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.     

Waterborne metals impair inducible defences in Daphnia pulex: morphology, life-history traits and encounters with predators

1.  Inducible defences may be temporary and favoured where predation is intermittent and have been demonstrated in several invertebrates and vertebrates when prey detect chemical cues (kairomones) released by predators. Daphnia pulex (a water flea) exposed to Chaoborus (midge larvae) kairomones produce small neckteeth on the dorsal surface of the head as a defence against this gape-limited predator and survive better in the presence of Chaoborus . Recent studies have shown that waterborne copper (Cu) impairs the induction of neckteeth which could lead to lower survival.
2.  Here, we examined the effects of Cu on morphological changes and shifts in life-history traits in D. pulex exposed to kairomone from Chaoborus americanus . We exposed D. pulex mothers to chemical cues of C. americanus fed on either D. pulex neonates or on brine shrimp Artemia salina , the same Chaoborus cues combined with an environmentally relevant concentration of copper (10 μg L⁻¹), or dechlorinated tap water. We examined several morphological characteristics of neonates and life-historical characteristics of adults as well as assessing survival of neonates by staging encounters with predators.
3.  Neonates from mothers exposed to kairomone plus copper had fewer and shorter neckteeth than neonates from mothers exposed to kairomone alone. Moreover, neonates exposed to Cu had lower survival during encounters with predators than neonates exposed to kairomone without Cu.
4.  Adult female Daphnia exposed to kairomones released more neonates within the first 24 h of brood release and emptied their brood pouches quicker than mothers not exposed to kairomones, irrespective of the presence of Cu.
5.  Impairment by metals of morphological defences in zooplankton could lead to a decline in population density and alter community structure.     

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.     

Embryology of Chaoborus-induced spines in Daphnia pulex

Daphnia pulex (Crustacea: Cladocera) embryos were found to be sensitive to a chemical cue (kairomone) in an extract of the predator Chaoborus americanus (Insecta:Diptera). Sensitivity of embryos to the kairomone remains throughout embryonic development. Apparently declining sensitivity as development proceeds may be due to the amount of time the embryos are exposed to the kairomone. Male embryos were also found to be sensitive to the kairomone. The smallest eggs within a brood produced small offspring, which showed the antipredator morphology to a significantly lower degree than largest eggs. The production of the neckteeth is described, at the developmental stage in the maturation of the Daphnia coinciding approximately with the escape of the embryos from the brood chamber.     

The effects of food and temperature regimes on life-history responses to fish kairomones in Daphnia hyalina × galeata*

Life-history responses to two concentrations of fish released info-chemicals at two temperature and food regimes were investigated for one clone of Daphnia hyalina × galeata. The presence of fish kairomones had a negative impact on size at maturity, carbon allocation to individual eggs and size of neonates in all treatments. Food concentration and temperature had positive effects on size of adult stages, independent of kairomone treatment. However, kairomone treatment were not found to interact with food or temperature. Age at maturity was positively influenced by increased temperature and food concentrations, whereas no direct kairomone effects were detected for this trait. Clutch size was not directly influenced by kairomone treatment, whereas both food concentration and temperature had strong, positive effects.     

Pesticides as chemical agents inducing helmet formation in Daphnia ambigua

SUMMARY. 1. Daphnia ambigua was exposed to harmful concentrations of pesticides (six insecticides, two herbicides, one fungicide) for 10 h from the final embryonic stage to the first instar, and effects on morphology were investigated.
2. The animals developed helmets at the second instar after exposure to the insecticides, but did not show the same response when exposed to the herbicides and the fungicide.
3. Some stimuli due to the insecticides on the nervous system of the animals may switch on the formation of the helmet, an antipredator morphology, which originally evolved as a response to chemicals released by predators.
4. It is suggested that a range of chemicals other than the predator/prey kairomone can induce the helmet formation in Daphnia .     

Does microcystin disrupt the induced effect of Daphnia kairomone on colony formation in Scenedesmus?

In natural aquatic system, Scenedesmus and Microcystis species usually coexist. Microcystins are released into water after lysis of Microcystis cells during the collapse of heavy blooms. The released toxins can then come into contact with a wide range of aquatic organisms. In this study, we used filtered Daphnia test water containing kairomone from Daphnia magna to stimulate the inducible colony formation in Scenedesmus obliquus under microcystin-contaminated system, to examine how microcystin affects the induced effect of Daphnia kairomone on colony formation in S. obliquus. The results showed neither microcystin nor Daphnia kairomone affected the growth of S. obliquus. Microcystin neither promoted nor impaired the overall Daphnia-induced colony formation in S. obliquus, except reducing the proportion of eight-celled colonies on day 2, indicating that the effect of microcystin was just short-term and in general did not disrupt grazer-induced colony formation of S. obliquus.     

Combined effect of the insecticide carbaryl and the Chaoborus kairomone on helmet development in Daphnia ambigua

The cladoceran Daphnia ambigua was exposed to both the insecticide carbaryl and the kairomone released from the predator Chaoborus simultaneously, and its morphological changes were analyzed. Daphnia developed helmets in response to the kairomone, but not in response to carbaryl at low (sublethal) concentrations (1–3 µg 1^–1). However, the carbaryl enhanced the development of high helmets and prolonged the maintenance period of the helmets over instars in the presence of the kairomone. These results suggest that sublethal concentrations of the insecticide alter predator-prey interactions by inducing helmet formation in Daphnia, which may reduce vulnerability of the Daphnia to predation.     

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.     

Swimming of Daphnia galeata x hyalina in response to changing light intensities: Influence of food availability and predator kairomone

Experiments showed that phototactic downward swimming in Daphnia galeata x hyalina as caused by a relative increase in light intensity (stimulus) is influenced by predator kairomone and food availability. The swimming responses at four different combinations of food availability and fish kairomone were analysed. Addition of both food and kairomone led to a significant increase in percentage of animals that responded to the light stimulus, but there was no significant interaction effect.We also found that kairomone and food had significant impact on displacement velocity and on the time between start of the stimulus and onset of the response.     

Variation in the neonate size of Daphnia pulex: the effects of predator exposure and clonal origin

Daphnia pulex clones originating from twelve small pond habitats were exposed to chemical cues from a size-selective predator, larvae of the phantom midge Chaoborus. Exposure delayed the onset of reproduction and increased the size at first reproduction. On the other hand, the neonates produced by these larger mothers were slightly smaller than the neonates produced by the smaller control mothers. In cladocerans, neonate size is usually positively correlated to the size of the mother. Thus exposure to Chaoborus kairomone apparently had direct effects on neonate size counterbalancing the maternal effects. Daphnia clones collected from Chaoborus-free and Chaoborus-rich environments exhibited different responses. In first adult instar, the clones from Chaoborus inhabited environments increased their offspring size under Chaoborus exposure whereas clones from Chaoborus-free environments did not. This may reflect clonal adaptation to the predation prehistory of their original habitat since larger neonates more quickly reach a size protected from the predator.     

Non-lethal effects of invertebrate predators on Daphnia: morphological and life-history consequences of water mite kairomone

1. Here, we report morphological and life-historical changes in the cladoceran Daphnia ambigua in response to chemical cues released by the predatory water mite Piona chilensis . Both species are common inhabitants of southern temperate lakes.
2. We found significant differences in adult body size at first, second and third reproduction. Also, individuals exposed to kairomones had longer tail spines at first reproduction, and the resultant offspring had smaller bodies and shorter tail spines.
3. Exposure to mite cues did not exert effects on brood size at first reproduction, but decreased offspring number in subsequent broods. Similarly, only the second and third reproduction events were delayed by kairomone exposure.
4. The intrinsic population growth rate of predator-induced animals was lower than that in controls, but simulations based on a parameterized matrix model showed that the fitness costs could be overcome if the reported phenotypic responses reduced predation rate moderately. The gain in protection from predators needed to cancel out the reduction in fitness associated with predator cues was directly related to juvenile survival and fertility, and inversely related to adult survival.
5. This is the first work reporting phenotypic plasticity in Cladocera in response to kairomones released by water mites, which are conspicuous predators in many austral fresh waters.     

Components of additive variance in life-history traits of Daphnia hyalina: seasonal differences in the response to predator signals

We attempted to separate the additive variance of life-history parameters (size at first reproduction (SFR), proportion of total production allocated to reproduction) of Daphnia hyalina in a mesotrophic lake during different seasons into genetic components and phenotypic plasticity. Every month we randomly isolated juveniles of 20 clones from the lake and measured their life-history parameters immediately after isolation, i.e., under the influence of all modifying factors in the lake. The measurements were repeated after the clones had been kept in the laboratory for at least six generations without predator signals (controls) and with the addition of fish and Chaoborus kairomones. SFR increased monotonously from July to December in fresh field isolates. Laboratory controls showed always much larger SFR, but approached field value in December. Most of the size difference was due to maternal effects. Reproductive allocation showed a different pattern than SFR with a minimum in September both in field samples and laboratory controls. Fish kairomone reduced SFR in July and August when fish predation is high, but not later in the year. On the contrary, Chaoborus kairomone increased SFR in September and October when Chaoborus larvae are abundant in the lake, but not in summer. This indicates a seasonal shift in the clonal composition of D. hyalina populations towards clones adapted to the specific predation pressure. Reproductive allocation changed in response to fish kairomone in July and August, but not in response to Chaoborus kairomone. In this mesotrophic lake, fish have a stronger direct and indirect impact on Daphnia life history than Chaoborus larvae.     

Multiple predator defence strategies in Daphnia pulex and their relation to native habitat

Daphnia may respond with an array of anti-predator defences(behavioural, morphological and life history) to a chemicalcue (kairomone) exuded by its predators: fish and Chaoborus.Given the wide array of potential responses, it is an interestingquestion whether anti-predator defences are coupled or independentof each other. Since anti-predator responses are costly andeven possessing the genetic information to respond to a certainpredator might involve a cost, clones may only react to predatorsthey co-occur with in nature. In this study, we provide evidencefor an uncoupling of responses by Daphnia pulex in several anti-predatordefences against Chaoborus. We were unable to detect a correlationbetween behavioural (migration), morphological (neck-spine induction)and life history [growth rate, neonate size and size at firstreproduction (SFR)] responses. Furthermore, anti-predator responsesdid not always comply with what is commonly believed. We foundthat Daphnia clones can migrate up or down when exposed to fishor Chaoborus kairomone and that population growth rate, neonatesize and SFR can increase or decrease in response to Chaoboruskairomone. We also show patterns in anti-predator defences thatseem to relate to the habitat from which clones were derived.Daphnia clones that were collected in habitats with Chaoborusas the dominant predator tended to react strongly to Chaoboruskairomone by migrating upward and producing neck-spines. Themigration behaviour against fish kairomone in these clones wasoften an unexpected upward migration. The Daphnia clone thatco-existed with fish predators showed a downward migration inthe presence of fish as well as Chaoborus kairomone. Clonesthat had occurred with either both or no predators had mixedresponses. We sometimes found an upward migration in combinationwith smaller body size as a response to Chaoborus kairomone.This may be interpreted as a behavioural defence against Chaoborusand a life-history defence against fish. Daphnia seem not toexhibit defence behaviour against predators they do not co-occurwith. It might be costly for Daphnia to maintain genetic informationto respond to these predators and protect that information fromgenetic drift.     

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.     

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.     

Progress towards characterization of a predator/prey kairomone: Daphnia pulex and Chaoborus americanus

Predatory larvae of the midge Chaoborus americanus induce an antipredator defense (neckteeth) in prey individuals of the cladoceran Daphnia pulex. The signal for presence of predator is a water-soluble chemical. We provide evidence that this kairomone originates in the intestinal tract of the predator. The active compound is an organic molecule of intermediate polarity which is heat stable and partially destroyed by acid and base digestion. It is stable to digestion by the general peptidase Pronase. Hydroxyl groups, but not primary amines, carbonyls or thiols are essential to activity. Low-pressure liquid chromatography on a reverse-phase silica gel (Amicon Matrex C-18) column suggests there may be more than one active component.     

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.      

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.