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.     

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.     

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.     

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.     

Impact of Daphnia pulex on a metalimnetic microbial community

A well-structured metalimnetic community, composed mainly ofphototrophic purple bacteria, Cryptomonas, and a few speciesof ciliates and rotifers, was regularly found between 1984 and1991 in Lake Cis. These populations appeared during spring,reached high concentrations and remained in the metalimnionuntil winter mixing. We had previously postulated that thesemetalimnetic populations could persist in such high numbersbecause they were free of efficient predation, since the oxygen-sulfideinterface provided a refuge from predation. In September 1992,an abundant Daphnia pulex population developed in the lake whichresulted in drastic changes in the formerly stable community.The presence of D.pulex induced an extreme clear-water phasein the epilimnion and the metalimnetic populations were severelyreduced. Feeding experiments with Cryptomonas and heterotrophicand phototrophic bacteria as food for D.pulex resulted in clearancerates around 0.7 ml individual^–1 h^–1. The impactwas very high on the microaerophilic populations, whereas theanaerobic populations were least affected, since sulfide limitedthe vertical distribution of ^D.pulex. We conclude from thisevidence that the metalimnetic populations in previous yeanwere mostly food limited (bottom-up control) and that theirhigh abundances were in great part due to a lack of efficientpredation.     

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     

A change in the pattern of vertical migration of Chaoborus flavicans after the introduction of trout

The pattern of diel vertical migration exhibited by Chaoborusflavicans in Lake Lenore, Washington has changed over the pastdecade. Formerly Chaoborus larvae and pupae were present inthe water column during the day. Since 1982, a strong patternof diel vertical migration has been evident in this population.Third and fourth instar larvae and pupae reside in the sedimentsduring the day and then ascend to the surface waters at night.The change in migratory activity of C. flavicans was coincidentwith the introduction of cutthroat trout (Salmo clarki henshawi)into Lake Lenore in 1979. Predation by trout on fourth instarlarvae and pupae of C. flavicans was probably responsible forthe observed changes in migratory behavior.     

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.     

Horizontal distribution of Daphnia pulex in response to toxic and non-toxic algal extracts

We studied the horizontal distribution of Daphnia pulex as aresponse to gradients of toxic extracts of two cyanobacteria,Microcystis aeruginosa and Oscillatoria agardhii and non-toxicextracts of the green alga Scenedesmus obtusiusculus. The experimentwas performed in the dark using a flow through system with fivechambers. Daphnia pulex aggregated at the inlet of Scenedesmusextract, but showed similar responses to extracts of toxic cyanobactenaand food-free medium. Chemical cues seem to affect food search,but do not effect Daphnia pulex's avoidance of toxic algae.     

Diel horizontal migration and swarm formation in Daphnia in response to Chaoborus

Dense swarms of Daphnia longispina (up to 4000 animals l^–1) were recorded along the littoral zone in a lake where Chaoborus flavicans is considered the main predator. D. longispina coexisted with D. pulex, but there were no D. pulex in the littoral swarms. Swarms were less dense at night (about 1/10 the density), and D. longispina exhibited diel horizontal migrations by aggregating in the littoral during the day and spreading out at night. Laboratory experiments showed that Chaoborus capture efficiency on juvenile daphnids was higher in the light compared to darkness, and that Daphnia exhibited a behavioural response to water that had previously contained Chaoborus. We conclude that predation from Chaoborus can be an important factor affecting the distribution patterns of Daphnia observed in this lake. The behavioural experiments indicated that this influence might be partly mediated by chemical agents.     

Changes in the structure of a zooplankton community during a Ceratium (dinoflagellate) bloom in a eutrophic fishless pond

The community structure of zooplankton was studied in a eutrophic,fishless Japanese pond. The ecosystem was dominated by a dinoflagellate,Ceratium hirundinella, two filter-feeding clado-cerans, Daphniarosea and Ceriodaphnia reticulata, and an invertebrate predator,the dipteran Chaoborus flavicans. The midsummer zooplanktoncommunity showed a large change in species composition (theDaphnia population crashed) when a heavy Ceratium bloom occurred.It is shown that (i) the rapid density decline of D.rosea inmid-May was mainly caused by a shortage of edible phytoplankton,which was facilitated by the rapid increase in Chirundinellaabundance; (ii) the low density of D.rosea in June-July wasconsidered to be mainly caused by the blooming of Ceratium hirundinella(which may inhibit the feeding process of D.rosea), while predationby Cflavicans larvae, the changing temperature, the interspecificcompetition and the scarcity of edible algae were not judgedto be important; (iii) the high summer biomass of the planktonicCflavicans larvae was maintained by the bloom of C.hirundinella,because >90% of the crop contents of C.flavicans larvae wereC.hirundinella during this period. The present study indicatesthat the large-sized cells or colonies of phytoplankton arenot only inedible by most cladocerans, but the selective effectof the blooming of these algae can also influence the compositionand dominance of the zooplankton community, especially for thefilter-feeding Cladocera, in a similar way as the selectivepredation by planktivorous fish. The large-sized phytoplanktoncan also be an important alternative food for ominivorous invertebratepredators such as Chaoborus larvae, and thus may affect theinteractions between these predators and their zooplanktonicprey. In this way, such phytoplankton may play a very importantrole in regulating the dynamics of the aquatic food web, andbecome a driving force in shaping the community structure ofzooplankton.     

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.     

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     

Daphnia dominance and zooplankton community structure in fishless ponds

Predation by fish has commonly been viewed as a primary driverof spatial and seasonal variation in Daphnia dominance and thesize structure of zooplankton communities. Yet, previous researchsuggests that large Daphnia do not always dominate in the absenceof predation. As alternatives to the planktivory model, numerousmechanisms have been put forth, including the effect of resourcecompetition and its interaction with resource quantity and qualityand abiotic factors (e.g. temperature). Here results are presentedof a field survey of 18 fishless, permanent ponds in southwestMichigan in which spatiotemporal variation in Daphnia pulexabundance and several potential determinants of this variationare explored. Results revealed a large amount of variation inD. pulex incidence and relative biomass, with some ponds exhibitingseasonal losses, some having few or no Daphnia, and some beingdominated by D. pulex for the entire sample period. Redundancyanalysis of zooplankton composition and pond environmental variables(biotic and abiotic) showed no relationship between D. pulexbiomass and measures of Chaoborus abundance, algal resourceproduction, or algal resource quality (including seston C:N:P).Instead, pH and temperature (both of which covaried) showedthe strongest relationship with D. pulex biomass.     

COMPETITIVE GRAZERS AND THE PREDATORY WHELK LEPSIELLA FLINDERSI (GASTROPODA: MURICIDAE) STRUCTURE A MUSSEL BED (XENOSTROBUS PULEX) ON A SOUTHWEST AUSTRALIAN SHORE

On a southwest Australian exposed rocky shore within King GeorgeSound, the predatory muricid Dicathais orbita was observed feedingnon-selectively on an array of sessile prey, including Austromegabalanusnigrescens, Galeolaria caespitosa, Patelloida nigrosulcata,Serpulorbis sipho, Siphonaria sp. and the mussel Xenostrobuspulex. On a more sheltered, contiguous, platform of the same shore,however, a mat of Xenostrobus pulex occurred which was beingpredated by another muricid, Lepsiella flindersi. X. pulex occupieda wide vertical range on this shore. Higher-zoned, supralittoral,individuals were small and occurred as clusters in crevicesand pits in the rock. A mat of mussels in the lower eulittoralzone was heavily predated by the drilling L. flindersi whichattacked selectively the largest individuals. Between, in thehigh eulittoral, the mussel bed was formed into patches whichwere isolated by the grazing activities of an array of herbivorousgastropods. Recruitment here by X. pulex was to the patch edgesand the grazer's habits of clustering against them, furtherkept them discrete. Little predation by L. flindersi occurredat this shore level. The Xenostrobus pulex community was, therefore, highly structureddown the shore sequentially by: (a), physiological stresses;(b), competitive grazing pressures and (c), predation. (Received 2 February 1998; accepted 5 January 1999)     

Is mating of copepods associated with increased risk of predation?

In laboratory experiments, we tested whether the cyclopoid copepodCyclops vicinus is more vulnerable to predation by juvenile(young-of-the-year) roach (Rutilus rutilus) and/or larvae ofthe phantom midge Chaoborus flavicans during mating than individualadult copepods of the same species. We also tested whether C.vicinusavoided mating, displayed shorter mating times and/or loweractivity when a predator (Chaoborus) was present, or when exposedto water in which predators (Chaoborus) were previously held.Fish ate the same quantity of pairs in copulation and individualegg-bearing females but significantly fewer females withouteggs. Chaoborus ate similar quantities of pairs and femalesbut fewer males. Pairs in copulation and egg-bearing femaleswere detected earlier by fish than individual non-ovigerousfemales or males, and pairs in copulation were captured mosteasily by fish. Cyclops vicinus mated less often when Chaoboruslarvae were present than in water in which Chaoborus was previouslyheld, or in pure tap water. However, predator presence or exposureto predator-treated water had no effect on (i.e. did not reduce)mating duration. Activity of C.vicinus pairs during copulationwas significantly lower when a predator was present, or in predator-treatedwater, than in pure tap water, and activity of pairs decreasedwith increasing activity of the predator. Although our experimentswere carried out under artificial conditions which cannot betransferred to the complex conditions in the field, they suggestthat mating in copepods is dangerous and that copepods haveevolved particular strategies to reduce the risk of predationduring mating.     

Experimental studies of food and suspended sediment effects on growth and reproduction of six planktonic cladocerans

Life-long somatic growth and egg production responses of Daphniabarbata, Daphnia gibba, Daphnia laevis, Daphnia pulex, Moinamicrura and Diaphanosoma excisum were examined in relation todifferent food and suspended sediment levels, in factorial experimentsat 20°C. Food treatments involved additions of 0, 100, 500and 2500 µg C l^–1 of Selenastrum to 20 µmfiltered water, generally from source lakes. These food levelswere tested at two suspended sediment levels in all species,viz. (i) natural source-lake nephelometric turbidities of 7–65nephelometric turbidity units (NTU) ({small tilde}10–70mg l^–1 TSS) and (ii) {small tilde}3- to 4-fold enrichmentof natural levels (8-fold in D.excisum). A third sediment-freetreatment was tested in all species of Daphnia other than D.gibba.Growth in body length and reproductive output were assesseddaily for individual animals. Main and interactive effects offood and sediment on growth were assessed at selected ages fromday 3 through subsequent life using analysis of variance (ANOVA).Strong and highly significant positive food effects were apparentat all ages in all species examined, with the curious exceptionof D.excisum. The onset of maturity and fecundity were alsopositively related to food level. Sediment effects on growth,age of maturity and fecundity were variable, but tended to bemuch weaker than food effects. Both stimulatory (positive, especiallyat low food levels) and inhibitory (negative) effects of sedimenton growth were apparent, both between and within species. Performancein sediment-free water was very poor, except in D.pulex. Food-sedimentinteraction effects were variable. Generally, turbidwater specieswere influenced less adversely by sediment than clear-waterspecies, indicating the existence of environmentally appropriateadaptive responses. Overall, the findings indicate that lightlimitation of algal resources by suspended sediments, ratherthan the condition of high turbidity per se, is responsiblefor the apparently negative impact of suspended sediments frequentlyobserved on natural populations of cladoceran zooplankters.     

Factors contributing to coexistence of Chaoborus flavicans and C. punctipennis (Diptera,Chaoboridae) in a small meromictic lake

In Crawford Lake, a small meromictic water body in southern Ontario, Canada, the life cycles of planktonic Chaoborus flavicans and C. punctipennis were out of phase by about two months, the former pupating from mid May through mid June and the latter from July through September. C. flavicans possibly produced a second annual generation. Fourth instars of both species were strong diel migrators and occupied similar strata at most times. C. punctipennis fourth instar diet consisted almost entirely of rotifers. C. flavicans ate rotifers but fed heavily also on daphnids in May and August. C. punctipennis fourth instars showed little growth until early spring, possibly owing to a sparseness of rotifers, then grew rapidly until pupation. C. flavicans had a slow, but relatively constant growth rate at all times during the open water season, presumably because its greater mouth gape allowed it a wider range of food items.     

Attraction of the amphipod <Emphasis Type="Italic">Gammarus pulex</Emphasis> to water-borne cues of food

We examined the ability of the amphipod Gammarus pulexto detect chemical cues released from potential food sources. Therefore, response of G. pulex to chemical cues from food was tested in paired-choice laboratory experiments. Comparisons were made between artificial and natural leaves, with and without the importance of aufwuchs, and with different components of the aufwuchs community. Our study demonstrated that G. pulex actively chose its food and that G. pulex is most strongly attracted to the aufwuchs on discs rather than to the leaf itself. Fungi and bacteria are more important in the food selection process than algae probably because fungal and bacterial cues are more specific cues for decaying leaves than algal cues, since algae also grow on mineral substrates and then do not contribute to leaf decomposition.     

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.