Morphological defenses induced in situ by the invertebrate predator Chaoborus : comparison of responses between Daphnia pulex and D. rosea

The presence of plankton predators may induce altered morphology in their potential prey. To date, the mechanism of induction and adaptive value of such defensive responses have been examined in the laboratory. This study investigated the morphological defense structures induced by the invertebrate predator Chaoborus in two coexisting Daphnia species, D. pulex and D. rosea, in the field. In Piscivore Lake (Gr?fenhain, Germany), continuous and intense biomanipulation had led to near elimination of planktivorous fish and greatly increased abundances of Chaoborus (up to >10 larvae l^–1). Here, the density of Chaoborus was manipulated within the lake by an enclosure/exclosure setup and resulting morphological responses of Daphnia spp. were investigated in situ. Three replicate enclosures (4.6 m³) contained no Chaoborus (predator exclusion bags), whereas Chaoborus entered three others at ambient densities (predator enclosures). In both species of Daphnia, formation of neckteeth and elongation of the tail spine were recorded in the predator enclosures, but not in the predator exclusion treatments. Additionally, D. rosea responded to predator inclusion with an increase of the size at first reproduction. Despite the induced defense structures, the presence of Chaoborus caused increased mortality of both Daphnia species. In addition, Chaoborus affected the coexistence of the two populations of Daphnia by causing higher relative mortality in D. rosea. Neckteeth formation was always more pronounced in D. pulex than in D. rosea of the same size. Neckteeth were induced specifically in vulnerably sized juvenile instars of D. pulex, but were not found in all vulnerable instars of D. rosea. In D. rosea, neckteeth were few or absent in the ephippial hatchlings, and neckteeth formation ceased before juveniles reached a body size outside the range that larger larval stages of Chaoborus could ingest. This study provides the first experimental demonstration in the field of the inducibility of morphological defense structures in Daphnia at ambient densities of Chaoborus larvae, and quantifies these in situ responses. This expands on earlier observations of a correlation between predator density in the field and the expression of neckteeth in Daphnia. The term ”maximum size for neckteeth formation” (MSNF) is defined as the limit in body size above which no production of neckteeth was evident. This limit was used to distinguish the size classes of Daphnia that show a sensitive response to Chaoborus kairomone. This new term may be used for further comparisons among species and among different types of predator-induced responses as well as for the evaluation of the adaptive value of defense structures. Received: 10 April 1999 / Accepted: 6 April 2000     

Ionotropic Glutamate Receptors Mediate Inducible Defense in the Water Flea Daphnia pulex

Phenotypic plasticity is the ability held in many organisms to produce different phenotypes with a given genome in response to environmental stimuli, such as temperature, nutrition and various biological interactions. It seems likely that environmental signals induce a variety of mechanistic responses that influence ontogenetic processes. Inducible defenses, in which prey animals alter their morphology, behavior and/or other traits to help protect against direct or latent predation threats, are among the most striking examples of phenotypic plasticity. The freshwater microcrustacean Daphnia pulex forms tooth-like defensive structures, “neckteeth,” in response to chemical cues or signals, referred to as “kairomones,” in this case released from phantom midge larvae, a predator of D. pulex. To identify factors involved in the reception and/or transmission of a kairomone, we used microarray analysis to identify genes up-regulated following a short period of exposure to the midge kairomone. In addition to identifying differentially expressed genes of unknown function, we also found significant up-regulation of genes encoding ionotropic glutamate receptors, which are known to be involved in neurotransmission in many animal species. Specific antagonists of these receptors strongly inhibit the formation of neckteeth in D. pulex, although agonists did not induce neckteeth by themselves, indicating that ionotropic glutamate receptors are necessary but not sufficient for early steps of neckteeth formation in D. pulex. Moreover, using co-exposure of D. pulex to antagonists and juvenile hormone (JH), which physiologically mediates neckteeth formation, we found evidence suggesting that the inhibitory effect of antagonists is not due to direct inhibition of JH synthesis/secretion. Our findings not only provide a candidate molecule required for the inducible defense response in D. pulex, but also will contribute to the understanding of complex mechanisms underlying the recognition of environmental changes, which form the basis of phenotypic plasticity.     

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.     

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.     

Temperature affects selectivity of Chaoborus larvae-eating Daphnia

In ponds, a chemical produced by predaceous Chaoborus (Insecta, Diptera) larvae changes the development of juvenile Daphnia pulex (Crustacea, Branchiopoda) so the juveniles grow spines (neckteeth) on the back of their head. It is generally assumed that the spined phenotype is (or is an indicator of) a morphological predator defense. The research reported here tests the hypothesis that the induced neckteeth do in fact increase Daphnia survivorship, over a range of temperatures. Predation experiments were conducted over a range of temperatures from 6 to 22 °C using fourth instar Chaoborus americanus larvae as the predator. The prey were a mixture of spined (induced necktooth phenotype) and unspined (uninduced) juvenile Daphnia pulex. At 6 and 11 °C, Chaoborus selected the unspined phenotype over the spined phenotype, as expected. However, at 22 °C, the selectivity was reversed: significantly fewer on the spined survived compared to the unspined phenotype. These results suggest that the spined phenotype may either increase or decrease Daphnia pulex survival, depending on temperature and clone.     

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.     

Pricklier with the proper predator? Predator‐induced small‐scale changes of spinescence in Daphnia

Phenotypic plasticity in defensive traits is a common response of prey organisms to variable and unpredictable predation regimes and risks. Cladocerans of the genus Daphnia are keystone species in the food web of lentic freshwater bodies and are well known for their ability to express a large variety of inducible morphological defenses in response to invertebrate and vertebrate predator kairomones. The developed defenses render the daphnids less susceptible to predation. So far, primarily large‐scale morphological defenses, like helmets, crests, and tail‐spines, have been documented. However, less is known on whether the tiny spinules, rather inconspicuous traits which cover many Daphnia’s dorsal and ventral carapace margins, respond to predator kairomones, as well. For this reason, we investigated two Daphnia species (D. magna and D. longicephala) concerning their predator kairomone‐induced changes in dorsal and ventral spinules. Since these small, inconspicuous traits may only act as a defense against predatory invertebrates, with fine‐structured catching apparatuses, and not against vertebrate predators, we exposed them to both, an invertebrate (Triops cancriformis or Notontecta maculata) and a vertebrate predator (Leucaspius delineatus). Our results show that the length of these spinules as well as spinules‐covered areas vary, likely depending on the predator the prey is exposed to. We further present first indications of a Daphnia species‐specific elongation of the spinules and an increase of the spinules‐bearing areas. Although we cannot exclude that spinescence is altered because it is developmentally connected to changes in body shape in general, our results suggest that the inducible alterations to the spinule length and spinules‐covered areas disclose another level of predator‐induced changes in two common Daphnia species. The predator‐induced changes on this level together with the large‐scale and ultrastructural defensive traits may act as the overall morphological defense, adjusted to specific predator regimes in nature.     

Predator-induced alterations in Daphnia morphology

The freshwater cladocerans Daphnia pulex and Daphnia schodleriprotect themselves from predation by morphological alterationsinduced in response to water-soluble chemicals released by theirrespective predators. Daphnia pulex is induced by larvae ofthe phantom midge, Chaoborus. Populations of D.pulex which areinduced are those most likely to have intense interaction withthe predator. This is true both on a broad geographic scaleas well as locally Cephalic expansion in D.schodleri is inducedby notonectids, in particular Buenoa sp. This predator preferslarger prey and consequently small instars of D.schodleri showno evidence of induction Both examples of predator-induced alterationssuggest that this type of response is costly to the prey andis manifested only in those individuals and populations mostthreatened     

Competition, predation and the relative abundances of two species of Daphnia

We investigated the factors controlling the relative abundancesof two Daphnia species, D.pulex and D.laevis, in a small Wisconsinpond. D.pulex was the dominant Daphnia species in fall 1977and summer-fall 1978; D.laevis was the only Daphnia speciespresent in summer 1979. The abundance of D.laevis was positivelycorrelated with the abundance of the notonectid, Buenoa confusa.In predation trials, notonectides exhibited a distinct preferencefor D.pulex over similarly-sized D.laevis, but Chaoborus larvaefed at similar rates on both Daphnia species. Behavioral observationsrevealed that Buenoa adults were much less efficient at capturingD.laevis than D.pulex. Quantitative results of these predationtrials were combined with estimates of predator and prey densityand distribution to evaluate the effect of predation on thedaphnid populations. The effect of predation varied throughtime and microhabitat, and only infrequently could predationaccount for total prey mortality. D.laevis was most abundantat times and in places where Buenoa predation was most intense.Competition experiments illustrated the competitive superiorityof D.pulex over D.laevis. D.pulex was able to competitivelyexclude D.laevis in long term experiments, and D.pulex's fecunditywas higher than that of D.laevis in shorter experiments. Inlong-term experiments, Chaoborus larvae at natural densitieswere able to keep both Daphnia species at low, constant levelsand neither species clearly dominated when Chaoborus was present.The relative abundances of D.pulex and D.laevis were controlledby a complex of biotic and abiotic factors. Pond depth and predatordensity determined the intensity of predation on daphnid populations.When notonectid predation was intense, D.laevis dominated; whenthe intensity of predation by notonectids was low, D.pulex dominateddue to its superior competitive abilities. At different timesselective predation or high resource levels promoted the co-existenceof these two species. ¹Current address of both authors: Department of Biological Sciences,University of California, Santa Barbara, CA 93106, USA     

Chaoborus crystallinus predation on Daphnia pulex: can induced morphological changes balance effects of body size on vulnerability?

Juvenile Daphnia pulex form neckteeth in reponse to chemicals released by predatory Chaoborus crystallinus larvae. Formation of neckteeth is strongest in the second instar followed by the third instar, whereas only small neckteeth are found in the first and fourth instar of experimental clones. Predation experiments showed that body-size-dependent vulnerability of animals without neckteeth to fourth instar C. crystallinus larvae matched the pattern of neckteeth formation over the four juvenile instars. Predation experiments on D. pulex of the same clone with neckteeth showed that vulnerability to C. crystallinus predation is reduced, and that the induced protection is correlated with the degree of neckteeth formation. The pattern of neckteeth formation in successive instars is probably adaptive, and it can be concluded that neckteeth are formed to different degrees in successive instars as an evolutionary compromise to balance prediation risk and protective costs.     

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.     

Gene up-regulation in response to predator kairomones in the water flea, <Emphasis Type="Italic">Daphnia pulex</Emphasis>

Background

Numerous cases of predator-induced polyphenisms, in which alternate phenotypes are produced in response to extrinsic stimuli, have been reported in aquatic taxa to date. The genus Daphnia (Branchiopoda, Cladocera) provides a model experimental system for the study of the developmental mechanisms and evolutionary processes associated with predator-induced polyphenisms. In D. pulex, juveniles form neckteeth in response to predatory kairomones released by Chaoborus larvae (Insecta, Diptera).

Results

Previous studies suggest that the timing of the sensitivity to kairomones in D. pulex can generally be divided into the embryonic and postembryonic developmental periods. We therefore examined which of the genes in the embryonic and first-instar juvenile stages exhibit different expression levels in the presence or absence of predator kairomones. Employing a candidate gene approach and identifying differentially-expressed genes revealed that the morphogenetic factors, Hox3, extradenticle and escargot, were up-regulated by kairomones in the postembryonic stage and may potentially be responsible for defense morph formation. In addition, the juvenile hormone pathway genes, JHAMT and Met, and the insulin signaling pathway genes, InR and IRS-1, were up-regulated in the first-instar stage. It is well known that these hormonal pathways are involved in physiological regulation following morphogenesis in many insect species. During the embryonic stage when morphotypes were determined, one of the novel genes identified by differential display was up-regulated, suggesting that this gene may be related to morphotype determination. Biological functions of the up-regulated genes are discussed in the context of defense morph formation.

Conclusions

It is suggested that, following the reception of kairomone signals, the identified genes are involved in a series of defensive phenotypic alterations and the production of a defensive phenotype.

     

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.     

Costs of predator‐induced morphological defences in Daphnia

1. Inducible defences are advantageous because they protect the prey while limiting associated fitness costs. The presence of these costs is an essential component of this conditional strategy, since their absence would favour constitutive (fixed) defences. In some cases, however, these costs have been difficult to measure because of complex interactions between the defences themselves, resultant life history changes and the organism’s environment. 2. The pond‐dwelling water flea, Daphnia pulex, forms defensive neck spines in response to kairomones released by predatory larvae of the phantom midge, Chaoborus. This predator–prey interaction and the formation of these inducible defences have been well studied, but costs associated with the development of neck spines remain unclear. In this study, I address this problem by analysing the effect of Chaoborus kairomones on the life history responses (and fitness costs associated with these responses) of two clones of D. pulex that are from the same pond population, but differ greatly in their degree of neck spine development. 3. Both D. pulex clones exhibited the same predator‐induced shifts in life history: larger size at birth, reduced juvenile growth rate (producing a smaller size at maturity), delayed reproduction and a reduction in the number of neonates produced after the first clutch. Relative fitness decreased significantly and to the same degree (c. 10% reduction in r) in each clone. This observed fitness cost was not directly related to the neck spines per se since the cost was the same in both clones, despite their considerable differences in neck spine development. Rather, it appears to be indirectly related to this antipredator morphology via a combination of delayed reproduction and a set of life history trade‐offs (decreased growth rate, decreased reproduction after the first clutch) for increased neonate body size, which is necessary for neck spines to be effective defences. This suite of induced responses is probably a result of local adaptation of these two D. pulex clones to their common pond environment. 4. Costs of inducible defences do not always entail direct allocation costs associated with forming and maintaining a defence, but may also involve indirect life history responses that are specific to particular environmental situations. This local adaptation would explain the highly variable life history responses observed among D. pulex clones from different pond environments.     

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.     

Density-dependent effects of prey defences

In this study, we show that the protective advantage of a defence depends on prey density. For our investigations, we used the predator-prey model system Chaoborus-Daphnia pulex. The prey, D. pulex, forms neckteeth as an inducible defence against chaoborid predators. This morphological response effectively reduces predator attack efficiency, i.e. number of successful attacks divided by total number of attacks. We found that neckteeth-defended prey suffered a distinctly lower predation rate (prey uptake per unit time) at low prey densities. The advantage of this defence decreased with increasing prey density. We expect this pattern to be general when a defence reduces predator success rate, i.e. when a defence reduces encounter rate, probability of detection, probability of attack, or efficiency of attack. In addition, we experimentally simulated the effects of defences which increase predator digestion time by using different sizes of Daphnia with equal vulnerabilities. This type of defence had opposite density-dependent effects: here, the relative advantage of defended prey increased with prey density. We expect this pattern to be general for defences which increase predator handling time, i.e. defences which increase attacking time, eating time, or digestion time. Many defences will have effects on both predator success rate and handling time. For these defences, the predator’s functional response should be decreased over the whole range of prey densities. Received: 15 September 1999 / Accepted: 23 December 1999     

Demographic costs of Chaoborus-induced phenotypic plasticity in Daphnia pulex

Summary It has been proposed that morphological defenses against predation have demographic costs. We measured the cost of a predator-induced morphological defense, using predaceous phantom midge larvae Chaoborus americanus (Insecta, Diptera) and the prey species Daphnia pulex (Crustacea, Cladocera). The induced defense is a neck tooth (and other pleiotropic structures) developed in juvenile D. pulex in the presence of C. americanus. Laboratory life table experiments, in the absence of predation, indicated the population growth rate of typical D. pulex was 11% to 39% greater than that of D. pulex exposed to C. americanus extract, or C. americanus-conditioned water. The reduction in population growth rate was most frequently associated with an increase in the time between birth and first reproduction. Induced individuals required twenty more hours at 23°C, and twenty five more hours at 20°C, to develop to the age of first reproduction. Under limiting food conditions age-specific survivorship and the number of offspring produced per female by the induced form were reduced relative to the typical form. As a result, the difference in population growth rates among forms was greater at the low food level as indicated by a highly significant food by form interaction effect. In addition to neck teeth and lowered reproductive rates, the offspring of induced form individuals had significantly longer tail-spines (7.2–7.5%), and primiparous adults from the induction treatment were significantly shorter than controls (3–8%).     

Chaoborus predation and the function of phenotypic variation in Daphnia

To investigate the role of helmet formation in defense against predation, laboratory experiments were used to analyze the effects of morphological changes in Daphnia on susceptibility to Chaoborus predation. Behavioral observations of Chaoborus preying on helmeted and non-helmeted Daphnia suggest pre-contact advantages for helmeted prey but post-contact advantages for non-helmeted prey. Helmeted Daphnia are better at evading capture by Chaoborus but may also be more easily handled by the predator. Swimming behavior of the prey, which is influenced by the presence of a tailspine, may affect Chaoborus strike distance. These results re-emphasize the potential hydromechanical importance of body shape changes in defense against predation.     

Biogeographic variation in behavioral and morphological responses to predation risk

The expression of prey antipredator defenses is often related to ambient consumer pressure, and prey express greater defenses under intense consumer pressure. Predation is generally greater at lower latitudes, and antipredator defenses often display a biogeographic pattern. Predation pressure may also vary significantly between habitats within latitudes, making biogeographic patterns difficult to distinguish. Furthermore, invasive predators may also influence the expression of prey defenses in ecological time. The purpose of this study was to determine how these factors influence the strength of antipredator responses. To assess patterns in prey antipredator defenses based upon geographic range (north vs. south), habitat type (wave-protected vs. wave-exposed shores), and invasive predators, we examined how native rock (Cancer irroratus) and invasive green (Carcinus maenas) crab predators influence the behavioral and morphological defenses of dogwhelk (Nucella lapillus) prey from habitats that differ in wave exposure across an ~230 km range within the Gulf of Maine. The expression of behavioral and morphological antipredatory responses varied according to wave exposure, geographic location, and predator species. Dogwhelks from areas with an established history with green crabs exhibited the largest behavioral and morphological antipredator responses to green crabs. Dogwhelk behavioral responses to rock crabs did not vary between habitats or geographic regions, although morphological responses were greater further south where predation pressure was greatest. These findings suggest that dogwhelk responses to invasive and native predators vary according to geographic location and habitat, and are strongly affected by ambient predation pressure due to the invasion history of an exotic predator.     

Reciprocity in predator–prey interactions: exposure to defended prey and predation risk affects intermediate predator life history and morphology

A vast body of literature exists documenting the morphological, behavioural and life history changes that predators induce in prey. However, little attention has been paid to how these induced changes feed back and affect the predators’ life history and morphology. Larvae of the phantom midge Chaoborus flavicans are intermediate predators in a food web with Daphnia pulex as the basal resource and planktivorous fish as the top predator. C. flavicans prey on D. pulex and are themselves prey for fish; as D. pulex induce morphological defences in the presence of C. flavicans this is an ideal system in which to evaluate the effects of defended prey and top predators on an intermediate consumer. We assessed the impact on C. flavicans life history and morphology of foraging on defended prey while also being exposed to the non-lethal presence of a top fish predator. We tested the basic hypothesis that the effects of defended prey will depend on the presence or absence of top predator predation risk. Feeding rate was significantly reduced and time to pupation was significantly increased by defended morph prey. Gut size, development time, fecundity, egg size and reproductive effort respond to fish chemical cues directly or significantly alter the relationship between a trait and body size. We found no significant interactions between prey morph and the non-lethal presence of a top predator, suggesting that the effects of these two biological factors were additive or singularly independent. Overall it appears that C. flavicans is able to substantially modify several aspects of its biology, and while some changes appear mere consequences of resource limitation others appear facultative in nature.