Specificity of predator-induced neck spine and alteration in life history traits in Daphnia pulex

It has been proposed that the predator-induced defensive neck spine in Daphnia pulex has a demographic cost. Our results show that this cost is not merely an allocation cost related to the formation and maintenance of the neck spine. In a life table experiment, we tested whether spine induction and life history traits in D. pulex are affected by different invertebrate predators: first and third instar Chaoborus, fourth instar Mochlonyx and two size classes of Notonecta and Dytiscus larvae. D. pulex showed sensitivity to the different predators. Predator-exposure affected one or more of the following life history traits of D. pulex: the timing of first reproduction, clutch size, and growth. In some cases, exposure to predators altered life history traits when neck spine induction did not occur. These shifts in life history traits occurring in the absence of spine induction may be caused by behavioral or physiological changes triggered by the predators.     

Predator-induced phenotypic plasticity in Daphnia pulex: uncoupling morphological defenses and life history shifts

Chemical cues from a predator Chaoborus sp. induce morphological defense (neck spine) and life history shifts (later reproduction, decreased fecundity but larger juvenile size) in the waterflea Daphnia pulex. These shifts have been interpreted either as costs of defense or as separate adaptation. In order to investigate if the life history shifts can be separated from the morphological defense, Daphnia pulex individuals were exposed to chemical cues from Chaoborus at different stages of life for variable periods. The daphnids that were exposed to Chaoborus started their reproduction later than the controls, although the differences were not statistically significant. Neck spine was induced only if daphnids were exposed to Chaoborus in an early stage of their life. Numbers of eggs produced were not affected by the different treatments, but egg mortality was higher in mothers exposed to Chaoborus. With these treatments it was possible to see neck spine induction without measurable life history changes or costs. On the other hand, irrespective of neck spine presence, the Chaoborus chemical(s) had an effect on Daphnia pulex mothers.Publication no 2159. Netherlands Institute of Ecology, Centre for LimnologyPublication no 2159. Netherlands Institute of Ecology, Centre for Limnology     

Modification of life-history parameters of Daphnia pulex Leydig and D. magna Straus by the presence of Chaoborus sp.

Contamination of the culture water by high densities of phantom midge larvae, Chaoborus sp. resulted in size diminution, retarded reproduction and decrease in the clutch size of D. pulex, and size diminution of D. magna. Furthermore, D. pulex suffered heavy mortality. The results are discussed in the context of the hypothesis that energy is expended in the formation of defensive cyclomorphic spines. Other hypotheses are also discussed.     

Phosphorus availability mediates plasticity in life-history traits and predator–prey interactions in Daphnia

We analysed growth plasticity of two Daphnia pulex clones under low‐phosphorus (LP) and high phosphorus (HP) conditions, in the presence of Chaoborus kairomones to examine how food quality (P‐availability) might impact life‐history responses and vulnerability to predation. Overall, clone 1 grew faster, and was larger at maturity. Under HP, both clones responded to kairomones by increasing growth, age and size at maturity, and decreasing fecundity. Under LP, both clones suffered reduced growth, and fecundity. However, the magnitude of response to kairomones depended on a clone by P‐availability interaction. Chaoborus presented a 1 : 1 clonal mixture under HP or LP, consumed more individuals under LP. Moreover, fewer clone 1 individuals were consumed. Studying the effects of P‐availability on life histories, and predator–prey interactions may help us understand the mechanisms generating and maintaining plasticity, as well as influencing genotypic diversity and microevolutionary processes in natural populations.     

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.     

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.     

Neck spine protects Daphnia pulex from predation by Chaoborus, but individuals with longer tail spine are at a greater risk

We tested the prey preference of Chaoborus sp. on Daphnia pulexwith different defensive morphologies. The protective functionof inducible morphological defences, such as neck spine andlonger tail spine, was evaluated Second instar D.pulex individualsof two clones differing in their strength of neck spine inductionwere offered as prey to both Chaoborus obscuripes and Chaoborusflavicans. We used logistic regression analysis to evaluatethe effect of morphometry on the vulnerability of Daphnia. Thepresence of a neck spine and increased total length protectedD.pulex from Chaoborus predation. However, individuals witha longer tail spine were more vulnerable to Chaoborus predationChaoborus obscuripes was able to eat daphnids with a neck spinedue to the larger gape size of this chaoborid. The smaller speciesC.flavicans almost always ate prey with no neck spine.     

Demographic costs of Chaoborus-induced defences in Daphnia pulex: a sensitivity analysis

Summary We examined the demographic costs of Chaoborus-induced defensive spine structures in Daphnia pulex. Our aim was to assess the role of resource limitation and the interaction effects of limiting food level and antipredator structures on fitness of D. pulex and to pinpoint those life stages that are most sensitive to changes in the defence regime. Chaoborus-induced and typical morphotypes of D. pulex were reared at high and low food concentrations. Instar-based matrix population models were used to quantify the effects of predator-induction, food and their interaction on fitness of D. pulex. Predator-induction caused a statistically significant reduction in fitness at low food levels, but not at high food levels. Sensitivity analyses revealed that the fitness effects were primarily due to changes in the growth rate in instars 1–5, and secondarily to small reductions in the fertility of instars 5–10. The interaction between Chaoborus exposure and low food concentration was negative, and mediated through growth and fertility components. Both these components were reduced more in the Chaoborus-exposed, low food treatment than would be expected in the absence of interaction.     

Chaoborus predation and delayed reproduction in Daphnia: a demographic modeling approach

I develop a demographic model that examines the impact of Chaoborus predation on the population dynamics and life history of Daphnia. Predation effects are determined through analysis of the various components of the predator-prey interaction (encounter, attack, strike efficiency), and are integrated into a stage-classified matrix population model. The model is parameterized with data from interactions between D. pulex and fourth-instar C. americanus. I test this model with two laboratory experiments that examine population growth of D. pulex under the influence of five different levels of Chaoborus predation. With the exception of a single predation treatment in each experiment, the model accurately predicted the observed reduction in Daphnia numbers with increasing Chaoborus predation. I then use this model to investigate the evolution of delayed reproduction in D. pulex that are exposed to Chaoborus. I ask whether delayed reproduction may evolve in Daphnia that are subjected to Chaoborus predation as a trade-off for the benefits of larger body size. The model predicts that the effectiveness of such a life history trade-off depends on the relative sizes of predator and prey. In some interactions between Chaoborus and Daphnia, increasing Daphnia body length by as little as 5% from base growth trajectories sufficiently increases fitness (by reducing vulnerability to Chaoborus predation) to compensate for the cost of delayed reproduction. In other interactions, however, increased body length provides no benefit to Daphnia (and may even reduce fitness), and selection would act against the evolution of delayed reproduction. This revised version was published online in July 2006 with corrections to the Cover Date.     

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.     

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.     

Life-history responses to Chuoborus of spined and unspined Daphniu pulex

Water-borne chemicals released by the larvae of the predatoryphantom midge Chaoborus are known to induce morphological modificationsin its prey Daphnia pulex: these cladocerans develop neck spineswhich may carry several teeth. Some work has shown that thesemorphological variations enhance the prey's chances of escape.but since these neck teeth are not fixed defence reactions,they are thought to entail some form of cost, such as delayedmaturation and reduced fecundity. In this study. the relationshipbetween morphological and life-history changes in four clonesof Daphnia pulex reared in the presence and absence of Chaoborusflavicans was examined. Special emphasis was placed on the genotypiccomparison of the modifications. While all four clones showeda delay in maturation time in the presence of Chaoborus, theneck spine responses differed markedly among the genotypes:one clone never had any neck teeth, another always producedone single tooth, and two clones produced varying numbers ofteeth per spine (means 2.9 and 4. respectively). These resultsindicate that there is no general pattern of neck teeth productioncorresponding to delayed maturation. What there appears to beis genetic variability in two independent and possibly adaptiveresponses. However, the clone without neck teeth was the onlyone which showed no predator-induced reduction in fecundity.Another common morphological response to Chaoborus was thatjuveniles of all clones developed elongated tail spines.     

Effects of predator-released chemicals on some life history parameters of Daphnia pulex

The effects of chemicals released by fish and Chaoborus larvae on some life history traits in Daphnia pulex were studied in an in situ enclosure experiment. The mean size of Daphnia individuals was smaller in the presence of fish-released cues. Also the minimal size of an egg bearing female in the presence of fish exudates was smaller than in the population exposed to the chemicals released by Chaoborus larvae as well as in the control population. Fish-released chemicals caused the increase in clutch size in Daphnia. There were no statistically significant differences between the studied life history parameters of the control and Chaoborus treatments. The results are discussed in reference to recent laboratory research.     

CHAOBORUS PREDATION AND LIFE-HISTORY EVOLUTION IN DAPHNIA PULEX: TEMPORAL PATTERN OF POPULATION DIVERSITY,FITNESS, AND MEAN LIFE HISTORY

The effect of predation by the aquatic dipteran larva Chaoborus americanus on genetic diversity and life-history evolution in the cladoceran Daphnia pulex was investigated in large replicate laboratory populations. Instantaneous daily loss rates of clonal diversity and genetic variance for fitness indicate that 93–99% of initial genetic diversity can be removed from populations during the 8–12 generations of clonal reproduction that occur each year in natural populations. In the absence of predation, the principal evolved changes in mean population life history were smaller immature body size and increased and earlier fecundity. In the presence of size-selective Chaoborus predation, populations evolved toward larger body size and increased and earlier reproduction. The difference between these two trajectories is an estimate of the direct additive effect of Chaoborus predation. This effect was manifested as evolution toward larger body size with a trend toward earlier and increased reproduction.     

Life history responses of Daphnia clones to toxic Microcystis at different food levels

We examined how the amount of food of good quality, Scenedrsmusobtusiusculus, influenced the toxic effects of the cyanobacteriumMicrocystu aeruginosa on Daphnia pulex in a 21 day life tableexperiment. Our results show that all life history traits studied,i.e. longevity, growth and reproduction, of D.pulex were negativelyaffected by toxic Microcystis. The detrimental effects on theselife history traits were less pronounced at increasing foodlevels. In addition, D.pule.x clones differed in their lifehistory responses to toxic Microcystis, suggesting that thepresence of toxic cyanobacteria may modify the outcome amongD.pulex clones.     

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.     

Reproductive costs of Chaoborus-induced polymorphism in Daphnia pulex

Although the Chaoborus-induced spined morph of Daphnia pulex survives attacks by Chaoborus over twice as frequently as the typical morph, the spined morph is never found in the absence of Chaoborus. This implies that a disadvantage is associated with the spined morph in the absence of Chaoborus predation. The present study tested the hypothesis that the typical morph has a higher intrinsic rate of increase than the spined morph, by measuring several life history characteristics in controlled laboratory experiments at constant temperature and unlimited food.The results suggest that the spined morph of D. pulex takes longer to reach maturity, is smaller at maturity, but has similar egg number and egg size as the typical morph. These results are consistent with the hypothesis that the Chaoborus-induced spined morph is reproductively inferior to the typical morph.     

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.     

Reproductive allocation in Daphnia exposed to toxic cyanobacteria

We investigated experimentally how resources were allocated to reproduction in Daphnia pulex and Daphnia longispina when varying levels of toxic Microcystis were added to higher quality food. We used multiple regression models to estimate mean offspring size and clutch size in relation to maternal size and clutch number, and analysed effects of treatments on residuals from the models. We also measured variation in per offspring investment. At a high cyanobacterial level, D.pulex was virtually unable to reproduce. At a lower level, D.pulex produced small clutches. However, the regression model residuals indicated that the presence of cyanobacteria increased the portion of available resources allocated to reproduction. The observed allocation may be a means to maximize reproduction under diminished longevity. Effects on mean offspring size were marginal in D.pulex but variation in per offspring investment sometimes decreased in cyanobacterial exposures. Daphnia longispina was affected by a higher cyanobacterial level only, where offspring sized was reduced. Deviations from the regression model indicated that effects on maternal size alone do not explain this effect. Clutch size residuals and per offspring investment were unaffected by treatments in D.longispina. The observed responses differ from theoretical models on reproductive allocation under food imitation.      

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.