Inter-clonal variation in phototactic behaviour and key life-history traits in a metapopulation of the cyclical parthenogen Daphnia ambigua: the effect of fish kairomones

We quantified genetic variation for ecological relevant traits in the presence and the absence of fish chemicals of eleven Daphnia ambigua clones that were isolated from six interconnected ponds that differed in water transparency. In a cohort life table experiment, we tested whether genetic variation for a set of key life history traits was present among these clones. In addition the phototactic behaviour of these clones cultured in the presence and the absence of fish kairomones was quantified using a biotest. We detected a significant effect of fish kairomones on the phototactic behaviour and a highly significant genetic variation among clones for this trait in D. ambigua clones isolated from ponds in De Maten. Differences in size at maturity among D. ambigua clones in De Maten were highly significant, whereas differences in spina length among D. ambigua clones in De Maten were not significant. The presence of fish chemicals did not affect the studied life-history traits. We observed a significant positive relationship between average phototactic behaviour for each population and size at maturity both in the presence as in the absence of fish kairomones. Most of the genetic differences could be attributed to a clone isolated from one clearwater pond that is not directly connected to the remainder of the pond complex.     

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.     

Vertical distribution of Chlamydomonas changes in response to grazer and predator kairomones

Individuals in aquatic communities frequently assess their biotic environment through infochemicals. In particular, kairomones are commonly involved in interactions between predator and prey. However, the relationship between individuals and chemicals produced by other organisms that are not direct predators, but may indicate the presence of a predator, is not well characterized. We used experimental microcosms to test whether the unicellular green alga Chlamydomonas reinhardtii alters vertical migration patterns in response to kairomones produced by zooplankton ( Daphnia ) and planktivores (fish). Our results suggested that phototaxis in C. reinhardtii was strongly affected by the type of kairomone present, the concentration of the kairomone, and the duration of exposure to the kairomone. Kairomones generally increased phototaxis in C. reinhardtii . The adaptive significance of such behavioral changes in natural settings would depend largely on local community composition. The similarity in phototactic responses of C. reinhardtii to Daphnia and fish kairomone suggest that, in at least this species of phytoplankton, the underlying genetic elements responsible for kairomone detection may be responsive to a broad range of chemical stimuli, allowing this species to adjust its phototaxis in response to not only the presence of its grazers, but also to predators of its grazers.     

Temperature effects on chemical signalling in a predator–prey system

SUMMARY 1. We investigated the effect of temperature on chemical signalling in a predator–prey model system (planktivorous fish and Daphnia galeata ). Life-history changes in Daphnia in response to chemical cues (kairomones) derived from fish have become a paradigm for chemically induced anti-predator defences.
2. As temperature can affect both predator and prey, we carried out two experiments to disentangle these effects. In order to test for temperature effects on the predator, we kept prey at a single temperature and exposed them to kairomones from fish exposed to two different temperatures. Daphnia exhibited a higher intrinsic rate of population increase ( r ) when exposed to fish kairomones produced at high rather than low temperature. Assuming a positive correlation between r (because of an earlier maturation and/or increased clutch sizes) and kairomone concentration, our results suggest that kairomone production increases with rising temperature.
3. In the second experiment, to study the influence of temperature on the prey, Daphnia were kept at two different temperatures and exposed to fish kairomones produced at one constant temperature. We found no interaction between the effects of fish kairomone and temperature on Daphnia life history, suggesting that temperature does not directly alter life-history responses to fish kairomones.
4. Our results suggest that temperature influences Daphnia life history through its effects on fish kairomone concentration, but that temperature does not affect the strength of the response of Daphnia to the presence of fish.     

Predator-mediated plasticity in morphology, life history, and behavior of Daphnia: the uncoupling of responses

We studied the way 12 traits responded to fish kairomones in a set of 16 Daphnia magna clones derived from four different habitats-two where daphnids co-occur with fish and two without fish. These clones differed widely in their response to predator kairomones, with none of the clones showing a significant response in all traits and all clones showing a response for at least one trait. Most of the clones showed a significant response in one to four traits, with no evidence for an association between different traits. Clones from fish habitats were slightly more responsive to the presence of fish kairomones than clones from fishless locations. We conclude that most clones show an induced response to the presence of their predators (fish) but that there is a large genetic variability with respect to the traits for which clones show a response. Our results indicate that the major distinction is not between inducible and noninducible genotypes but rather that the genotypes differ in the combination of traits for which they show inducible responses.     

Differential life history responses of several pelagic Daphnia clones differing in migratory behaviour

Females of the hybrid Daphnia galeata × hyalina were isolated from a natural population in Lake Maarsseveen and from these individuals clones were cultured in the laboratory. Some clones were assumed to be migrating and some non-migrating. Life history experiments were performed with these clones in the presence and absence of fish kairomones. Results show that clones differed in life history strategy in concert with their presumed migration strategies which suggests a link between life history and behaviour. However, no sharp border exists between migrating and non-migrating clones since a gradual response pattern was found for the traits investigated. In the absence of fish kairomones, the relation between length at maturity and number of eggs was found to differ between the clones of the non-migrating and the migrating group. The latter had a lower number of eggs at similar length values. In the presence of fish kairomones, the length–clutch size relation was the same. However, non-migrating clones were smaller at the age at maturity and had fewer eggs. Although clones of both groups were thus found to differ significantly, overlap existed. Age at maturity was found to be the same.     

Tail spine length in the Daphnia galeata complex: costs and benefits of induction by fish

We studied the combined effect of fish kairomones and food conditions on the relative tail spine length (RTL) of five Daphnia taxa, and the interaction of these factors with the vertical distribution of the daphnids. The experiment was done in two large-scale indoor containers, the so-called plankton towers in Plön, Germany. We conducted a competition experiment in which food level and the presence of fish chemicals and later fish were varied. A strong response of RTL to fish kairomones (e.g., longer tail spines), significant differences in RTL between species, but no differences in RTL with water depth were found. Further, we observed that these Daphnia taxa produced a higher RTL only under high food conditions. This suggests that there is a cost related to the production of longer tail spines.In a preliminary study in lake Plußsee, we found that Daphnia had longer average RTL than in the towers. Further, we noted significant differences in RTL between the two sampling dates, which may be related to a lower food level. We also detected a strong inverse correlation between RTL and depth. We discuss the implications of these findings for the co-existence of co-occurring Daphnia species and their hybrids.     

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.     

Predator-induced life-history changes and the coexistence of five taxa in a Daphnia species complex

Interspecific hybridization is common in water fleas of the Daphnia galeata species complex (e.g. D. galeata , D. cucullata , D. hyalina and their interspecific hybrids). We studied the effect of fish on the life histories of five taxa of this species complex originating from the Plußsee, northern Germany. Using four clones per taxon, we found that fish kairomones reduce size at birth and size at maturity significantly. For size at maturity larger taxa showed a significantly stronger reaction to fish kairomones than the smaller taxa. With respect to the intrinsic rate of increase, r , we compared two predation regimes (positive size selective and not selective). We found that under the fish predation regime most clones had a higher r when cultured with fish kairomones, leading to a higher r , and a stronger reaction for the smaller taxa. We conclude that fish predation might be an important factor influencing the co-occurrence of Daphnia parental taxa with their hybrids.     

Interactions Between Predator Kairomone and Food Level Complicate the Ecological Interpretation of Daphnia Laboratory Results

The effect of food concentration on the phenotypic responseof life history traits to two predator kairomones was investigatedin Daphnia. For the experiment, one clone of Daphnia galeatawas used as the prey organism and solutions containing infochemicals(kairomones) of Chaoborus (phantommidge) and Perca (perch) simulatedthe presence of potential predators. The combined effect offood level and predator kairomone on phenotypic plasticity ofDaphnia life history is complex. At low food levels, the responsesin life history traits to kairomones are enhanced. For example,in the Perca treatment, this leads to a younger age at firstreproduction. The presence of Chaoborus kairomone decreasessurvival so that death often occurs before reproduction is reached.This results in a strong decrease in the intrinsic rate of populationincrease and might contribut to the pronounced summer declineof some Daphnia populations during periods of food shortage.     

The influence of food quality on the phototactic behaviour of Daphnia magnaStraus

We examined the influence of food quality on the phototactic behaviour of Daphnia magna. Cohorts of a positively phototactic D. magna clone were fed nine diets differing in quality. Diets were obtained by substitution of a fraction of unicellular algae ( Scenedesmus acutus) by a biomass-equivalent of fresh yeast ( Saccharomyces cerevisiae). Some of the diets were enriched with an inoculum of ciliates and organic compounds added as a hay infusion filtrate. Animals fed with a diet containing at least 25% algae showed a similar phototactic behaviour as animals fed with a diet that contained 100% algae. Addition of ciliates to the yeast diets resulted in a lower mortality and a higher reproductive rate compared to diets without a ciliate supplement. The presence of ciliates did not influence phototactic behaviour. Experiments testing for a maternal effect showed that the phototactic behaviour of the animals was strongly influenced by diet during the early developmental stages, but was not influenced by the diet of the mother. This revised version was published online in July 2006 with corrections to the Cover Date.     

The combined effects of hypoxia and fish kairomones on several physiological and life history traits of Daphnia

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Effects of neonate size and food concentration on the life history responses of a clone of the hybrid Daphnia hyalina × galeata to fish kairomones

1. The influence of fish kairomones on the life history parameters of a clone of the hybrid Daphnia galeata × hyalina was measured in laboratory experiments with small and large neonates at one food concentration. The influence of fish kairomones on neonates of the same size at two food concentrations was also investigated.
2. Neonate size (maternal investment per egg) changed the influence of fish kairomones on life history parameters. Daphnids that were small at birth showed greater differences between fish (kairomones present) and no-fish (kairomones absent) treatments for age at maturity and number of eggs in the first clutch than animals that were large at birth. On the other hand, animals that were large at birth differed more in size at maturity between fish and no-fish treatments than small neonates.
3. The food concentrations used in the experiments (0.25–0.75 mg C l^–1) hardly affected the influence of fish kairomones on the life history characteristics studied.
4. The effect of fish kairomones on the size of neonates from the first clutch was similar for large and small daphnids. In the no-fish treatment significant differences were found between small and large neonates for age at maturity and number of eggs in the first clutch. In the fish treatment size at maturity differed significantly between small and large neonates.
5. In life history experiments, neonate size has to be taken into account when measuring the effects of fish kairomones because size at birth influences the results.     

Effects of neonate size and food concentration on the life history responses of a clone of the hybrid Daphnia hyalina × galeata to fish kairomones

1. The influence of fish kairomones on the life history parameters of a clone of the hybrid Daphnia galeata × hyalina was measured in laboratory experiments with small and large neonates at one food concentration. The influence of fish kairomones on neonates of the same size at two food concentrations was also investigated.
2. Neonate size (maternal investment per egg) changed the influence of fish kairomones on life history parameters. Daphnids that were small at birth showed greater differences between fish (kairomones present) and no-fish (kairomones absent) treatments for age at maturity and number of eggs in the first clutch than animals that were large at birth. On the other hand, animals that were large at birth differed more in size at maturity between fish and no-fish treatments than small neonates.
3. The food concentrations used in the experiments (0.25–0.75 mg C l^–1) hardly affected the influence of fish kairomones on the life history characteristics studied.
4. The effect of fish kairomones on the size of neonates from the first clutch was similar for large and small daphnids. In the no-fish treatment significant differences were found between small and large neonates for age at maturity and number of eggs in the first clutch. In the fish treatment size at maturity differed significantly between small and large neonates.
5. In life history experiments, neonate size has to be taken into account when measuring the effects of fish kairomones because size at birth influences the results.     

Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi

1. The exotic cladoceran Daphnia lumholtzi has recently invaded freshwater systems throughout the United States. Daphnia lumholtzi possesses extravagant head spines that are longer than those found on any other North American Daphnia. These spines are effective at reducing predation from many of the predators that are native to newly invaded habitats; however, they are plastic both in nature and in laboratory cultures. The purpose of this experiment was to better understand what environmental cues induce and maintain these effective predator‐deterrent spines. We conducted life‐table experiments on individual D. lumholtzi grown in water conditioned with an invertebrate insect predator, Chaoborus punctipennis, and water conditioned with a vertebrate fish predator, Lepomis macrochirus. 2. Daphnia lumholtzi exhibited morphological plasticity in response to kairomones released by both predators. However, direct exposure to predator kairomones during postembryonic development did not induce long spines in D. lumholtzi. In contrast, neonates produced from individuals exposed to Lepomis kairomones had significantly longer head and tail spines than neonates produced from control and Chaoborus individuals. These results suggest that there may be a maternal, or pre‐embryonic, effect of kairomone exposure on spine development in D. lumholtzi. 3. Independent of these morphological shifts, D. lumholtzi also exhibited plasticity in life history characteristics in response to predator kairomones. For example, D. lumholtzi exhibited delayed reproduction in response to Chaoborus kairomones, and significantly more individuals produced resting eggs, or ephippia, in the presence of Lepomis kairomones.     

Life history shifts in response to different levels of fish kairomones in Daphnia

Life history parameters, such as age and size at maturity, neonatesize and number of eggs in the first clutch, of a clone of thehybrid Daphnia galeata x hyalina were determined at six levelsof fish kairomones. It was found that the age and size at maturitydecreased gradually with increasing kairomone level, while thenumber of eggs in the first clutch increased linearly. At thesame time, neonate size decreased linearly with increasing kairomonelevel. In a starvation experiment, newly born neonates of mothersnot cultivated in the presence of kairomones survived the longest.These results show that Daphnia is able to adjust its life historytraits to different levels of kairomones, and thus to differentfish densities.     

Relationship between fish kairomone concentration in a lake and phototactic swimming by Daphnia

Light-induced swimming behaviour of Daphnia can lead to dielvertical migration. When this occurs, Daphnia may escape frompredation by juvenile 0+ fish. For this to happen, swimmingin response to the change in light intensity at dawn and duskmust be enhanced. This enhanced swimming reaction can be elicitedby fish-associated kairomone in the laboratory. We studied theeffect of these fish-associated kairomones in Lake Maarsseveen,The Netherlands. A bioassay was conducted in which light-inducedswimming reactions of Daphnia were used to quantify the kairomonesignal strength. In two successive years, 1998 and 1999, waterfrom Lake Maarsseveen was tested weekly in early summer. Sampleswere taken from the epilimnion at 3 m depth and from the hypolimnionat 15 m depth. Simultaneously, we caught 0+ perch (Perca fluviatilis)with bongo nets to determine its abundance. The length and weightof individuals caught in 1998 were determined to establish alength–weight relationship. Using this relationship andthe information on perch density from the trawls, the relativefish biomass was calculated for these two years. It was shownthat water from the epilimnion layer increasingly enhanced light-inducedswimming reactions until the second week of June, then the effectgradually disappeared. Water from the hypolimnion had no sucheffect. In 1998, these changes in signal strength correlatedwith the relative biomass of the 0+ perch, but in 1999, themaximum of the enhancement lagged 2 weeks behind the maximumof the biomass of the 0+ perch. This lag may be due to a differentdevelopment of the thermocline. We conclude that kairomone concentrationmay well correlate with 0+ perch biomass and thereby might informDaphnia not only about the presence, but also about the abundance,of juvenile perch.     

Effect of vertebrate and invertebrate kairomones on the life history of Daphnia magna Straus (Crustacea: Branchiopoda)

The history of selection of Daphnia magna populations living in North African temporary ponds may differ from populations inhabiting permanent ponds. Laboratory experiments were conducted to examine the effect of fish Gambusia holbrooki and invertebrate Notonecta glauca kairomones on the life history traits of the freshwater Cladocera Daphnia magna Straus. With fish kairomones, Daphnia reproduced early and had a significantly smaller size at first reproduction (SFR) and a smaller size of neonates compared to control. In contrast, daphnids reared in water treated with Notonecta glauca had no effect on the age at first reproduction but females were also smaller and produced smaller neonates.     

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.