The ecological role of chemical stimuli for the zooplankton: predator-induced morphology in Daphnia

Summary Numerous adaptive predator-induced responses occurred when eight clones representing seven Daphnia (Crustacea: Cladocera) species were tested against three common predators: fourth instar larval phantom midge Chaoborus americanus, adult backswimmer Notonecta undulata, and small sunfish Lepomis macrochirus. The predators were confined within small mesh bags, suggesting that the signal for induction is chemical. The induced responses included longer tail spines, longer heads, smaller bodies, increased egg clutches, and decreased lipid reserves. Each Daphnia species responded to each of the three predators in a unique manner. Induced responses in the above characters showed no significant association. The induced morphological changes are generally consistent with current theories of what is an adaptive response for the various sizes of Daphnia exposed to tactile and visual predators. The abundance of induced responses in these experiments suggests that predator-induced responses are a widespread and ecologically important phenomenon of the freshwater zooplankton.     

Habitat segregation and interactive effects of multiple predators on a prey assemblage

1. In a field experiment we examined the interactive effects of two common predators of zooplankton, bluegill sunfish (Lepomis macrochirus) and Chaoborus spp. on the growth rate and habitat use of three congeneric prey species (Daphnia). Bluegill and Chaoborus both consume Daphnia, but bluegill also prey on Chaoborus. The prey species, Daphnia pulicaria, D. rosea and D. retrocurva, differed in body size and vertical distribution. We expected the largest species, D. pulicaria, to be most vulnerable to fish predation and the smallest species, D. retrocurva, to be most vulnerable to Chaoborus predation. 2. As we expected, the population growth rate of D. pulicaria was significantly reduced by fish. However, Chaoborus also significantly reduced the growth rate of this species. No significant interaction effect was detected, indicating that the effect of these predators was additive. The growth rates of D. rosea and D. retrocurva were significantly reduced by Chaoborus, but a significant interaction effect indicated that the effect of Chaoborus was stronger in the absence of fish than when fish were present. Therefore the impact of Chaoborus and fish on D. rosea and D. retrocurva was non-additive. The interactive effect of the two predators on D. retrocurva was greater in magnitude than on D. rosea. 3. In the absence of predators, the three Daphnia species showed no differences in mean habitat depth between day and night. Both predators significantly affected diel habitat use of D. pulicaria and D. rosea. Fish caused both of these Daphnia species to move deeper during the day, whereas Chaoborus caused Daphnia to move into shallower water at night. Daphnia retrocurva tended to migrate upwards at night in all predator treatments, but no significant differences in migration were observed among the predator treatments. The effects of predators on habitat use were not interactive for any prey species. 4. Our results suggest that body size, habitat use and the diel migratory response to predators are important factors mediating the interactive effects of multiple predator types on zooplankton.     

Inducible defences in Daphnia depend on latent alarm signals from conspecific prey activated in predators

Some water fleas (Daphnia spp.) undergo phenotypic changes when exposed to chemical signals from predators. The chemical signals have been assumed to be of predator origin (i.e. kairomones), since juices of crushed Daphnia have been found ineffective. We speculated that latent alarm signals could be present in Daphnia, to be activated in predators following ingestion. Accordingly, fish predators were fed earthworms for 10 weeks to remove Daphnia remains from their gastro-intestinal tracts. Following another 6 days of earthworm feeding, water conditioned by fish induced no morphological changes in D. galeata. When fish were alternatively fed Daphnia for 6 days, changes were induced with fish-conditioned water. Extracts made from intestines of earthworm-fed fish, homogenized with earthworms, gave no morphological changes, but intestines of the same origin homogenized with Daphnia did. Similar results were found when earthworms and Daphnia were homogenized with fish liver. Freshly frozen extracts of homogenized Daphnia gave no detectable changes at first instar stage in test animals, whereas extracts of Daphnia that had been kept at room temperature did induce such changes. Our results suggest that Daphnia respond to latent conspecific alarm signals (i.e. 'dormant' pheromones) that are activated by intestinal or bacterial enzymes in predators or in the water.     

Trophic interactions in rockpool food webs: regulation of zooplankton and phytoplankton by Notonecta and Daphnia

We studied trophic interactions in experimental rockpools with three different food web structures: phytoplankton and small-bodied zooplankton; phytoplankton, small-bodied zooplankton and Daphnia ; and phytoplankton, small-bodied zooplankton, Daphnia and Notonecta . Nutrients, primary productivity, chlorophyll a and zooplankton species composition and biomass were measured over eight weeks.
2. Daphnia had a negative impact on other zooplankton and reduced the phytoplankton biomass and primary productivity. In the absence of Daphnia , small-bodied zooplankton species were abundant, in particular cyclopoid copepods. Concentrations of dissolved nutrients were lower and the standing crop of primary producers was higher when Daphnia was absent.
3. The presence of the invertebrate predator Notonecta produced a top-down effect which was similar to that reported for planktivorous fish, i.e. a selective reduction of daphnids followed by an increase of small-bodied zooplankton species and phytoplankton biomass.
4. The study showed that consumer regulation of Daphnia by Notonecta and of algae by Daphnia are important, but also demonstrated that trophic level biomasses were controlled by a combination of predation and resource limitation.     

Environmental correlates of the intrinsic rate of natural increase in primates

Morphological and life history traits of two clones of the cladoceran Daphnia pulex were measured in the presence and absence of size-selective insect predators, the midge larva Chaoborus flavicans, which preys on small Daphnia, and the water bug Notonecta glauca, which preys on large Daphnia. The aim was to detect predator-induced phenotypic changes, particularly the effect of simultaneous exposure to both types of predators. Other work has shown that in the presence of Chaoborus americanus, Daphnia pulex produce a socalled neck spine which may carry several teeth. The morphological modifications are supposed to serve as an anti-predator device. Furthermore, females exposed to Chaoborus often delay their maturation; this has been interpreted as a cost that balances the benefits of the neck teeth. In this investigation, females of both clones produced fewer but larger offspring than control animals when reared in the presence of Chaoborus flavicans. The offspring showed the typical neck spine and delayed first reproduction. In the presence of Notonecta glauca, one of the clones produced more and smaller offspring, and maturation occurred at earlier instars. The other clone also produced more offspring than the control but there was no size difference. When both predators were present, in most cases the reactions of the daphnids were similar to those in the Notonecta experiment. The response to Chaoborus appeared to be suppressed. The observed modifications are interpreted as evolved strategies that reduce the impact of size-selective predation. They are consistent with predictions of life-history theory.     

Fish-induced life-history shifts in the cladocerans Daphnia and Simocephalus: are they positive or negative responses?

The cladocerans Daphnia and Simocephalus were exposed to fishsmells under different food conditions, and their life-historyparameters were analysed. They showed similar responses to fishsmells and food shortage: lowered juvenile growth rate, reducedmature size, elongated maturation time, reduced brood size andincreased offspring size. The life-history changes induced bythe fish smell might be a result of deleterious effects of thefactor. Although it has been considered that fish-induced life-historyshifts in Daphnia are positive responses to predators, our resultssuggest that they are negative responses of animals that showsome other positive responses to fish, such as behavioural andmorphological changes to reduce mortality due to predation.Synergism was detected in the effects of the fish smell andfood deficiency, which suggests that fish smell reduces thetolerance of Daphnia to an environmental stress, food shortage.     

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     

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.     

Size-selective dispersal of Daphnia resting eggs by backswimmers (Notonecta maculata)

Freshwater zooplankton is increasingly used to study effects of dispersal on community and metacommunity structure. Yet, it remains unclear how zooplankton disperses. Clearly, birds and wind play a significant role as zooplankton dispersal agents, but they may not always be the main vectors. This experimental study shows that a cosmopolitan aquatic insect, Notonecta, can be an important vector of cladoceran resting eggs (ephippia). Dispersing Notonecta frequently transported ephippia during flight, with a bias towards smaller ephippia in two species. A similar trend was present at the species level: Daphnia species with smaller ephippia were more often dispersed, suggesting that Notonecta could generate specific colonist communities. In addition, buoyancy appeared a critical trait, as non-floating ephippia of Daphnia magna were never dispersed. Our data suggest that Notonecta could be important dispersers of Daphnia, and that knowledge of dispersal dynamics of Notonecta may be used to predict Daphnia dispersal, colonization and resilience to disturbance.     

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.     

Effects of prey-size and predator-instar on the predation of Daphnia by Notonecta

Abstract. 1. Attack rates and handling times are measured by a series of separate functional response experiments for each instar of Notonecta glauca attacking four size classes of Daphnia magna as prey. The resulting attack rate and handling time surfaces are complex, with maximum attack rates for small predators attacking small prey, and large predators attacking large prey. Adult Notonecta have lower attack rates than the two previous juvenile instars (4 and 5).
2. The literature on attack rates and handling times in other predator—prey interactions that involve a series of different predator and prey size or age classes is reviewed in the context of the Notonecta-Daphnia results. The data suggest that small predator instars will usually compete with large instars for food, unless there is spatial or temporal separation between them.
3. Complex attack rate and handling time surfaces are to be expected wherever a wide range of prey and predator sizes is involved.
4. Size related changes in attack rates and handling times can introduce very complex dynamics into predator-prey interactions.     

Environmental cues for cyclomorphosis in Daphnia retrocurva Forbes

SUMMARY.

• 1 The invertebrate predators. Chaohorus, Leptodora, Hydra, Utricularia, and cyclopoid copepods were ineffective as inducers of high helmets in laboratory reared Daphnia retrocurva. Lako water from different sources, when used as culture medium, was also ineffective.
• 2 High helmets were induced when clones were grown under warm and turbulent conditions. Presence or absence of illumination and varying photoperiod did not affect helmet growth in warm turbulent cultures. Different clones grown under warm turbulent conditions differed in their responsiveness to the treatment, but no relationship between helmet size in clones and helmet size in the field on the dates of clone isolation was demonstrated. Laboratory-induced phenotypes were rarely as extreme as those of field animals.

     

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.     

Two threats at once: encounters with predator cues alter host life-history and morphological responses to parasite spores

Parasites and predators are ubiquitous threats in every ecosystem. Host and prey species, respectively, have evolved effective protective mechanisms which are assumed to involve costs. In this study, we analyzed potential interactions between both threats. We exposed waterfleas (Daphnia longicephala) simultaneously to parasite spores (the yeast Metschnikowia) and cues from predatory notonectids (Notonecta glauca). In response to the parasite, D. longicephala had a delayed maturation time and produced less and smaller offspring, even though the parasite developed no spores. This suggests that hosts can successfully fight off the parasite invoking defensive costs. Some of these effects were altered or even reversed by the presence of predator cues. For example, time to maturity was further delayed when the Daphnia were exposed to both threats than under parasite stress alone. In addition, more offspring were produced in the presence of both threats, although parasites alone reduced their number. However, there was no effect of parasite exposure on the expression of morphological defenses. Our results imply that the impact of parasites on host species depends strongly on the presence of further threats. Similar types of experimental approaches may enhance our understanding of the effects of multiple stressors in natural systems.     

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.     

Predator-specific inducible morphological defenses of a water flea against two freshwater predators

The expression of inducible morphological defenses in Daphnia in response to a single predator is a well-known phenomenon. However, predator-specific modifications of the same defensive traits as an adaption to different predator regimes is so far only described for Daphnia barbata. It is unknown if this accounts only for this species or if it is a more widespread, general adaptive response in the genus Daphnia. In the present study, we therefore investigated whether a clone of the pond-dwelling species Daphnia similis responds to different predatory invertebrates (Triops cancriformis; Notonecta maculata) with the expression of predator-specific modifications of the same defensive traits. We showed that Triops-exposed individuals express a significantly longer tail-spine, while body width decreased in comparison to control individuals. Additionally, they also expressed inconspicuous defenses, that is, significantly longer spinules on the dorsal ridge. The Notonecta-exposed D. similis showed a significantly longer tail-spine, longer spinules and a larger spinules bearing area on the dorsal ridge than control individuals as well. However, a geometric morphometric analysis of the head shape revealed significant, predator-specific changes. Triops-exposed individuals expressed a flattened head shape with a pronounced dorsal edge, while Notonecta-exposed individuals developed a high and strongly rounded head. Our study describes so far unrecognized inducible defenses of D. similis against two predators in temporary waters. Furthermore, the predator-dependent change in head shape is in concordance with the ‘concept of modality’, which highlights the qualitative aspect of natural selection caused by predators.     

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.     

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     

Costs and benefits of defences induced by predators differing in dangerousness

While theoretical studies predict that inducible defences should be fine-tuned according to the qualities of the predator, very few studies have investigated how dangerousness of predators, i.e. the rate at which predators kill prey individuals, affects the strength of phenotypic responses and resulting benefits and costs of induced defences. We performed a comprehensive study on fitness consequences of predator-induced responses by involving four predators (leech, water scorpion, dragonfly larva and newt), evaluating costs and benefits of responses, testing differences in dangerousness between predators and measuring responses in several life history traits of prey. We raised Rana dalmatina tadpoles in the presence of free-ranging predators, in the presence of caged predators, and exposed naive and experienced tadpoles to free-ranging predators. Tadpoles adjusted the intensities of their behavioural and morphological defences to predator dangerousness. Survival was lower in the nonlethal presence of the most dangerous predator, while we could not detect costs of induced defences at or after metamorphosis. When exposed to free-ranging predators, small, but not large, tadpoles benefited from exhibiting an induced phenotype in terms of elevated survival when compared to naive tadpoles, but we did not observe higher survival either in tadpoles exhibiting more extreme phenotypes or in tadpoles exposed to the type of predator they were raised with. These results indicate that while predator-induced defences can mirror dangerousness of predators, costs and benefits do not necessarily scale to the magnitude of plastic responses.     

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.