Cyclomorphosis inDaphnia galeata mendotae: variation and stability in phenotypic cycles

Phenotypic change is studied in a cyclomorphicDaphnia galeata mendotae population known from previous studies to be clonally diverse. Morphological analyses revealed cyclical changes in both adult and juvenile helmet length and tailspine length which were: 1) strongly correlated with mean water temperature; and 2) repeated annually during the 3-year study period. Field populations exhibited high (5% to 30%) coefficients of variation (CV) for both helmet length and tailspine length; the CV also exhibited seasonal fluctuations such that it was lowest in late summer. The period of highestDaphnia helmet development coincides with peak densities of the common invertebrate predatorsChaoborus andLeptodora. The fluctuations in CV may be due to both differential phenotypic expression of the coexisting clones and invertebrate predation.     

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.

     

The cyclomorphic response of Daphnia galeata mendotae: polymorphism or phenotypic plasticity

This study tests the hypothesis that cyclomorphosis in Daphniagaleata mendotae is equated with seasonal changes in the geneticstructure of populations. Multilocus electrophoretic genotypingof individual D. g. mendotae was used to identify related parthenogeneticlines. Between different clones and genotypes, there was phenotypicvariability in both laboratory and field populations. Withinclones and within genotypes, and in the absence of intense invertebratepredation, phenotypic expression was conservative. These patternssuggested that there was a correlation between phenotypic andgenetic change. However, in the field, only two of three populationsshowed seasonal changes in genotypic frequency, whereas allthree showed seasonal changes in phenorype. Furthermore, thepatterns of phenotypic change seen in the field populationswere different and appeared to be correlated with changes inphysical conditions and predation pressure. We conclude thathelmet morphology within genotypes is plastic enough to accountfor much of the seasonal variability observed in three populationsof D. g. mendotae and that genotypic frequency changes are notnecessary to explain seasonal changes in D. g. mendotae phenotype.     

Cyclomorphosis as a factor explaining success of a Daphnia hybrid in Tjeukemeer

Recent studies have shown that Daphnia hybrids are intermediate to their parental species for several life history traits, and that they combine advantageous traits of the parental species, thereby decreasing their risk of being preyed upon by planktivorous fish. In this study D. galeata, D. cucullata and their interspecific hybrid are compared with respect to cyclomorphosis and juvenile growth as a potential mechanism to avoid invertebrate predation. Helmets and tail spines are known to reduce predation risk, whereas fast juvenile growth reduces the period that Daphnia are vulnerable to predation. In laboratory cultures, I tested the hypothesis that, with regard to cyclomorphosis, juvenile hybrids are more comparable to the juveniles of D. cucullata, and with respect to growth rate, they are more comparable to D. galeata. The hybrid did not differ significantly from D. galeata in the time needed to reach 0.9 mm body length. In contrast, the relative spine and helmet length of juvenile hybrids were more comparable with those of D. cucullata, whereas in adult instars these characters were more similar to D. galeata. Thus during the first juvenile instars, the hybrids combine the relative long helmet and spine of D. cucullata, with the faster growth of D. galeata. This combination of characteristics might reduce hybrid vulnerability to invertebrate predation in field situations.     

Interspecific variation in ephippial size between Daphnia galeata and D. pulicaria in Lake Biwa,Japan

Limnology - Daphnia, keystone herbivores in lakes, routinely produce immediately hatching eggs; additionally, they also produce resting eggs enveloped by an ephippial case, a thickened carapace...     

Cyclomorphosis in Daphnia cucullata: morphometric and population genetic analyses

The cyclomorphic change of head and tailspine of Daphnia cucullatahas been analysed morphometrically and compared with temporalanalyses of enzyme variability. During June, round-headed animalsare rapidly replaced by specimens with high helmets; the rateof increase of the relative helmet length is more rapid thanthe rate of decrease later in the year. The relative sizes ofhelmet and tail spine are not always coupled. The tailspinelength remains approximately the same year round and grows withnegative allometry, so that small animals have the relativelylongest spines. In contrast, the helmet grows in a positivelyallometric fashion and exhibits high seasonal variation. Helmetgrowth is strongly correlated with water temperature but notwith food abundance. The morphometric results are consistentwith the hypothesis that helmet formation is a response to fishpredation while the tail spine provides protection against invertebratepredators. There is no indication of changes in the gene orgenotype frequencies at two loci during the period of rapidmorphological change. Thus cyclomorphosis apparently appearsin the absence of clonal replacement.     

Quaternary diversification in a sexual Holarctic zooplankter, Daphnia galeata

The effects of Quaternary glacial range partitioning on the diversification of Holarctic biota remain unclear. Glacial refugial lineages may form vicariant species, hybrid products, or merge after secondary contact. Here, we assess the effects of Quaternary glaciation on a Holarctic sexual zooplankter, Daphnia galeata, with apparently marked dispersal capacity and a widespread hybrid lineage in the New World. We collected samples of this species from 148 Holarctic lakes, analysed the nuclear and mitochondrial gene sequences, and tested predictions for hypotheses that account for the origin and spread of the New World D. galeata. We detected five nuclear phylogroups and four mitochondrial phylogroups, most of which were restricted to either the New World or the Old World. The oldest mitochondrial phylogroup was restricted to Japan. One major mitochondrial clade was distributed throughout the Holarctic, but only four haplotypes were shared among continents, and analysis of molecular variance indicated significant structure at the continental level. Haplotype sharing among continents could largely be attributed to anthropogenic introductions. Mismatch distributions, haplotype networks, phylogenetic trees, longitudinal haplotype diversity erosion and coalescence analyses are consistent with colonization from an Old World and a New World refugium. Our nuclear and mitochondrial DNA sequence evidence supports the hypothesis that the New World D. galeata underwent introgression with Daphnia dentifera, with dispersal being enhanced by glaciation. We conclude that Quaternary glaciation had a pronounced effect on the diversification of a Holarctic sexual zooplankter.     

Demography of a natural population of Daphnia retrocurva in a lake with low food quality

The hypothesis was tested that Daphnia exhibit low populationrecruitment in a lake with phosphorus (P)-deficient food, whereDaphnia populations failed to increase in response to greatlylowered minnow density. Egg ratio analysis was performed onDaphnia retrocurva from L110 of the Experimental Lakes Area,Ontario, in 1994. L110 has high food abundance (seston carbon(C) 100 µM C), but the seston is P deficient (C:P atomic- 600). Chrysophytes dominated the algal community. The fishcommunity in this lake was manipulated in 1993 and 1994 by theaddition of northern pike, Esox lucius. Zooplanktivorous minnowswere greatly reduced after the piscivore addition, but the expectedincrease in abundance of the Daphnia to this altered predationregime was not observed, If food quality constrains the responseof the Daphnia to changed predation, there should be low recruitment in the relatively sparse Daphnia population in this lake.Birth rates estimated by standard egg ratio analysis were <0.1day^–1 for most of the sample period. In comparison toannual averages from the literature, recruitment in L110 wasmoderately, but not dramatically, low. Daphnia exhibited pronounced‘normal’ vertical migration (up at night, down duringthe day) all year, and a strongly declining size at first reproductionthrough the season. Population density and birth rates seemedto show much less short-term change than previously observedin other lakes. Although the demo graphic predictions for foodquality constraints seemed clear, in situ demography unfortunatelyneither supported nor strongly rejected the overall hypothesisof food quality limitation in this lake with very high C:P ratios.Possibly, direct demographic effects of low food quality willbe difficult to observe in nature.     

Diversity of Daphnia galeata life history traits in a vertically structured environment

We used laboratory experiments to investigate the life historytraits of clonal lineages of Daphnia galeata isolated from twovertically segregated subpopulations in a deep dimictic reservoir:one from the epilimnion and the other from the deep hypolimnion.We collected clones twice for the experiments, first at thebeginning of thermal stratification in May and then towardsthe end of the season in September. The results for May showedlonger postembryonic development (PED), bigger eggs in the firstclutch and slightly higher somatic increments in the hypolimneticclones. In addition, a remarkable tendency to produce ephippiawas recorded in the hypolimnetic clones, but not in the epilimneticclones. In September, the results were reversed—hypolimneticclones had shorter PED, lower somatic increments and a slightlyhigher number of eggs in the first clutch. Our results suggesta differentiation of life history traits in the two D. galeatapopulations inhabiting contrasting microhabitats of a reservoiras a result of (i) different depth preferences of certain clonesin the beginning of thermal stratification in spring and (ii)divergent selection processes due to segregation in differentenvironmental conditions. The ability of Daphnia to live indiverse environments, causing divergent selection processes,enhances the overall phenotypic and genotypic diversity of thewhole reservoir population.     

Resource depression in Daphnia galeata, Daphnia cucullata and their interspecific hybrid: life history consequences

In this study, the effect of the food concentration on severallife history parameters of Daphnia galeata, Daphnia cucullataand the hybrid between these two species was examined. The foodconcentration had a significant effect on both growth and reproductionof all three taxa. Mortality was highly species specific, andto a lesser extent dependent on the food concentration. Changesin life history parameters resulted in changes in the intrinsicrate of population increase (r). The food dependence of thedifferent species was found to be different. Daphnia cucullatahad a relatively constant and low r. The r values for the hybridvaried most, with low values compared with the parental specieswhen grown at low food levels and relatively high values athigher food concentrations. Our results suggest that when foodconcentrations are high the hybrid will have a selective advantageover both parental species, but that at lower food levels D.galeatawill have an advantage over both D.cucullata and the hybrid.     

Reproductive effort in Daphnia galeata: comparison of reservoir and pond populations

Populations of Daphnia galeata from the deep stratified moderately eutrophic reservoir and the shallow highly eutrophic carp ponds differed in the reproductive effort of the first laboratory generation cultivated at a rich algal diet. The reservoir animals were smaller at the first adult instar and exhibited longer time between hatching of one brood and forming the eggs of the next one.     

Generational and dual-species exposures to invertebrate predators influence relative head size in Daphnia mendotae

Laboratory cyclomorphosis experiments with crustacean zooplanktonoften fail to produce morphological trait expression as extremeas that observed in field populations. A seven-generation laboratoryexperiment found that the maximum expression of relative headarea in a round-helmet morph of Daphnia mendotae was delayeduntil the third generation of non-lethal, chemical exposureto Leptodora kindtii. By the third generation and after, relativehead area remained high and comparable in degree to field specimens.The induction pattern from parents to offspring was statisticallypositive into the fourth generation. Published studies on kairomoneinduction of morphological trait expression extending only onegeneration may fail to measure transgenerational effects, whichcould account for mismatch between laboratory and field results.In a second laboratory experiment with a pointed-helmet morphof D. mendotae exposed to L. kindtii and Chaoborus punctipennis,we show that induction levels are not the same for all predatorsor combinations of predators. The maximum relative head areafor pointed morph individuals exposed to both predator cueswas still not as extreme in the laboratory as in the field.This is the first demonstration that delayed generational effectsof kairomone induction of helmet expression in the Cladoceracan reconcile laboratory experiments with the field observationsof cyclomorphosis.     

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.     

Feeding in Daphnia galeata on Oscillatoria limnetica and on Detritus Derived from It

Oscillatoria spp. are generally very abundant in many shallow,eutrophic lakes in the Netherlands. However, this is less truefor Daphnia galeata. The main aim of this study was to investigatewhether the edibility of live Oscillatoria limnetica by Daphniagaleata, and of the detritus derived from this filamentous cyanobacterium,was, among others, an important limiting factor for the daphnids.We measured the consumption and assimilation rates of Daphniausing dual-labelling radio-tracer techniques (¹⁴C and ³²P) tolabel separately the live Oscillatoria filaments and detritusprepared from these filaments. The two food types were mixedin different proportions, and both the food ingestion and foodincorporation rates by daphnids were measured. The main findingsof this study were that specific clearance rates of Daphniaon shorter Oscillatoria filaments were significantly higherthan on the longer filaments, in other words the weight-specificingestion rates were higher on the shorter Oscillatoria filamentsthan on the longer filaments from the batch cultures. The longerOscillatoria filaments are more likely to clump and, therefore,are more liable to be rejected by Daphnia during the food collectionand ingestion processes. The shorter filaments, in comparison,are apparently less prone to clumping and, therefore, are clearedby the daphnids at higher rates than the longer filaments. Feedingthe daphnids on double-labelled (¹⁴C and ³²P) shorter filamentsrevealed that the assimilationefficiency of shorter Oscillatoriafilaments was generally higher for P than for C, probably becauseof a high C/P ratio of Oscillatoria. Daphnia (0.75–1.85mm in size) fed significantly better on dead (detritus) Oscillatoriafilaments than on live Oscillatoria filaments, even if the relativeproportion of detritus in the food was only about one-quarterthat of the live filaments. This preference for detritus overlive Oscillatoria, as indicated by Chesson's selectivity coefficienta, was apparently a passive process, rather than a case of activefood selection. This ‘selective’ feeding on detrituswas apparently facilitated by the relatively greater rejectionof the live filaments than the detrital filaments. At very highfood concentrations (15–25 mg C l^–1), with the shareof the live Oscillatoria filaments 2 to 2.5 times greater thanthat of the detritus, the ingestion rates increased proportionallyless with increase in daphnid size than was expected on thebasis of the allometric relationship between the length andweight of these animals. This implies that the larger animalshad greater interfering effects of the Oscillatoria filamentson the food collection and ingestion processes.     

Swimming of Daphnia galeata x hyalina in response to changing light intensities: Influence of food availability and predator kairomone

Experiments showed that phototactic downward swimming in Daphnia galeata x hyalina as caused by a relative increase in light intensity (stimulus) is influenced by predator kairomone and food availability. The swimming responses at four different combinations of food availability and fish kairomone were analysed. Addition of both food and kairomone led to a significant increase in percentage of animals that responded to the light stimulus, but there was no significant interaction effect.We also found that kairomone and food had significant impact on displacement velocity and on the time between start of the stimulus and onset of the response.     

Morphological adaptations in filtering screens of Daphnia galeata to food quantity and food quality

We reared clones of the waterflea Daphnia galeata, a common grazer in many types of lakes, under several food regimes to study adaptations to feeding conditions in filter screen morphology and life history. As food regimes, we used low and high concentrations of the green alga Scenedesmus, a high concentration of the filamentous cyanobacterium Oscillatoria, and a mixture of Scenedesmus and clay. Natural seston from Lake IJsselmeer was also tested. Clones from two contrasting habitats (mesotrophic versus hypertrophic lake) did not differ in either population growth rate, r, or filtering structures. However, all the clones exhibited phenotypic plasticity when reared under low and high food concentrations. In relation to their body length, daphnids grew larger filter screens with longer setae in response to low food concentrations, thus enhancing filtering efficiency. Supplementing the low food concentration with inert clay particles had no effect on either the growth performance or filter screen morphology. In both cases, the growth and reproduction were low and filtering areas large. Filter screens were of intermediate size when daphnids were supplied with food supporting intermediate growth and reproduction. From these laboratory results, we concluded that the nutritional status of Daphnia is a more important cue for the phenotypic response of the filter screen morphology than particle concentration.      

Absence of sterols constrains carbon transfer between cyanobacteria and a freshwater herbivore (Daphnia galeata)

A key process in freshwater plankton food webs is the regulation of the efficiency of energy and material transfer. Cyanobacterial carbon (C) in particular is transferred very inefficiently to herbivorous zooplankton, which leads to a decoupling of primary and secondary production and the accumulation of cyanobacterial biomass, which is associated with reduced recreational quality of water bodies and hazards to human health. A recent correlative field study suggested that the low transfer efficiency of cyanobacterial C is the result of the absence of long-chain polyunsaturated fatty acids (PUFA) in the diet of the zooplankton. By supplementation of single-lipid compounds in controlled growth experiments, we show here that the low C transfer efficiency of coccal and filamentous cyanobacteria to the keystone herbivore Daphnia is caused by the low sterol content in cyanobacteria, which constrains cholesterol synthesis and thereby growth and reproduction of the herbivore. Estimations of sterol requirement in Daphnia suggest that, when cyanobacteria comprise more than 80% of the grazed phytoplankton, growth of the herbivore may be limited by sterols and Daphnia may subsequently fail to control phytoplankton biomass. Dietary sterols therefore may play a key role in freshwater food webs and in the control of water quality in lakes dominated by cyanobacteria.     

Contrasting migration behaviour of Daphnia pulicaria and D. galeata x hyalina, in avoidance of predation by 0+perch (Perca fluviatilis)

In spring and early summer, a small population of the large-bodied Daphnia pulicaria coexists with a much larger population of the medium-sized hybrid Daphnia galeata × hyalina in the epilimnion of Lake Maarsseveen (The Netherlands). When large shoals of juvenile perch (Perca fluviatilis) appear in the open water, both species start to migrate vertically. Since D. pulicaria has a larger body-size than D. galeata × hyalina, and is therefore competitive dominant over the hybrid, it is unlikely that both species interact via their common food resource, but they react both to fish predation. However, since they differ in size, and therefore in vulnerability for fish predation, both species adopt different strategies. The smaller bodied, and less vulnerable D. galeata × hyalina exhibits diel vertical migration ascending to the surface at dusk, and staying there during the night. In this way, benefiting from the higher temperatures of the surface layers. In contrast, the large-bodied, and more vulnerable D. pulicaria selects the deep cold hypolimnion water layers as refuge against fish predation. In this way it benefits from a safe habitat, free from fish predators, but on the other hand suffers from low water temperatures, which decrease its fitness. It is likely that the relatively higher temperature in the upper water layers serves as a proximate factor for the downward migration of D. pulicaria.     

Predation by underyearling perch (Perca fluviatilis) on a Daphnia galeata population in a short-term enclosure experiment

1. The predation impact of underyearling perch (20 mm total length) on the dynamics of Daphnia galeata was studied in three 6.5-m³ enclosures during a 17-day experiment in June 1995. These data were compared with zooplankton succession in three fish-free control enclosures and in the pelagic zone of Bautzen reservoir, Germany. 2. Due to individual growth during the experiment, fish biomass in the enclosures increased from 210 mg wet body mass (w.b.m.) m^–3 to 830 mg w.b.m. m^–3, equivalent to an increase from 20 kg ha^–1 to 75 kg ha^–1. 3. In the enclosures with fish, biomass of daphnids decreased steadily to values below 1 mg wet weight (w.w.) l^–1 within 17 days, whereas in the fish-free controls and in Bautzen reservoir the Daphnia biomass fluctuated around 8 mg w.w. l^–1. Other zooplankton species exhibited little or no change. Approximately 60 kg ha^–1 was calculated as the critical underyearling perch biomass which may induce a drastic decline of the Daphnia galeata population in Bautzen reservoir. Comparison with values from other lakes is difficult due to differences in water depths and Daphnia biomasses. 4. Mean individual biomass of daphnids, egg ratio and proportion of adult daphnids were significantly lower in the enclosures with fish compared with the control enclosures at the end of the experiment. This may be explained partly by preferential predation of the large, egg-carrying daphnids by fish. However, no difference was found in clutch size and size at first reproduction, possibly due to the short duration of the experiment. 5. It must be assumed that the ‘summer depression’ of daphnids observed in many waters is not the exclusive effect of direct reduction of daphnids by fish predation. Even the high biomass of underyearling perch stocked in the enclosures did not completely account for Daphnia mortality. Instead, the selective loss of large size classes, combined with low food resources and reduced reproduction rates, may induce the marked declines in daphnids.