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.     

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.     

Chaoborus and gasterosteus anti-predator responses in Daphnia pulex are mediated by independent cholinergic and gabaergic neuronal signals

Many prey species evolved inducible defense strategies that protect effectively against predation threats. Especially the crustacean Daphnia emerged as a model system for studying the ecology and evolution of inducible defenses. Daphnia pulex e.g. shows different phenotypic adaptations against vertebrate and invertebrate predators. In response to the invertebrate phantom midge larvae Chaoborus (Diptera) D. pulex develops defensive morphological defenses (neckteeth). Cues originating from predatory fish result in life history changes in which resources are allocated from somatic growth to reproduction. While there are hints that responses against Chaoborus cues are transmitted involving cholinergic neuronal pathways, nothing is known about the neurophysiology underlying the transmission of fish related cues. We investigated the neurophysiological basis underlying the activation of inducible defenses in D. pulex using induction assays with the invertebrate predator Chaoborus and the three-spined stickleback Gasterosteus aculeatus. Predator-specific cues were combined with neuro-effective substances that stimulated or inhibited the cholinergic and gabaergic nervous system. We show that cholinergic-dependent pathways are involved in the perception and transmission of Chaoborus cues, while GABA was not involved. Thus, the cholinergic nervous system independently mediates the development of morphological defenses in response to Chaoborus cues. In contrast, only the inhibitory effect of GABA significantly influence fish-induced life history changes, while the application of cholinergic stimulants had no effect in combination with fish related cues. Our results show that cholinergic stimulation mediates signal transmission of Chaoborus cues leading to morphological defenses. Fish cues, which are responsible for predator-specific life history adaptations involve gabaergic control. Our study shows that both pathways are independent and thus potentially allow for adjustment of responses to variable predation regimes.     

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.     

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.     

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.     

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.     

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.     

UV radiation affects antipredatory defense traits in Daphnia pulex

In aquatic environments, prey perceive predator threats by chemical cues called kairomones, which can induce changes in their morphology, life histories, and behavior. Predator‐induced defenses have allowed for prey, such as Daphnia pulex, to avert capture by common invertebrate predators, such as Chaoborus sp. larvae. However, the influence of additional stressors, such as ultraviolet radiation (UVR), on the Daphnia–Chaoborus interaction is not settled as UVR may for instance deactivate the kairomone. In laboratory experiments, we investigated the combined effect of kairomones and UVR at ecologically relevant levels on induced morphological defenses of two D. pulex clones. We found that kairomones were not deactivated by UVR exposure. Instead, UVR exposure suppressed induced morphological defense traits of D. pulex juveniles under predation threat by generally decreasing the number of neckteeth and especially by decreasing the size of the pedestal beneath the neckteeth. UVR exposure also decreased the body length, body width, and tail spine length of juveniles, likely additionally increasing the vulnerability to Chaoborus predation. Our results suggest potential detrimental effects on fitness and survival of D. pulex subject to UVR stress, with consequences on community composition and food web structure in clear and shallow water bodies.     

Predation by chaoborids on typical and spined Daphnia pulex

SUMMARY. 1. In laboratory predation experiments, predation rates were determined for fourth-instar larvae of the chaoborids (Insecta: Diptera) Mochlonyx sp. and Chaoborus americanus preying on four juvenile instars and adult Daphnia pulex (clone SBL). In the case of Mochlonyx , predation was most intense on second-instar juvenile Daphnia while Chaoborus preyed equally on second and third instars.
2. Mochlonyx and Chaoborus induced an antipredator defence (neck-teeth) which was most frequently expressed in second-instar juvenile Daphnia . Expression of this antipredator phenotype was correlated with a reduced rate of Mochlonyx predation.     

Implications of Chaoborus pupation and ecdysis in cold water

1. Cold water acted differently to delay and lengthen the pupation period for the larvae of two species of the zooplankton predator Chaoborus (Diptera: Chaoboridae). During Chaoborus pupation, the zooplankton community is released from predation, while the dark-coloured Chaoborus pupae are more susceptible to their own predators.
2. Fourth instar larvae of Chaoborus americanus and C. trivittatus , collected from an oligotrophic lake, were reared individually at 5 °C in the dark. Chaoborus americanus was also reared at 9 and 12 °C under spring photoperiod conditions (L : D, 16 : 8 h). Individuals were observed through pupation to emergence (ecdysis) or death.
3.  Chaoborus americanus pupated at 5, 9 and 12 °C with substantial emergence only at 12 °C. In comparison, C. trivittatus emerged at 5 °C. Light was not a necessary cue for pupation and ecdysis, contrary to previous reports. Cold water delayed the onset and lengthened and increased the variability of the duration of pupation.
4. In Shirley Lake, C. americanus pupated in late June–early July while C. trivittatus pupated first in April and again in June–July.
5.  Chaoborus americanus pupae needed a temperature cue to complete ecdysis. The ecdysis temperature threshold helps to explain the difference in pupation timing, and the geographical distribution, of C. americanus and its relatively inflexible life history contrasted with C. trivittatus . Delayed predator pupation in years with low spring temperature can affect the community dynamics of the prey.     

The supposed lack of trade-off among Daphnia galeata life history traits is explained by increased adult mortality in Chaoborus conditioned treatments

In recent years, some studies addressing the modification of phenotypically plastic traits of Daphnia in the presence of chemical cues (kairomones) from invertebrate predators have reported a lack of trade-off among resource allocation of traditional life history traits (growth and reproduction) (Spitze, 1991; Black, 1993; Weber & Declerck, 1997). In this study, we term this finding the `Chaoborus paradox'. The Chaoborus paradox contrasts with the generally accepted theory that facultative changes in life history traits are associated with costs or a modification in resource allocation. In order to unravel the Chaoborus paradox, we have tested four groups of traits that may explain resource allocation. These were (1) the trade-off between present and future reproduction, (2) reduced growth of morphological features (body length, helmet length, spine length, carapace width) prior to maturity (pre-maturity) or (3) during the first adult instar (at maturity), and (4) an increase in feeding and assimilation rates to fuel the amount of resources available to the organism. As experimental animal we used Daphnia galeata (Cladocera) and to simulate invertebrate predation we used the Chaoborus (phantom midge larvae) kairomone. A clear trade-off existed between present and future reproduction. Survival was less in the presence of Chaoborus kairomone and therefore more resources could be channelled into growth and reproduction early in life at the cost of dying younger when compared to control animals. The other groups of traits (reduced growth of morphological features and an increase the amount of resources) offer partial solutions to the Chaoborus paradox for single clones only and not for the whole population.     

Ecology of predator-induced morphological defense traits in Daphnia longispina (Cladocera,Arthropoda)

Oecologia - Inducible defenses against predators are widespread among plants and animals. For example, some Daphnia species form neckteeth against predatory larvae of the dipteran genus Chaoborus....     

Predation risk perception and food scarcity induce alterations of life-cycle traits of the mosquito Culex pipiens

Abstract.  1. Predators may affect prey populations by direct consumption, and by inducing defensive reactions of prey to the predation risk. Food scarcity frequently has effects on the inducible defences of prey, but no consistent pattern of food–predation risk interaction is known.
2. In this study the combined effect of food shortage and predation-risk perception in larvae of the mosquito Culex pipiens was investigated. Water exposed to the aquatic predator bug Notonecta glauca was used as a source of predation intimidation. Mosquito larvae were reared in three different media containing either no predator cues or the cues of N. glauca that had been fed on either C. pipiens larvae or on Daphnia magna . Food was provided in favourable or limited amount for these set-ups.
3. The results showed that chemical cues from the predators fed with prey's conspecifics caused a decreased survival, delayed pre-imaginal development, and reduction in body size of emerged mosquitoes, whereas chemical cues from predators fed with D. magna caused only delayed development. Food scarcity significantly exacerbates the negative effect of the predator cues on pre-imaginal development of C. pipiens . Effects of the cues on larval development and body size of imagoes are significantly stronger for females than for males.
4. The present study suggests that when food is limited, predators can affect population dynamics of prey not only by direct predation, but also by inducing lethal and sublethal effects due to perception of risk imposed by chemical cues. To understand the effects of predators on mosquito population dynamics, environmental parameters such as food deficiency should be considered.     

Morphological responses of four species of cyclomorphic Daphnia to a short-term exposure to the insecticide carbaryl

Four species of cyclomorphic Daphnia (D.pulex, D.galeata mendotae,D.retrocurva, D.lumholtzi) were exposed to the insecticide carbarylfor a short term (8–4 h) from the final embryonic stageto the first instar. Daphnia pulex formed neckteeth, and theremaining three Daphnia species developed high helmets and longtailspines. The results suggest that the development of suchprotuberant structures (anti-predator morphologies) in responseto the insecticide exposure is a general phenomenon in Daphnia,and that stimuli on the nervous system of Daphnia may inducethe morphological changes, which originally evolved as a responseto predator kairomone. Two clones of D.pulcx were examined anda clone which was more sensitive to the predator Chaobonts kairomonethan another developed more marked neckteeth in response tocarbaryl, suggesting that the sensitivity in morphological responseto the insecticide may be related to the sensitivity to thekairomone. ¹Present and permanent address: Regional Environment Division,National Institute for Environmental Studies Onogawa, Tsukuba,Ibaraki 305, Japan     

Cyclomorphosis in Daphnia galeata mendotae Birge and D. retrocurva Forbes as a predator-induced response

SUMMARY. 1. Populations of Daphnia galeata mendotae and D. retrocurva were exposed for one generation to predators enclosed in mesh bags. The exposed Daphnia showed adaptive morphological changes that mimic cyclomorphosis in nature. The invertebrate predators Chaoborus and Notonecta induced longer helmets, while the fish Lepomis induced shorter bodies but had no effect on helmet length. Longer tail spines (relative to body length) were induced by Notonecta and Lepomis.
2. The responses of D. retrocurva were influenced by algae concentration, with the more extreme responses occurring at a higher food concentration and higher lipid index.     

Phenotypic plasticity of Daphnia life history traits: the roles of predation, food level and toxic cyanobacteria

1. We studied the life history responses of Daphnia pulex under different biotic conditions. In a factorially designed experiment, we tested the impacts of water conditioned by the invertebrate predator Chaoborus, low and high food level (10 000 and 100 000 Scenedesmus cells ml^–1), and exposure to toxic Microcystis (5000 cells ml^–1) on twelve D. pulex clones originating from different habitats. Our aim was to compare the phenotypic plasticity of different clones, and to study the interactions among biotic factors.
2. Individuals cultured in Chaoborus -conditioned water started to reproduce at a larger size than individuals cultured in water not conditioned by the predators. We found interactions between food level and Chaoborus -conditioned water on age at first reproduction and total offspring number. In addition, the impact of the Chaoborus treatment on the size at first reproduction was reduced by Microcystis exposure.
3. Clonal differences were found in the degree of phenotypic plasticity of different life history traits. However, there was no obvious connection between the original habitat of the clone and the degree of plasticity.     

Inducible defences in Daphnia: responses to two closely related predator species

The predator-induced responses of two species of Australian Daphnia, with contrasting distributions and life history patterns, to the kairomones of two species of Anisops predators, were measured. Daphnia longicephala produced a large crest and attained a larger size when exposed to both predators. D. carinata sl matured earlier than D. longicephala and did not produce a crest. Surprisingly, kairomones of both predators inhibited the production of ephippia in D. carinata sl. Anisops stali, the larger of the two predator species, induced a significantly larger crest size in D. longicephala, and larger brood size in both species compared with the smaller A. gratus, indicating a quantitative but not qualitative effect of predator species on inducible defences. Received: 18 August 1999 / Accepted: 14 April 2000     

Reduced investment in sex as a cost of inducible defence in Brachionus calyciflorus (Rotifera)

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Complex effects of a kairomone of Chaoborus and an insecticide on Daphnia pulex

Daphnia pulex were reared in Chaoborus-conditioned water containingthe insecticide carbaryl, and their life history parametersand morphologies were investigated. The insecticide inhibitedthe animals' growth and reproduction and delayed their maturationtime more intensely in the chaoborus-conditioned water thanin the control Chaoborus-free water, indicating that a kairomoneof Chaoborus made the Daphnia more sensitive to the insecticide.The Chaoborus conditioned water induced neckteeth formationof D.pulex in instars 1–2 and elongated the intermoultingperiod of juveniles. The moulting to the spined morphs and elongationin duration of juvenile stages seemed to increase the risk ofdamage from the insecticide. The potential population growthrate of D.pulex in treatments was estimated as a possible fitnessindicator of the animals. It was reduced synergistically bythe kairomone of Chaoborus and the insecticide. Some individualskept neckteeth until the third or fourth instar stage when theywere exposed to sublethal concentrations of the insecticidein the Chaoborus-conditioned water. This was considered as aresult of synergistic effects of both the kairomone and theinsecticide. Insecticides may be a factor inducing further developmentof protuberant structures in cyclomorphic Daphnia in naturalwater bodies.