crushed conspecific individuals. However, chemicals from crushed chironomid larvae combined with fish kairomones did not induce a similar response in D. magna. The relative advantage of utilization of alarm cues or predator kairomones in the induction of defence responses in prey organisms is discussed. Received: 8 June 1998 / Accepted: 11 January 1999     

Fish Faeces as the Primary Source of Chemical Cues Inducing Fish Avoidance Diapause in Daphnia Magna

In a laboratory batch culture experiment, females of Daphnia magna were exposed to five different experimental media containing either:(1) water from an aquarium with fish, (2) extract of fish faeces, (3) mixture of both media, (4) extract of homogenised conspecific Daphnia, or (5) control water without the addition of extra cues. The experiment was planned to test potential pathways of excretion of the chemical cues that induce resting-egg formation in D. magna and to find an effective way of collecting these chemical cues. The results indicate that fish faeces are the prevailing source of the chemical cues that induce resting-egg production in D. magna. The ease of collection and the possibility of storing it in a frozen state make it a convenient cue for inducing diapause response in Daphnia. The results of the experiment imply that in natural conditions Daphnia may face high concentration of the inductive signals once migrating to the bottom zone where fish faeces commonly accumulate.     

Hide, rest or die: a light-mediated diapause response in Daphnia magna to the threat of fish predation

1. In a laboratory batch culture experiment, a diapause response of Daphnia magna to a simulated threat of fish predation was tested at various light intensities, which under natural conditions determine potential vulnerability of Daphnia to visual planktivorous fish. 2. Under moderate light intensity (1.4 μmol m^?2 s^?1) that allows effective predation by fish, the proportion of females producing dormant eggs was significantly higher than under dim light conditions (0.001 μmol m^?2 s^?1) that are not favourable for visual detection of prey. Production of dormant eggs was not observed in complete darkness or in treatments missing fish kairomones, irrespective of tested light conditions. 3. The observed phenomenon is interpreted as a flexible response of prey to the conditional risk of predation assessed by Daphnia according to the presence of fish‐derived cues on the one hand and the presence of dark refugia on the other. Irrespective of the presence of fish kairomones, Daphnia may not produce resting eggs as long as a safe, dark, bottom zone is accessible.     

Role of temperature in diapause response to fish kairomones in crustacean Daphnia

The effect of non-lethal thermal conditions on the diapause response to a simulated threat of fish predation was tested in the freshwater planktonic crustacean Daphnia magna.From an early developmental stage, female Daphnia were either exposed or not exposed to fish kairomones that notified of the threat of fish predation at the benign growth temperatures of 18, 22 or 26 °C. The proportion of females switching from the production of subitaneous to diapausing eggs and their rate of reproduction were recorded.Besides the faster development and more intense reproduction observed at higher temperatures, a smaller proportion of the females formed protective, diapausing eggs when exposed to fish kairomones than was the case in colder conditions. The production of diapausing eggs was not observed when the threat of fish predation was absent. These results indicate an interactive effect of fish kairomones and thermal conditions on diapause induction in D. magna.We interpret these findings in the context of strategies for the maximisation of reproductive success. The production of well protected diapausing eggs (which assures low yet stable gains under diverse thermal conditions) may be a more beneficial life history strategy at lower temperatures, where the chances of survival of active individuals until maturation and successful reproduction are low. Higher temperatures permit faster maturation and more intensive reproduction that may surpass numerical losses of active descendants due to predation, making diapause a less rewarding option.     

Sediments,not plants,offer the preferred refuge for Daphnia against fish predation in Mediterranean shallow lakes: an experimental demonstration

1. Different behavioural responses of planktonic animals to their main predators, fish, have been reported from shallow lakes. In north temperate lakes, large‐bodied zooplankton may seek refuge from predation among macrophytes, whereas in subtropical lakes, avoidance of macrophytes has been observed. The prevalent behaviour probably depends on the characteristics of the fish community, which in Mediterranean lakes is typically dispersed in both the open water zone and in the littoral, as in temperate lakes, and is dominated by small size classes, as in subtropical lakes. 2. We performed ‘habitat choice’ experiments to test the response of Daphnia magna to predation cues at both the horizontal and vertical level by mimicking a ‘shallow littoral’ zone with plants and a ‘deeper pelagic’ zone with sediments. 3. Initial separate response experiments showed that natural plants, artificial plants and predation cues all repelled D. magna in the absence of other stimuli, while sediments alone did not trigger any significant response by D. magna. 4. The habitat choice experiments showed that, in the presence of predation cues and absence of plants, Daphnia moved towards areas with sediment. In the presence of both plants and sediments, Daphnia moved away from the plants towards the sediments under both shallow and deep water treatment conditions. 5. Based on these results, we suggest that Daphnia in Mediterranean shallow lakes avoid submerged macrophytes and instead prefer to hide near the sediment when exposed to predation risk, as also observed in subtropical shallow lakes. This pattern is not likely to change with water level alterations, a common feature of lakes in the region, even if the effectiveness of the refuge may be reduced.     

Interclonal variation in diel horizontal migration behaviour of the water flea <Emphasis Type="Italic">Daphnia magna</Emphasis>—searching for a signature of adaptive evolution

In shallow temperate lakes, zooplankton populations may exhibit diel horizontal migration (DHM) and move towards macrophytes during the day to avoid fish. Using a natural Daphnia magna population, we undertook an experimental investigation aimed to describe the genetic variation for DHM and to study whether an adaptive micro-evolutionary response occurred to changes in macrophyte coverage and fish predation pressure through time. Twenty-seven D. magna clones were hatched from ephippia in the sediment of shallow Lake Ring, Denmark. This lake was eutrophied during the 20th century and was subject to restoration measures in the 1970s. The DHM behaviour of the clones was observed both in the presence and absence of fish kairomone. Significant interclonal variation in DHM behaviour occurred in both treatments. To study the micro-evolutionary response of the Lake Ring D. magna population, two approaches were used. First, we compared the DHM behaviour of clones derived from ephippia collected at different depths. A comparison was conducted between clones resurrected from the period of eutrophication (1960–1980) and from the period of recovery (1986–2000). A significant treatment (presence and absence of fish kairomone) × period interaction effect was identified, suggesting a significant micro-evolutionary response for DHM behaviour. The D. magna clones exhibited a significantly stronger horizontal migration response during the period of eutrophication than in the recovery phase. Second, clonal means, representing the influence of the genotype on the trait, were correlated with environmental conditions (macrophyte cover, fish predation pressure and Secchi depth). The results of this analysis also suggest that a micro-evolutionary response by Daphnia has occurred in reaction to changes in fish predation pressure. In periods with high fish predation pressure, Daphnia migrated more strongly towards the plants. Guest editor: Piet Spaak Cladocera: Proceedings of the 7th International Symposium on Cladocera     

Molecular genetic identification and phylogeny of Daphnia species (Crustacea, Cladocera) from water bodies of the Lake Chany basin

The data on the molecular genetic identification of Daphnia species from the water bodies of the Lake Chany basin are presented. Phylogenetic relationships between these species have been established. The fragments of the mitochondrial DNA genes were used as genetic markers. According to the data obtained, the water bodies examined were inhabited by five Daphnia species, including Daphnia (Daphnia) galeata Sars, D. (D.) longispina O. F. Müller, D. (D.) curvirostris Eylmann, D. (D.) pulex Leydig, and D. (Ctenodaphnia) magna Straus. In addition, longispina a-like individuals that form a separate phylogenetic lineage was identified.     

Predators can induce swarming behaviour and locomotory responses in Daphnia

1. Exposure to chemical cues released by fish induced a tendency to form and maintain aggregations in two Daphnia clones originating from habitats inhabited by fish (and invertebrate predators), while Daphnia from a clone originating from a fishless habitat did not aggregate in response to fish cues.
2. Daphnia from one of the two clones responsive to fish cues, also aggregated in response to chemical cues released by invertebrate predators or to a substance released from homogenized Daphnia .
3. Chemical cues released by predators and the substance released from homogenized conspecifics induced a significant decrease in Daphnia' s swimming speed and an increased readiness to perform a somersaulting escape behaviour, especially in response to light cues.     

Predator-mediated genotypic shifts in a prey population: experimental evidence

We demonstrate the effect of fish predation on genotype frequencies in a laboratory population composed of two Daphnia magna clones, with historically contrasting exposures to fish predation. The two clones differed in their responsiveness to predation via differential avoidance/escape behavior. The clone which coexists with fish in nature is more responsive to the presence of a fish predator, while the clone not exposed to fish predation does not exhibit the defensive reaction. Fish caused a rapid (within 18 h) and significant shift in Daphnia clonal composition, from 1:1 to 8:1, in favor of the responsive clone. Genotype-specific defensive abilities (modus defendi) can contribute greatly to the phenomenon of genotype replacement under selective predation.     

Constitutive but no Triops-induced differences in bet-hedging strategies for hatching in Daphnia

Since cladocerans from the genus Daphnia are known to have evolved several inducible defenses (morphological and life history shifts) against the notostracan predator Triops, we investigated whether hatching was also altered in response to Triops. We tested whether dormant eggs of Daphnia magna are able to detect Triops cancriformis kairomones in the water as a signal of predation pressure and alter their hatching response accordingly to avoid predation. We predicted that, in the presence of Triops kairomones, hatching fractions might be reduced (postponing hatching to a next growing season) and/or that hatching might peak earlier (increasing chances to reproduce before Triops becomes predatory). We also tested whether this response depended on the origin of the population. Ephippia from three D. magna populations, originating from one permanent lake and two temporary pond systems, were exposed to Triops kairomone and control treatments. We observed significant population differences in hatching patterns, both in terms of the fraction of eggs that hatch as well as the timing of hatching, with evidence for within-season bet-hedging through delayed hatching in the populations inhabiting temporary habitats. However, no indication was found that the populations also adjust their hatching pattern to the presence of Triops kairomones.     

Species and clone-dependent effects of tilapia fish (Cichlidae) on the morphology and life-history of temperate and tropical <Emphasis Type="Italic">Daphnia</Emphasis>

In aquatic systems, tilapia introductions may result in marked changes in the structure of prey communities. In this study, we experimentally examined the effects of tilapia-mediated water at the individual and population levels of prey by exposing three Daphnia species to predation cues. We hypothesized that tilapia-mediated water determines reduced age and size at primipara, greater and faster reproduction, enhanced intrinsic rates of population increase (r), and longer tail spines in Daphnia; but that the magnitude of these changes would be species and clone-dependent. When three tropical D. laevis and one temperate D. similis clones were exposed to predation cues, adaptive changes were observed in some of the aforementioned parameters for each clone. The three D. laevis clones exhibited changes in all life-history and morphological measures. Temperate Daphnia spinulata displayed no changes but decreased r values in the presence of predators. The observed changes in the species and clones tested here suggest that, overall, both temperate and tropical Daphnia can detect and adaptively react to the risk of tilapia predation. However, only a fraction of the possible defenses may be displayed by individual clones. In contrast, D. spinulata seems more vulnerable to tilapia predation, given its long body length and absence of adaptive changes. Our study indicates that Daphnia can respond to tilapia-mediated water, and that interspecific and clonal variation exists between temperate and tropical species.     

Evolution of predator avoidance in a Daphnia population: evidence from the egg bank

Dormant propagule pools (egg banks) of zooplankton populations that accumulate in sediments provide biological archives of past conditions and enable the investigation of evolutionary changes in populations over relatively long periods of time (many decades). This study examined the egg bank of a Daphnia pulicaria population in a lake that has been stocked annually with rainbow trout (a zooplanktivore) since 1961. Resting eggs from sediments from the 1920s to 2001 (determined by ²¹⁰Pb dating) were hatched and established as isofemale clonal lines. The phototactic behavior (a proxy for vertical migration behavior) of clones was assessed in the presence and absence of fish kairomones to evaluate the hypothesis that the heavy and consistent level of predation imposed by the stocked trout would have selected for clones that are more negatively phototactic. In addition, exposure to kairomones was expected to induce stronger negative phototaxis for all clones relative to control conditions. The behavior of clones derived from resting eggs from the trout era (after 1961) was significantly more negatively phototactic than it was for pre-trout era clones. Kairomone exposure induced a more negative phototactic response in clones from both eras, but the response was much greater for the pre-trout era clones. These results suggest that the consistently high level of predation by trout over several decades has selected for a conservative (less plastic) vertical migration strategy in which Daphnia maintain a deep daytime distribution with or without the presence of chemical cues from fish predators.     

Controlling Harmful Cyanobacteria: Taxa-Specific Responses of Cyanobacteria to Grazing by Large-Bodied Daphnia in a Biomanipulation Scenario

Lake restoration practices based on reducing fish predation and promoting the dominance of large-bodied Daphnia grazers (i.e., biomanipulation) have been the focus of much debate due to inconsistent success in suppressing harmful cyanobacterial blooms. While most studies have explored effects of large-bodied Daphnia on cyanobacterial growth at the community level and/or on few dominant species, predictions of such restoration practices demand further understanding on taxa-specific responses in diverse cyanobacterial communities. In order to address these questions, we conducted three grazing experiments during summer in a eutrophic lake where the natural phytoplankton community was exposed to an increasing gradient in biomass of the large-bodied Daphnia magna. This allowed evaluating taxa-specific responses of cyanobacteria to Daphnia grazing throughout the growing season in a desired biomanipulation scenario with limited fish predation. Total cyanobacterial and phytoplankton biomasses responded negatively to Daphnia grazing both in early and late summer, regardless of different cyanobacterial densities. Large-bodied Daphnia were capable of suppressing the abundance of Aphanizomenon, Dolichospermum, Microcystis and Planktothrix bloom-forming cyanobacteria. However, the growth of the filamentous Dolichospermum crassum was positively affected by grazing during a period when this cyanobacterium dominated the community. The eutrophic lake was subjected to biomanipulation since 2005 and nineteen years of lake monitoring data (1996–2014) revealed that reducing fish predation increased the mean abundance (50%) and body-size (20%) of Daphnia, as well as suppressed the total amount of nutrients and the growth of the dominant cyanobacterial taxa, Microcystis and Planktothrix. Altogether our results suggest that lake restoration practices solely based on grazer control by large-bodied Daphnia can be effective, but may not be sufficient to control the overgrowth of all cyanobacterial diversity. Although controlling harmful cyanobacterial blooms should preferably include other measures, such as nutrient reductions, our experimental assessment of taxa-specific cyanobacterial responses to large-bodied Daphnia and long-term monitoring data highlights the potential of such biomanipulations to enhance the ecological and societal value of eutrophic water bodies.     

Combined exposure to parasite and pesticide causes increased mortality in the water flea Daphnia

Organisms are exposed to multiple biotic and abiotic environmental stressors, which can influence the dynamics of individual populations and communities. Populations may also genetically adapt to both natural (e.g. disease) and anthropogenic (e.g. chemical pollution) stress. In the present study, we studied fitness consequences of exposure to both a parasite (i.e. biotic) and a pesticide (i.e. abiotic) for the water flea Daphnia. In addition, we investigated whether these fitness consequences change through time as a population evolves. Thus, we exposed Daphnia magna clones, hatched from dormant eggs isolated from different time layers of a natural dormant egg bank, to the parasite Pasteuria ramosa and the insecticide diazinon in a multifactorial experiment. While our experimental treatments for unknown reasons failed to induce disease symptoms in the Daphnia, we did observe a reduced survival of D. magna when simultaneously exposed to both the parasite and the pesticide. No increased mortality upon exposure to individual stressors was observed. We did not observe an evolutionary change in fitness response of the Daphnia clones hatched from different time horizons upon exposure to stressors.     

Interactive effects of fish kairomone and light on Daphnia escape behavior

We investigated the effects of fish kairomone and light intensity on the inducibility and effectiveness of escape behavior in four clones of the water flea Daphnia from different habitats. To characterize and determine the effectiveness of their escape responses, individuals were observed: (i) escaping from the hydrodynamic disturbances of a simulated predator (a small sphere dropped from above); (ii) being preyed upon by small fish (Poecelia reticulata); (iii) responding to encounters with conspecifics in crowded conditions. The simulated predation experiments revealed that when exposed to fish kairomone for 48 h, two Daphnia pulicaria clones, but not two hybrid clones, became about twice as sensitive to fluid disturbances when tested in the light, relative to no-kairomone and dark treatments. When tested in the dark, kairomone had no effect on sensitivity in any clone. All four clones had an all-or-none escape response, in which the strength of the response, as measured by escape distance and speed, was constant regardless of treatment. In the guppy predation trials, kairomone-treated D.pulicaria escaped significantly more often from guppies, in both bright- and dim-light conditions. In dim light, similar to natural lighting conditions, regardless of kairomone, all but the most weakly escaping clone were able to elude attacking guppies in a significant proportion of attacks. Finally, kairomone had no effect on the number of escapes performed by crowded individuals in response to the comparatively weak, non-threatening signals created by other Daphnia, indicating that the kairomone-induced alertness in the D.pulicaria clones did not make them 'excessively' sensitive. The results suggest that Daphnia escape behavior is under complex and efficient environmental regulation, and may play a significant role in aquatic trophic relationships.      

Responses to injured conspecifics and heterospecifics by water fleas,Chydorus sphaericus

Cladocerans have been shown to exhibit a variety of responses to chemical stimuli associated with predation risk, including those from predators and injured conspecifics. In this study, we tested the hypothesis that individuals of Chydorus sphaericus would respond with avoidance behavior to chemical cues from both injured conspecifics and injured heterospecifics. Avoidance behavior was seen in response to cues from C. sphaericus and Daphnia magna. Responses to cues from Daphnia pulex were intermediate between those of the other cues and the water control. We propose that a concentration effect may be responsible for the mixed responses to heterospecific cues and speculate that responses to a broad range of cues may help explain the expansive range of C. sphaericus.     

Depth selection and life history strategies as mutually exclusive responses to risk of fish predation in <Emphasis Type="Italic">Daphnia</Emphasis>

We tested if pelagic crustaceans of the genus Daphnia use different anti-predator defences in environmental conditions that do or do not offer deep refuge from planktivorous fish. We kept Daphnia catawba in two series of 9-m deep enclosures with and without caged cyprinid fish Phoxinus eos. In one series of enclosures, Daphnia could select its depth of residence and hide in deep dark water layers to avoid anticipated fish predation, while in another series of enclosures, a plankton net barrier fixed at 2-m depth forced them to stay in subsurface zone exposed to fish kairomones. We compared depth residence and migratory behaviour strategies with life history strategies (body size and size at first reproduction, diapause induction) in Daphnia exposed or not to fish kairomones with or without deep refuge. In deep enclosures with fish, Daphnia spent daytime hours in deep dark layers while at night, they resided closer to the water surface. Yet, no change in life history parameters of migrating individuals was observed compared to the fish-free conditions. In enclosures with fish, where the net barrier forced Daphnia to reside in subsurface zone, they produced smaller offspring, matured at smaller size and achieved lower maximum body length compared to the fish-free conditions. However, they did not produce diapausing eggs. Our experimental study supports the hypothesis that diel vertical migration behaviour with daytime residence in deep, dark water are the preferred antipredator strategy chosen by Daphnia facing anticipated fish predation over life history changes such as reduced size and low growth rate which are used when dark deep refuge is not present or accessible.     

Genetic differentiation in life history between Daphnia galeata populations: an adaptation to local predation regimes?

Species of the water flea Daphnia exhibit constitutive as wellas phenotypically inducible anti-predator defence strategies,involving life history, morphological and behavioural traits.We explored the hypothesis of genetic differentiation in anti-predatordefence strategies using Daphnia clones originating from twodifferent water bodies: Tjeukemeer (the Netherlands) and FishPond (Belgium). Both water bodies are inhabited by zooplanktivorousfish. In contrast to Tjeukemeer, Fish Pond is also inhabitedby larvae of the phantom midge Chaoborus. The life history responsesof the two sets of clones to kairomones from fish (Perca), tokairomones from Chaoborus, and to a mixture of both were compared.Clones from Tjeukemeer and Fish Pond showed strong responsesto the presence of fish kairomone, with reductions in adultand neonate body length, in age at first reproduction and inthe total number of neonates produced during the first threeadult instars. Responses to Chaoborus kairomone were much lesspronounced, although there was a tendency towards an increasein the number of neonates in the first brood. Significant inter-populationgenetic differences were found for all the investigated traits.However, there was no indication for genetic adaptation of theFish Pond clones to negative size-selective predation by Chaoborus.Compared to Tjeukemeer clones, Fish Pond clones had a lowersize at first reproduction, produced smaller neonates and produceda higher number of neonates in their first brood. This suggestsadaptation to positive rather than to negative size selectivepredation. Genetic differences between populations were observedmainly for constitutive life history traits, rather than forphenotypic shifts in response to the presence of predator kairomones.     

Role of melatonin in the control of depth distribution of <Emphasis Type="Italic">Daphnia magna</Emphasis>

Previous studies confirmed the presence of melatonin in Daphnia magna and demonstrated diurnal fluctuations in its concentration. It is also known that in several invertebrate species, melatonin affects locomotor activity. We tested the hypothesis that this hormone is involved in the regulation of Daphnia diel vertical migration (DVM) behaviour that is well recognized as the adaptive response to predation threat. Using ‘plankton organs’, we studied the effect of three concentrations of exogenous melatonin (10⁻⁵, 10⁻⁷, 10⁻⁹ M) on DVM of both female and male D. magna in the presence or absence of chemical cue (kairomone) of planktivorous fish. Depth distribution was measured six times a day, using infrared-sensitive closed circuit television cameras. Our results showed a significant effect of melatonin on the mean depth of experimental populations, both males and females, but only when melatonin was combined with fish kairomone. Females stayed, on average, closer to the surface than males, both responding to the presence of kairomone by descending to deeper strata. In the presence of exogenous melatonin and with the threat of predation, Daphnia stayed closer to the surface and their distribution was more variable than that of individuals, which were exposed to the kairomone alone. Approaching the surface in the presence of predation threat seems to be maladaptive. We postulate the role of melatonin as a stress signal inhibitor in molecular pathways of response to predation threat in Cladocera.