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.     

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.     

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     

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.     

Combined Effects of Algal (<Emphasis Type="Italic">Chlorella vulgaris</Emphasis>) Food Level and Temperature on the Demography of <Emphasis Type="Italic">Brachionus havanaensis</Emphasis> (Rotifera): a Life Table Study

We evaluated the combined effects of food (0.5 × 10⁶, 1.0 × 10⁶ and 2.0 × 10⁶ cells ml⁻¹ of Chlorella vulgaris) and temperature (15, 20 and 25 °C) on life history variables of B. havanaensis. Regardless of Chlorella density there was a steep fall in the survivorship of B. havanaensis at 25 °C. Both food level and temperature affected the fecundity of B. havanaensis. At any given food level, rotifers cultured at 15 °C showed extended but low offspring production. At 25 °C, offspring production was elevated, the duration of egg laying reduced and the fecundity was higher during the latter part of the reproductive period. The effect of food level was generally additive, at any given temperature, and higher densities of Chlorella resulted in higher offspring production. Average lifespan, life expectancy at birth and generation time were 2–3 times longer at 15 °C than at 25 °C. At 20 °C, these remained at intermediate levels. The shortest generation time (about 4 days) was observed at 25 °C. Gross and net reproductive rates and the rate of population increase (r) increased with increasing temperature and generally, at any given temperature, higher algal food levels contributed to higher values in these variables. The r varied from 0.11 to 0.66. The survival patterns and lower rates of reproduction at 15 °C suggest that the winter temperatures (10–15 °C) prevailing in many waterbodies in Mexico City allow this species to sustain throughout the year under natural conditions.     

Zooplankton-induced unicell-colony transformation in Scenedesmus acutus and its effect on growth of herbivore Daphnia

The effects of colonial ecomorphs of the green alga Scenedesmus acutus on growth of Daphnia cucullata and D. pulex were examined. In ecologically relevant densities (up to 200 animals l^-1) the relatively small D. cucullata did not induce colony formation in Scenedesmus acutus, whereas the larger congener D. pulex significantly promoted colony formation. Both clearance rate and population growth rate (r) were significantly lower in D. cucullata when fed colonial Scenedesmus then when fed unicellular food. However, for D. pulex no effects of food type were observed. These results show that large Daphnia may influence its food in such a way that smaller congeners and competitors are negatively affected.     

Population dynamics of daphnia pulex and utilization by the rainbow trout (salmo gairdneri)

The effect of rainbow trout (Salmo gairdneri) predation on the population dynamics of the water flea,Daphnia pulex, was examined during 1976 and 1977 in Becker Lake, a small, shallow, productive reservoir in northeastern Arizona.Rainbow trout were size-biased feeders, utilizing daphnids which were 1.3 mm in size or larger. Trout predation uponDaphnia pulex occurred mainly during winter and early spring when their numbers were relatively low but their clutch size high, suggesting that trout selectedDaphnia on the basis of brood pigmentation. By far the greatest proportion ofDaphnia mortality was due to nonpredatory sources, since generally less than 6% could be attributed to trout predation.TheD. pulex population exhibited a bimodal seasonal abundance curve which was attributed to ephippial egg production and trout predation during the winter and poor food quality/quantity during the summer.This work was supported in part by the Arizona Department of Game and Fish. The authors wish to thank Jim Novy and Joe Stone of that department for their invaluable assistance in the field collecting segment of this study.     

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.     

Influence of diet on life table parameters of <Emphasis Type="Italic">Iphiseius degenerans</Emphasis> (Acari: Phytoseiidae)

Studies on the reproduction, longevity and life table parameters of Iphiseius degenerans (Berlese) were carried out under laboratory conditions of 25 ± 1 °C, 75 ± 5% RH and 16L:8D h. As food sources for the predatory mite, Ricinus communis L. pollen, all stages of the spider mite Tetranychus urticae Koch, Frankliniella occidentalis (Pergande) larvae, and Ephestia kuehniella Zeller eggs were selected. All diets were accepted as food by the adult mites. Female longevity ranged from 29.5 to 42.4 days, the highest value was recorded on a diet of Ephestia eggs. The highest percentage of females escaping the experimental arena was observed on the diet consisting of thrips larvae. The highest oviposition rate (1.9 eggs/female.day) was recorded when the predator was fed on spider mites on an artificial substrate. For other diets, oviposition rates ranged from 1.0 to 1.3 eggs/female.day. The intrinsic rate of natural increase (r _m) of I. degenerans varied between 0.015 and 0.142 females/female.day. The diet consisting of castor bean pollen resulted in the highest population growth whereas the diet on spider mites brushed off onto a bean leaf arena resulted in the slowest population growth. This can be explained by the inability of the predator to cope with the webbing of T. urticae, and the high escape rate of the progeny when reared on spider mites. The percentage of females in the offspring ranged from 40 to 73%.This revised version was published online in May 2005 with a corrected cover date.     

Population dynamics of the collared lemming and the tundra vole at Pearce Point,Northwest Territories,Canada

From 1987 to 1989 we monitored population changes during summer of the collared lemming (Dicrostonyx groenlandicus) and the tundra vole (Microtus oeconomus) at Pearce Point, Northwest Territories, Canada (69° 48 N, 122° 40 W). Populations on four study areas did not cycle but remained at low density (<3/ha) each year and continued at low numbers for the following 3 years (Reid et al. 1995). Lemming numbers often declined throghout the summer in spite of continous reproduction, and population recovery occurred overwinter. Heavy predation losses of radio-collared lemmings occurred each summer and this lemming population may be trapped in a predator-pit. Collared lemmings breed in winter and only because of winter population growth do these populations persist. Tundra vole numbers increased rapidly in most summers but usually declined overwinter. Tundra voles do not seem able to sustain winter reproduction in this extreme environment and this prevents them from reaching high density because of the short summer. Population growth in both these rodents could be prevented by poor food or by predation losses, and landscape patchiness may also help to prevent population growth. For lemmings we do not think that a shortage of shelter or intrinsic limitations could be restricting population increase at Pearce Point. This is the first detailed study of a non-cyclic collared lemming population.     

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.     

Effects of food limitation and temperature on cladocerans from a tropical Brazilian lake

Food limitation was tested in the laboratory by individual growth and reproduction of two cladoceran species, Ceriodaphnia richardi and Daphnia gessneri, from the shallow tropical Brazilian Lake Monte Alegre. The cladocerans were fed cultivated green alga Scenedesmus spinosus in concentrations of 0.20, 0.10, 0.05, and 0.025 mg C l⁻¹. Higher biomass and growth rates occurred in the two highest-food concentrations; the two lowest ones negatively affected clutch size and first reproduction. The threshold food concentration is lower than 0.025 mg C l⁻¹ and the incipient limiting level is a value between 0.10 and 0.20 mg C l⁻¹. The largest species, D. gessneri, was more sensitive to low food concentrations. The effects of low and high temperatures (19 and 27°C) were evaluated by life table experiments with three cladocerans from the lake—Daphnia ambigua, D. gessneri, and Moina micrura—with no food limitation (1 mg C l⁻¹ of S. spinosus). Higher population growth rates for the three species were found at 27°C; better performance in most life table parameters was observed for the former two species at the highest temperature, D. gessneri being the most sensitive to the lowest temperature. There are indications that temperature is an important abiotic factor that constrains populations of cladocerans for a short period in winter in the lake, when temperature decreases to 18–19°C. However, its influence cannot be separated from a biotic factor such as food, whose effect is stronger in the cool season, when concentrations are lower and contribution of inedible algae is relatively higher.     

Fecundity,reproduction, and growth of Moina macrocopa fed different algae

Three micro algae, Ankistrodesmus convolutus, Scenedesmus incrassatulus and Chlorella vulgaris, at three concentrations, were tested as diets for Moina macrocopa. Their effect on reproduction, fecundity, growth and survival was evaluated. All three algae satisfied the nutritional requirements of M. macrocopa, despite their difference in size. The best concentration, expressed in dry weight, was 5 mg l^–1 for all three. Time to first reproduction was 4 days with all diets. Average time between clutches was 33 hours, and maximum number of clutches was 12; the highest average number of offspring per brood was 27. The largest broods were the fourth to sixth, depending on the diet. Ephippium hatching depends on temperature, taking only 24 hours at 30 °C and 48 hours at 27 °C. This species could be an important test organism in aquatic bioassays, and a live food in aquaculture.     

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.     

Trophic ecology of an aquatic mite (<Emphasis Type="Italic">Piona carnea</Emphasis>) preying on <Emphasis Type="Italic">Daphnia pulex</Emphasis>: effects of predator density,nutrient supply and a second predator (<Emphasis Type="Italic">Chaoborus americanus</Emphasis>)

As compared to other aquatic invertebrates, relatively little is known about the ecology of predaceous, pelagic water mites. Studies to date do, however, show that water mites can be important components of aquatic food webs. Here, we used manipulative field experiments to better understand the trophic ecology of a predaceous water mite (Piona carnea). Three experiments were conducted that examined (i) the effect of P. carnea density on the per-capita interaction strength (PCIS) of P. carnea preying on zooplankton; (ii) how the effects of P. carnea predation change with prey productivity; and (iii) how P. carnea interacts with another pelagic predator (Chaoborus americanus) to affect a shared prey species (Daphnia pulex). Results from the first experiment showed that P. carnea can strongly impact D. pulex populations, and that the PCIS of P. carnea decreases with an increase in P. carnea density. The second experiment showed that the effects of P. carnea on D. pulex populations depend on bottom-up factors that influence D. pulex population biomass and the reproductive potential of a D. pulex population relative to its size. The third experiment uncovered a non-additive interaction between P. carnea and C. americanus that resulted in a risk reducing situation for D. pulex in the presence of both predators. Together these experiments show that P. carnea imposes a strong negative impact on D. pulex, that the magnitude of this negative impact is dependent on the P. carnea density and the productivity of the system, and that the trophic ecology of P. carnea is modified by coexisting predator species.     

The influence of predator regime on reproductive traits in <Emphasis Type="Italic">Gammarus</Emphasis> <Emphasis Type="Italic">pulex</Emphasis> populations

Selection on traits conferring reduced predation may be opposed by selection on other traits associated with reproduction. Here, we examined the hypothesis that traits associated with reproduction in Gammarus pulex are driven by predation. We studied G. pulex originating from ponds with two different kinds of predator regimes: (1) ponds with fish—often large, non-gap-limited predators and (2) ponds without fish where invertebrates are the dominant predators—often small, gap-limited predators with a much more restricted prey size range. We examined the body size of males and females in G. pulex amplexus pairs originating from fish and fishless ponds. We also examined, in the laboratory, their mating success, the number of offspring per female and offspring mortality under different rearing conditions, with or without fish cue. Mating success, defined as the percentage of amplexus pairs that produced live offspring, was higher for G. pulex from fishless ponds independent of rearing condition. Individuals from fish ponds were larger and they produced a higher number of offspring which tended to be related to female body size. Offspring mortality was higher in populations from fish ponds compared to populations from fishless ponds. Despite the higher offspring mortality, females from fish ponds had a higher number of offspring alive after 13 weeks, which is the approximate time it takes for G. pulex to reach maturity. Our data imply that no trade-off between reducing body size to reduce mortality caused by fish and maximising reproductive success exist in G. pulex from fish ponds. The strategy with many offspring may be the correct strategy in fishponds where predation pressure generally is higher than in fishless ponds.     

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.      

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.     

Species-specific population-density thresholds in cladocerans?

The population density of a Daphnia species seems more dependent on properties specific to the species than on those specific to the point in the season, location within a lake basin or the given lake itself. In spite of week-to-week fluctuations, the population density for each of two common European Daphniaspecies was found to be remarkably similar within single lakes (from station to station on a single date, and from date to date at a single station) as well as from lake to lake, regardless of trophic state. All lakes on all dates revealed densities in the range 10–50 ind l^–1 for the smaller-bodied D. cucullata and 1–5 ind l^–1 for the larger-bodied D. hyalina, in spite of different intensity of reproduction resulting from different food levels (chlorophyll a between 0.2 and 4.2 g/l). It can be asserted that the population density of each species remains far below the carrying capacity of the habitat K, and does not depend on food levels, which merely set the rate of population increase, while the population density reflects the species' vulnerability to predation by planktivorous fish. The reactive distance (the distance over which a foraging fish can see its prey) in 1+ roach, a dominant planktivore in the lakes studied, has been found to be twice as great for D. hyalina as for D. cucullata, whatever the light intensity. The relative reactive field volume was therefore an order of magnitude greater for the former than for the latter, showing that the densities of the two prey species would be assessed by a foraging roach as equal when, in reality, they differed by an order of magnitude, as they do in various lakes and in various seasons.The first of the two conclusions is that whatever the growth and reproduction in a population of a cladoceran such as Daphnia, its density would be fixed by mortality induced by fish predation. The second would be, that the difference between the bottom-up and top-down effects in freshwater is more than merely the upward or downward direction along the food web, since the bottom-up effects are about the flow control (the rate of net production, individual growth rate, rate of reproduction) and the top-down about the standing-crop control (biomass, individual body size, population density level).     

Application of individual growth and population models of Daphnia pulex to Daphnia magna, Daphnia galeata and Bosmina longirostris

Daphnia models for individual growth and population dynamics have been developed in the manner of models developed by Gurney, McCauley, Andersen and others. All or most of the earlier models were parameterized for Daphnia pulex; we have used the D. pulex model as a baseline model for other species of Daphnia such as magna, galeata and also Bosmina longirostris. Because of the lack of ample data for D. magna, D. galeata and B. longirostris, some of the physiological data had to be relied on the other species whose data were available and in some case calibrated. We were able to produce reasonable results for individual growth as well as population dynamics under the controlled laboratory conditions. Most of the results were compared with the available laboratory data for population as well as growth. All the simulations have been done under high and low food concentrations. The animals are assumed to be feeding on green algae (Chlamydomonas reinhardtti) under the laboratory conditions of 18–20°C. The continuous growth until the end of the life was observed in smaller B. longirostris, whereas rapid growth in the beginning and slower after the start of the reproduction was observed in Daphnia species. The smaller species matured earlier than larger species. B. longirostris population sustained better than Daphnia species in medium food concentrations.