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.     

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     

Response of diapausing eggs hatching to changes in temperature and the presence of fish kairomones

It has been hypothesized that the production of diapausing eggs in Daphnia can be induced by fish kairomones. A population of Daphnia could survive severe predation using this predator avoidance strategy. However, in changing environments, diapausing eggs experience various temperature conditions, and hatchlings at emergence may be exposed to the same predation risks as their mothers. Therefore, staying in diapause or an immediate response upon hatching to available environmental information could be important for hatchling survival. For this study, we investigated the impact of water temperature (10, 15, 20, and 25°C) in the presence and absence of fish kairomones (Lepomis macrochirus) on the hatching success of resting eggs (D. galeata). Results show that no diapausing eggs hatched at the lowest temperature (10°C), and the highest hatch percentage occurred at 15°C. Although higher water temperatures reduced hatching success, diapausing eggs hatched more quickly. The number of hatchlings was significantly higher after exposure to fish kairomones, and this was more noticeable at higher temperatures (20 and 25°C). The present results suggest that the diapausing eggs were produced as a predator avoidance strategy in Daphnia; however, the presence of fish works as a positive signal to increase hatchlings when the diapausing stage is terminated.     

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.     

Salinity tolerance in <Emphasis Type="Italic">Daphnia magna</Emphasis>: characteristics of genotypes hatching from mixed sediments

The hatching of diapausing eggs is a means of temporal dispersal that can provide populations with genotypes adapted to different environments. In a salinity-variable shallow lake, we predicted that the mixing of different age-classes of eggs in the sediment may yield genotypes with different salinity optima. The alternative would be the absence of local adaptation and the presence of a homogenous population of salt-tolerant genotypes with high phenotypic plasticity. We tested these alternatives by isolating Daphnia magna resting eggs from different sediment depths, exposing them to hatching cues at different salinity levels and measuring the performance of hatched individuals. Results revealed a homogeneous sediment with generally broad-tolerance genotypes and some genotypes with low salt tolerance, which supports the second hypothesis. However, the disturbed character of the sediment hampered historical reconstruction. The absence of local adaptation in the diapausing egg bank may be the result of various scenarios in the response of D. magna populations to severe salinity changes in the lake.     

Uncovering Ultrastructural Defences in Daphnia magna – An Interdisciplinary Approach to Assess the Predator-Induced Fortification of the Carapace

The development of structural defences, such as the fortification of shells or exoskeletons, is a widespread strategy to reduce predator attack efficiency. In unpredictable environments these defences may be more pronounced in the presence of a predator. The cladoceran Daphnia magna (Crustacea: Branchiopoda: Cladocera) has been shown to develop a bulky morphotype as an effective inducible morphological defence against the predatory tadpole shrimp Triopscancriformis (Crustacea: Branchiopoda: Notostraca). Mediated by kairomones, the daphnids express an increased body length, width and an elongated tail spine. Here we examined whether these large scale morphological defences are accompanied by additional ultrastructural defences, i.e. a fortification of the exoskeleton. We employed atomic force microscopy (AFM) based nanoindentation experiments to assess the cuticle hardness along with tapping mode AFM imaging to visualise the surface morphology for predator exposed and non-predator exposed daphnids. We used semi-thin sections of the carapace to measure the cuticle thickness, and finally, we used fluorescence microscopy to analyse the diameter of the pillars connecting the two carapace layers. We found that D . magna indeed expresses ultrastructural defences against Triops predation. The cuticle in predator exposed individuals is approximately five times harder and two times thicker than in control daphnids. Moreover, the pillar diameter is significantly increased in predator exposed daphnids. These predator-cue induced changes in the carapace architecture should provide effective protection against being crushed by the predator’s mouthparts and may add to the protective effect of bulkiness. This study highlights the potential of interdisciplinary studies to uncover new and relevant aspects even in extensively studied fields of research.     

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.     

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.     

An evolutionary perspective on the resistance of Daphnia to the epizoic rotifer Brachionus rubens

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Local adaptation and embryonic plasticity affect antipredator traits in hatchling pond snails

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Is the exotic red swamp crayfish (Procambarus clarkii) a current threat for the Mediterranean tree frog (Hyla meridionalis) in the Camargue (Southern France)?

The non-indigenous red swamp crayfish (Procambarus clarkii) has been shown to be a threat for amphibian conservation. Many amphibian species breed in temporary ponds to diminish predation risk as such ecosystems are free of large predators. However P. clarkii, occurring as an invasive species in the Camargue delta, can readily disperse on the ground and thus colonize isolated ponds. We studied the current impact of the exotic crayfish on the reproductive success of the Mediterranean tree frog (Hyla meridionalis). In a mesocosm experiment, we tested the effect of two crayfish densities (1 and 3 crayfish/m²) on tadpole abundance. We also tested in a field experiment, within a temporary pond, the crayfish’s predation on the tree frog’s eggs. Finally, we developed site occupancy models using data from 20 ponds to assess the effect of crayfish abundance on tadpole abundance. Neither the experiments, nor the site occupancy models showed a negative impact of the current crayfish abundance on the tree frog populations breeding in ponds. We found that recorded crayfish densities were lower than in other areas where crayfish has impacted amphibian populations, but we hypothesize that current crayfish abundance in the area may increase in the future, thus impacting tree frog populations.     

Different thermal stimuli initiate hatching of <Emphasis Type="Italic">Daphnia</Emphasis> diapausing eggs originating from lakes and temporary waters

The simultaneous hatching of Daphnia resting eggs from a number of different lakes and ponds using one set of hatching cues can be difficult to achieve as environmental conditions differ considerably between water bodies. Therefore, optimal hatching conditions for ephippial eggs originating from shallow temporary waters may differ from those found in large lakes. The aim of our study was to compare the optimal thermal conditions for hatching ephippial eggs of Daphnia found in permanent lakes and those from shallow temporary ponds. We used ephippial eggs of Daphnia from the longispina species complex originating from two temporary city ponds and two deep lakes in Poland. The ephippia were protected against overheating at all stages of the field and laboratory work to prevent activation or killing of the eggs. After a refractory period (imposed storage in cool and dark conditions), ephippia were incubated at six different temperatures (6, 9, 12, 15, 18 and 21 °C) under a 16:8 L:D light regime. Our results indicate that hatching of resting eggs of Daphnia that inhabit lakes or ponds may require different thermal conditions. The hatching success of ephippial eggs originating from temporary waters was relatively high (30–56%) at all tested incubation temperatures, while for the ephippial eggs from the deep lakes it was lower (7–37%) and inversely related to water temperature. The divergent hatching responses of the ephippial eggs originating from temporary pools and lakes may reflect the typical thermal conditions during hatching in their native habitats. While in the deep lakes of the temperate zone Daphnia hatching typically occurs during the low water temperatures of early spring, in shallow ponds Daphnia hatching may occur throughout the year at varying water temperatures, from a few to over a dozen degrees Celsius.     

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.     

To eat or not to eat infected food: a bug’s dilemma

Parasites can adversely affect host population densities, but predators can regulate disease by reducing the density of susceptible hosts and consuming parasites contained in infected hosts. Some parasites induce phenotypic modifications in their hosts that potentially lead to increased predation. We investigated the role of parasite-induced modified appearance in the interactions between the crustacean Daphnia magna, its bacterial parasite Pasteuria ramosa, and its predator, the backswimmer Anisops sp. Our aim was to test the backswimmer’s prey preference between infected and uninfected D. magna to find out whether infection by P. ramosa can affect predation risk by Anisops. We found that Anisops sp. had a strong preference for uninfected D. magna under light, but under dark conditions the preference was reversed, which suggests that the modified appearance is the cause of this preference. Such anti-parasite preference by Anisops sp. could strongly influence host population dynamics as loss of fecundity, disease mortality, and predation are additive, resulting in host population decline.     

Hatching of Daphnia sexual eggs. II. The effect of age and a second stimulus

• 1 We examined the effect of age on the hatching response of Daphnia magna sexual eggs of specific families. For old eggs (>2 years), hatching characteristics were compared at two storage temperatures (4°C and 20°C). Also, the hatching response after a second dark incubation and subsequent incubation under conditions favourable for hatching was compared with that after the first stimulus.
• 2 Daphnia sexual eggs were found to remain viable for several (at least 4.5) years. The effect of age on the hatching rate was family dependent. At least in some families, hatching rate was higher for old (>2 years) than for young (<5 months) eggs. Low temperature (4°C) during dark incubation resulted in a higher hatching rate compared with incubation at 20°C.
• 3 The application of a second hatching stimulus resulted in a renewed hatching response. The overall hatching rate after the second stimulus was, however, lower than that of the first stimulus.
• 4 More than 80% of the hatchlings of young eggs appeared on Day 3 or 4, with minor between-family differences in time distribution of hatching. The timing of the response to hatching stimuli was more variable in old than in young eggs, with the average time at hatching being 6.4 instead of 4.0 days. The response to the application of hatching stimuli was also slower after the second stimulus compared with the first stimulus.

     

Influence of temperature on hatching of eggs of Lepidurus couesii (Crustacea,Notostraca)

Tadpole shrimps (Notostraca) occur sporadically in temporary ponds and their survival there depends largely upon the drought-resistant eggs they produce. Environmental conditions conducive to hatching of eggs of Lepidurus couesii were investigated in the laboratory. Almost all eggs hatched best at 20 °C, whether desiccated for a short or long period, with a prior freezing shock or without such a shock, with intact shells. Eggs that endured a longer period of desiccation and eggs with abraded shells displayed a more equivocal response to different temperatures for hatching. Long-term hatchability of eggs was demonstrated. Time required for successful hatching was shortest at 20 °C, with no discernible difference between 17 °C and 25 °C. Both short- and long-term survival of populations of the species appears to be fostered by the adaptive response to temperature shown by the eggs.     

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     

Prevalence of kairomone-induced diapause in Daphnia magna from habitats with and without fish

The prevalence of the diapause response of the freshwater crustacean Daphnia magna to chemical cues on fish predation was evaluated in 35 clones originating from 14 European water bodies—inhabited or not inhabited by fish. Clonal lineages of experimental animals were cultured for 4 weeks in the presence or absence of water to which an extract of faeces of crucian carps (Carassius carassius), that were fed with Daphnia, was added. The proportion of females producing diapausing forms during the experimental period was used as a measure of the diapause response. A positive diapause response to fish predation cues was observed in 43% of investigated clones that originated from 71% of the water bodies tested. This indicated that the diapause response to fish scent is a common phenomenon in Daphnia magna from various locations in Europe. Surprisingly, no signs of a stronger diapause reaction to the tested cues were found in Daphnia originating from water bodies inhabited by fish compared with those from fish-free habitats.     

Rapid habituation by mosquito larvae to predator kairomones

Larvae of some species of mosquitoes have been shown to respond to water‐borne kairomones from predators by reducing bottom‐feeding and replacing it with surface filter‐feeding, which uses less movement and is thus less likely to attract a predator. However, if no predator attack takes place, then it would be more efficient to use a risk allocation strategy of habituating their response depending on the predator and the overall risk. The larvae of Culiseta longiareolata Macquart live in temporary rain‐filled pools, where they are exposed to a high level of predation. Within one hour, they responded to kairomones from dragonfly or damselfly nymphs, or to the fish Aphanius, by significantly reducing bottom‐feeding activity. Continued exposure to the predator kairomones resulted in habituation of their response to damselflies, a slower habituation to fish, but no habituation to dragonflies even after 30 h. In contrast, the larvae of Culex quinquefasciatus Say normally live in highly polluted and thus anaerobic water, where the predation risk will be much lower. They also showed a significant reduction in bottom‐feeding after 1 h of exposure to predator kairomones but had completely habituated this response within 6 h of continuous exposure. Some species of mosquito larvae can thus show a very rapid habituation to predator kairomones, while others only habituate slowly depending on the predator and overall predation risk.     

Predator regime influences innate anti-predator behaviour in the freshwater gastropod Lymnaea stagnalis

1. Predation incurs high fitness costs in aquatic organisms either through direct consumption or through avoidance responses that reduce time for activities such as feeding and reproduction. Hence, avoidance responses of aquatic organisms should vary to match closely the predation threat in their environment.
2. The freshwater gastropod Lymnaea stagnalis occurs in a variety of environments which vary in the presence or absence of predatory fish. We used naïve snails reared from six populations of this species experiencing different predator regimes (three co-occurring with molluscivorous fish and three without) to assess whether populations differed in the type and degree of their avoidance behaviours. Innate behavioural responses to four treatments (control, conspecific alarm cues, fish kairomones and fish kairomones paired with alarm cue) were compared in laboratory trials.
3. The primary anti-predator behaviour of L. stagnalis in response to fish kairomones was to crawl out of the water rather than seek refuge under water. This response was strongest when fish kairomones were paired with alarm cues, and varied depending on population origin; snails reared from populations co-occurring with predatory fish showed a stronger response than those raised from populations not experiencing such predators. In addition, populations co-occurring with predatory fish responded to the fish kairomones presented alone.
4. Our findings suggest that the degree of innate anti-predator behaviour shown by L. stagnalis , in terms of both the level of risk to which it responds and the degree of response, varies depending on the predator regime experienced by field populations. Together with previous work on cue association, this demonstrates that this gastropod is able to match its avoidance behaviour very closely to short and long term predation threats within its habitat.