Warming erodes individual-level variability in life history responses to predation risk in larvae of the mayfly Cloeon dipterum

1. Warming and predation risk are ubiquitous environmental factors that can modify life histories and population dynamics of aquatic ectotherms. While separate responses to each of these factors are well understood, their joint effects on individual life histories and population dynamics remain largely unexplored. Current theory predicts that the magnitude of prey behavioural, physiological, and life history responses to predation risk should diminish with warming due to the reduced metabolic scope. However, empirical support for this prediction remains equivocal, and experiments covering a substantial proportion of individual prey ontogeny until maturation are lacking.
2. To fill these gaps, we ran a laboratory experiment to investigate how warming and non-consumptive predation risk influence life history responses in the larvae of the mayfly Cloeon dipterum, an aquatic insect with highly plastic development. We reared larvae of varying initial sizes at three temperatures (21, 24, and 27°C) in a risk-free environment and under predation risk signalled by chemical cues from dragonfly larvae (Aeshna cyanea), and followed their individual survival, growth, and development until emergence.
3. Some C. dipterum larvae substantially prolonged their development and the proportion of these slow individuals declined rapidly with temperature and increased with predation risk. We attribute this response to cohort splitting, a common life history strategy of aquatic insects and other taxa in unpredictable environment.
4. Growth, development, and maturation varied predictably with temperature in the fast larvae that did not prolong their development. They grew and developed faster but matured at smaller sizes with increasing temperature. Predation risk tended to slow down individual growth and development in line with the reduced metabolic scope hypothesis, but the differences were relatively minor and observable only at 21°C.
5. Survival to subimago increased with predation risk, possibly due to indirect effects mediated by dissolved micronutrients, but did not vary significantly with temperature. Survival also tended to be higher in the slow individuals. This partly compensated for a smaller final size relative to the fast individuals and made both strategies comparable in overall fitness.
6. Our results show that warming may erode individual-level variability in life history responses to predation risk. This implies that warming can synchronise population dynamics and consequently make such populations more vulnerable to unpredictable disturbances.

     

The influence of climate change scenarios on populations of the mayfly Cloeon dipterum

Populations of the mayfly Cloeon dipterum from 48 ponds (3000 l fibre-glass tanks of 1 m depth) were monitored over the course of 1 year. To simulate possible patterns of climatic change, the ponds were subject to three temperature treatments: continuous heating to 3 °C above ambient; heating to 3 °C above ambient during the summer only; and no heating. Further experimental complexity included enhanced nutrient input into the ponds and the presence or absence of fish, giving a factorial combination of 3 temperature regimes × 2 nutrient levels × presence/absence of fish predation.Few nymphs were found in the presence of fish. Where fish were absent, the temperature treatments did not significantly affect nymph abundances, and only marginally influenced mean nymph body-lengths. In contrast, the nutrient treatment had significant effects on both nymph abundance and size, with greater numbers of generally larger nymphs occurring in those fish-free ponds receiving additional nutrients. Adult emergence began earlier in the year from the heated ponds, particularly those ponds receiving additional nutrients. Adult body-length differed between temperature treatments, but consistent patterns were difficult to ascertain because of interactions with nutrient treatment and seasonal effects.Our results show that during the short term at least, elevated temperature as a simulation of climate change does not have an overwhelming influence on either mayfly abundance or size. The influence of temperature is subtle and subject to complex interaction with other habitat variables. We therefore suggest that the direct consequences of small changes in temperature will likely be of little significance to C. dipterum, relative to indirect effects operating through interactions with predation and nutrient input.     

Effects of food quality on life history of the rotifer Brachionus calyciflorus Pallas

1. Herbivorous zooplankton face considerable temporal and spatial variation in food quality, to which they respond by adapting their life histories. Zooplankton may even take up mineral nutrients directly, and use these to counter the effects of algal nutrient limitation (mineral compensation). This study examined the life history of the rotifer Brachionus calyciflorus fed phosphorus‐, and nitrogen‐limited Scenedesmus obliquus (Chlorophyta), and investigated whether B. calyciflorus was capable of mineral compensation. 2. Both phosphorus‐ and nitrogen‐limited algae gave similar life history responses: somatic growth and reproduction were reduced, whereas lifespan remained unaffected. 3. No evidence was found for mineral compensation in B. calyciflorus in relation to detrimental life history effects, so mineral compensation does not seem to be relevant for this species under field conditions. 4. The similarity in life history responses of B. calyciflorus and the low levels of ω‐3 PUFAs in both phosphorus‐ and nitrogen‐depleted algae suggest that ω‐3 PUFAs were limiting to B. calyciflorus, although other (bio)chemicals or mineral nutrients may also have been important. 5. No trade‐off was observed between life span and reproduction during algal nutrient limitation. Reduced population growth rates of B. calyciflorus were caused by shorter reproductive periods.     

Salinity and temperature influence in rotifer life history characteristics

A review of temperature and salinity effects on rotifer population dynamics is presented together with original data of these effects for three clones of Brachionus plicatilis. There is a clear relationship between temperature and the intrinsic rate of increase, r: an increase of temperature — within the natural environmental range — produces an exponential increase of r, and the slope of the response depends on the genotype. The effect of salinity is also genetically dependent; the highest r for each clone is observed at the salinity close to that of its environmental origin. The response of r to temperature is mainly a consequence of the response of the individual rates of development and reproductive timing. The effect of temperature on fecundity (number of descendents per individual life time) is negligible when temperature values are within the normal habitat ranges. On the other hand, salinity seems to affect primarily fecundity. The interaction salinity-temperature may be important in clones or species living in fluctuating environments with positive response to the more frequent combinations found in the corresponding habitats.     

Effects of aluminum,calcium and low pH on egg hatching and nymphal survival of Cloeon triangulifer McDunnough (Ephemeroptera: Baetidae)

Laboratory experiments were conducted to assess the effects of aluminum, calcium and low pH on egg hatching and nymphal survival of the mayfly Cloeon triangulifer. Percent successful hatch (living nymphs breaking free of the chorion) decreased and percent partial hatch (nymphs dying attached to the chorion) increased with increasing acidity (pH 7.5–3.0). Most hatches occurring below pH 5.0 were partial hatches. Decreased time of exposure to acidic waters increased percent successful hatch and decreased percent partial hatch. Time to first hatch was not affected by pH. Eggs were incubated in acidic waters (pH 4.0 and 5.5) with additions of calcium (10 and 100 mg l^–1) and aluminum (100 and 500 g l^–1). Aluminum decreased percent successful hatch and increased percent partial hatch and calcium increased both percent successful hatch and percent partial hatch. Time to first hatch was increased by both aluminum and calcium. The 96 h LC50 for small nymphs was pH 4.75. Addition of aluminum (100 and 500 µg l^–1) to acidic waters (pH 4.0 and 5.0) reduced nymphal mortality by 8–22%. Toxic effects of low pH on egg hatching and early nymphs may contribute to the absence of mayflies from acidified habitats.Contribution No. 1469 of the Maine Agricultural Experiment Station, University of Maine, Orono, Maine 04469 USA.Contribution No. 1469 of the Maine Agricultural Experiment Station, University of Maine, Orono, Maine 04469 USA.     

The synergistic effects of temperature and food concentration of life history parameters of Daphnia

Summary Daphnia parvula experiences a wide range of thermal (4°–30°C) and food conditions during its annual population cycle. We used cohort life table experiments to determine the synergistic effects of temperature and food concentration on its life history parameters. A 3×3 factorial design experiments was conducted with animals raised at all combinations of three naturally experienced temperatures (10°, 15° and 25° C) and food levels (0.02, 0.20 and 2.0 mg C/l). D. parvula showed an increase in survivorship with decreasing temperature at all food levels. Fecundity parameters (number of broods/female, brood size and net reproductive rate) increased with increasing food at the two lower temperatures but showed a mid-range food optimum at the highest temperature. Development rates and realized rates of increase (r) showed an increase with both increasing temperature and food such that they were maximum at the highest temperature-food level treatment. The life history parameters, average lifespan, age at first reproduction, brood duration time, brood size and number of young per reproductive female all showed significant interaction between temperature and food as was suggested by trends in R _o and r. Temperature had a reduced effect on fecundity, development rates and realized rates of increase at the low food level.Population birth rates of continuously reproducing zooplankton are typically calculated by the egg-ratio method (Edmondson 1960) and are based on thermally controlled development rates which neglect the effects of food limitation. Significant synergistic temperature-food effects on brood duration time and other life history parameters of Daphnia parvula suggest that food limitation and foodtemperature interaction should be considered when calculating field population birth rates. A comparison of realized rates of increase from this study with similar life table data for Daphnia parvula raised on natural food from Lake Oglethorpe indicate that synergistic effects are negligible in this eutrophic system due to abundant resources. However, synergistic effects are probably important in oligotrophic systems where resources are limited.This work was supported by National Science Foundation Grant DEB 8005582. Lake Oglethorpe Limnological Association, Contribution No. 24 and Harbor Branch Foundation, Inc. Contribution No. 369     

Antipredator reaction norms for life history traits in Daphnia pulex: dependence on temperature and food

Synergistic effects between temperature and food level on the vulnerability of Daphnia life histories to predation have previously received little attention, despite their potential significance for summer population dynamics. In this investigation, most traits in the early life history of Daphnia pulex altered in response to increasing concentrations of fish kairomone. Although there was some variation attributable to experimental temperature and food treatments, traits exhibited reaction norms which suggested at least some degree of kairomone dose-dependence. Temperature, food level and their interaction affected the mean values of every trait examined and in some cases also influenced the antipredator response via a three-way interaction with fish kairomone. The insertion of an extra juvenile instar resulted in later maturation at a larger size for most females raised under conditions of low temperature and low food, but this response was largely suppressed in the presence of fish kairomone. Earlier maturation due to deletion of an instar was observed most frequently under high food and temperature conditions with fish kairomone present, suggesting an effect of kairomone on the size threshold for reproductive development. Principal components analysis was used to produce an index reflecting the net potential vulnerability to fish predation of the suite of life history traits. Vulnerability generally declined with increasing kairomone level as a result of the apparently adaptive alterations in most life history traits. Raised temperature and food level also generally reduced potential vulnerability, but a highly significant interaction between these factors was also found. Potentially important implications of these results for optimal vertical migration and summer population dynamics are discussed.     

The rowing-to-flapping transition: ontogenetic changes in gill-plate kinematics in the nymphal mayfly Centroptilum triangulifer (Ephemeroptera, Baetidae)

Comparative studies encompassing a wide range of aquatic animals have shown that rowing is exclusively used at low Reynolds numbers ( Re  < 1), whereas flapping is predominantly used at Re  > 100, although few studies have been undertaken to document the transition in individual species that traverse the intermediate Re regime using a single set of appendages. Thus, it is not generally known whether a gradual increase in Re within a system results in a gradual or sudden shift between rowing and flapping. In the present study, we document ventilatory kinematics of a nymphal mayfly Centroptilum triangulifer that develops using a serial array of seven pairs of abdominal gill plates and operates at Reynolds numbers in the range 2–22 during ontogeny. We found that some kinematic variables (stroke frequency and metachronal phase lag) did not change during ontogeny but that others changed substantially. Specifically, gill kinematics in small instars used strokes with large pitch and stroke-plane deviations, whereas larger instars used strokes with minimal pitch and minimal stroke-plane deviation. Gills in larger instars also acquired an intrinsic hinge that allowed passive asymmetric movement between half strokes. Net flow in small animals was directed ventrally and essentially parallel to the stroke plane (i.e. rowing), whereas net flow in large animals was directed dorsally and essentially transverse to the stroke plane (i.e. flapping). The change in whole-gill kinematics from rowing to flapping occurred across a narrow Re range (3–8), which suggests a possible hydrodynamic demarcation between rowing and flapping.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 540–555.     

Combined effects of food shortage and oxygen deficiency on life history characteristics and filter screens of Daphnia

Daphnia magna were reared in environments with different concentrationsof food and dissolved oxygen, and their life history characteristicsand filter-screen areas were analyzed. Both low food concentrationand low oxygen concentration degraded Daphnia fitness (as measuredby individual growth and reproduction), and synergism was detectedstatistically for the effects of the two factors together. Lowfood concentration induced the development of large filter screensin Daphnia, but this development was suppressed by low oxygenconcentration, suggesting that low oxygen concentration reducesthe filtering rate of Daphnia in a food-limited environment.Therefore, energy uptake by Daphnia seems to be reduced by foodshortages and oxygen deficiencies jointly, and this reductionin energy uptake may be a possible mechanism causing the synergisticeffects of the two environmental stresses on the life historyof Daphnia.     

Effects of temperature, salinity and food level on the life history traits of the marine rotifer Synchaera cecilia valentina, n. subsp.

A strain of the marine rotifer Synchaeta cecilia valentina,n. subsp., isolated from the Hondo of Elche Spanish Mediterraneancoastal lagoon at 22 salinity, was cultured in the laboratoryin 20 ml test tubes and fed with the alga Tetrasemis suecica.The effect of two temperatures (20 and 24°C), four salinities(20,25,30 and 37) and two food levels (15 000 and 25000 cellsml^–1) on the life history traits of this rotifer werestudied in life tables performed with replicated individualcultures. Temperature and salinity had a significant negativeeffect (P < 0.001) on the average lifespan (LS) and on thenumber of offspring per female (R₀) The effect of food levelon LS is unclear, whereas R₀ is greater at 20°C with thelower concentration of algae and at 24°C with the higheralgal concentration. The maximum values of LS and R₀, 5.6 daysand 9.2 offspring per female, respectively, were recorded at20°C, 25o salinity and low food concentration. There isalso a clear negative effect on the intrinsic growth rate (r)due to salinity. The effect of temperature depends on the foodlevel and, as occurs with R₀ the maximum values of r occur withthe lower algal concentration at 20°C, whereas at 24°Cthey are obtained with the higher algal concentration. Theser values, from 1.04 to 1.10 day^–1, were reached at 24°C,salinities of 20–25 and with high food concentration.     

Influence of diet on growth,food retention time,and gill ventilation rate of nymphs of Cloeon sp. (Ephemeroptera: Baetidae)

Early instar nymphs of the mayfly, Cloeon sp. were kept on an algal or a detrital diet at 20 ± 1 °C in the laboratory. A control group was not given any food. Nymphs kept on algae showed significantly (P = 0.001) higher growth both in terms of length and biomass than for those kept on detritus. None of the nymphs given algae or detritus died during the experiment, and 40 per cent of those fed algae and 20 per cent fed detritus reached maturity by the termination of the experiment. Food retention time as well as gill ventilation rate of nymphs feeding on algae were significantly (P = 0.001) higher than those feeding on detritus. It is probable that these two factors largely enabled the nymphs to survive as well as to grow and reach maturity, though relatively slowly, solely on a detrital diet. However, algae was clearly shown to be a superior food resource for Cloeon sp. nymphs.     

Automictic parthenogenesis of a geographically parthenogenetic mayfly,Ephoron shigae (Insecta: Ephemeroptera,Polymitarcyidae)

In the geographically parthenogenetic mayfly, Ephoron shigae, egg maturation and counts of chromosome number of unfertilized, parthenogenetic eggs were studied, in comparison with fertilized eggs from a bisexual population. The primary oocyte becomes mature through two successive maturation divisions. The first maturation division (meiotic division) takes place in the primary oocyte to produce a secondary oocyte and a first polar body. The second maturation division soon occurs in the secondary oocyte, in which the nucleus is divided into a mature egg nucleus (female pronucleus) and second polar body nuclei. The first polar body, in some cases, was successively divided into two polar bodies; in other instances, it was not divided. After the successive maturation division, the egg nucleus and the sister second polar body nucleus drew near to fuse into the zygote nucleus. The chromosome number was doubled in the zygote, and this conjugation initiates subsequent embryonic development. This suggests that, in E. shigae, the process of parthenogenetic recovery of diploidy is the automictic type categorized as the ‘terminal fusion’ pattern. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 335–343.     

Trade-offs in the life history and energy budget of the parthenogenetic collembolan Folsomia candida (Willem)

Three clones of Folsomia candida from different locations in Europe were compared in four experiments investigating genetic and phenotypic correlations between life-history traits. The first three experiments focused on the effects of food type, clone and temperature on traits associated with the first clutch. Differences in clutch size between clones and treatments were almost completely attributable to body size. Clones differed in length of the juvenile period, but the difference decreased at low temperatures. Age and weight at first reproduction were negatively correlated in the food type experiment and positively correlated in the temperature experiment, an often-encountered result for which no general explanation is as yet available. In the temperature experiment egg size variation was considerable, and was highest at low temperatures. The fourth experiment, with two clones at two feeding levels, aimed at finding trade-offs, in particular between reproduction and survival. It was hypothesized that higher fecundity led to increased scenescence through a higher metabolic rate. The trade-off was clearly present among the clones: one combined fast growth, late reproduction and high lifetime fecundity with lower survival, while in the other the relation between these traits was opposite. The proposed mechanism, however, was not confirmed, as no difference in metabolic rate was found. The effect of food level was too small to result in significant differences in the life-history traits in either of the clones.     

Effects of temperature on gut-loading and gut-clearing times of the burrowing mayfly, Hexagenia limbata

SUMMARY. The effect of temperature on gut-loading times, gut-clearing times, and the calculated ingestion rates, egestion rates, and consumption indices of the deposit-feeding burrowing mayfly, Hexagenia limbata , were investigated in laboratory experiments. Rates of movement of two natural sediments of differing colour through the digestive tract were monitored to quantify feeding intensity when ambient water temperatures approached 5, 10, 15, 20, and 25°C.
At each temperature, gut-loading times (GLT) and gut-clearing times (GCT) increased as nymph length increased. Mean GLT and GCT values decreased as temperature increased from 5 to 20°C but were longer at 25°C than at 20°C. Relationships between GLT, GCT, and length of nymphs and temperature were best described by multiple regression equations. No diel variation in gutclearing times was observed. Low water temperatures resulted in lower ingestion and egestion rates and consumption indices. At most temperatures nymphs ingested over 100% of their dry body weights per day.     

Effects of temperature on life history variables in perch

Population structure, recruitment, mortality, life expectancy, age at maturity, gonad development, fecundity, net reproductive rate and energy storage were studied in a perch population exposed to thermal discharge. The experiment was conducted during 1978–1990 in an artificial enclosure at a nuclear power plant on the Baltic Sea coast. Abundance increased after the plant started operating, although the proportion of larger perch dropped to a low level. Recruitment improved, but adult mortality increased. This effect was accentuated as the fishes matured very early and at a very small size, reducing their ability to support a growing gonad in high winter temperatures. During the spawning period, condition dropped to very low levels accompanied by increased mortality. Surviving fish delayed the next spawning by one or more years and reduced their fecundity. Body condition thus improved in large perch at the end of the study period. Life-time fecundity was reduced, and reproductive performance shifted to youner ages.     

The influence of temperature on life history traits in the Iberian slug,Arion lusitanicus

The slug Arion lusitanicus is an invasive species which has recently become established in many European countries and is considered a serious pest, both in agriculture and private gardens. The effect of temperature on growth rate, survival, egg developmental time and hatchability of the slug are reported. The growth rate was positively correlated with temperatures up to 20°C and A. lusitanicus continued (on average) to grow until they die. A model describing how growth depends on temperature was developed, and a field survey found that the predicted growth matched the observed with reasonable accuracy. This study confirms the assumption that A. lusitanicus die after egg laying. Free‐ranging A. lusitanicus has an annual life cycle, but our data show that slugs also possess the ability to live for up to 3 years. The egg developmental time was, like growth, positively correlated with temperature and was shortest at 20°C, but the optimum temperature for egg development, when regarded as the temperature with highest hatchability was found to be 10°C. In conclusion, this study has shown that growth and the life‐history traits, egg developmental time and hatchability, of A. lusitanicus are highly influenced by temperature. However, data also show that temperatures within the range 2–20°C did not influence survival rates to any large degree, and that A. lusitanicus can quickly adjust to changes in temperature. The study provides a number of basic parameters which contribute to the understanding of the population dynamics of A. lusitanicus.     

Influence of temperature on the production of parthenogenetic and sexual females by Aphis fabae under short-day conditions

Leafdiscs of broadbean, Vicia faba, were used to raise successive generations of the black bean aphid, Aphis fabae, under short-day conditions (10 hr light per day) at different constant temperatures. The progeny of apterous virginoparae that were temporarily crowded consisted mainly of alatae at 11.5° and 15.5° C, alatae and apterae at 17.5°–25.5°, and apterae only at 28.5°. All of the apterae were virginoparae. At 11.5°–19.5° all of the alatae were gynoparae (produced at least one ovipara). From 22.5°–25.5° the proportion of gynoparae among the alatae declined from 96% to 8%. At 11.5° the gynoparae exclusively produced oviparae. At 15.5°–23.5° some gynoparae gave birth both to virginoparae and other gynoparae after depositing a number of oviparae. At 22.5° a few males were also produced by some gynoparae. Gynoparae therefore produced alate and apterous virginoparae, males, gynoparae, as well as oviparae under constant conditions favoring ovipara production. Alate virginoparae also produced some gynoparae at 23.5°.All the larvae engendered by crowded apterae at 17.5° that developed into alatae became gynoparae even if their entire post-natal development occurred at 28.5° (at which temperature no gynoparae were engendered). However, only few of the presumptively alatiform progeny of crowded apterae developed into alatae (and hence few gynoparae were produced) if the larvae were transferred to 28.5° within the first two instars.The ecological significance of certain aspects of the production of various morphs in relation to temperature is discussed.

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Zusammenfassung Blattscheiben von Ackerbohnen, Vicia faba, wurden verwendet zur laufenden Zucht der Schwarzen Bohnenlaus, Aphis fabae, bei Kurztag (10/14) bei verschiedenen, konstanten Temperaturen. Die Nachkommen von apteren Virginoparen, die vorübergehend (6 h) eng gedrängt in Röhrchen verbracht waren (crowded), bestanden überwiegend aus Geflügelten bei 11,5° und 15,5°, aus Geflügelten und Ungeflügelten bei 17,5° bis 25,5° und nur aus Ungeflügelten bei 28,5°. Alle Ungeflügelten waren virginopar. Bei 11,5°–19,5° waren alle Geflügelten gynopar (d.h. erzeugten mindestens eine Ovipare). Von 22,5°–25,5° sank der Anteil der Gynoparen unter den Geflügelten von 96% auf 8%. Bei 11,5° erzeugten die Gynoparen ausschliesslich Ovipare. Bei 15,5°–23,5° gebaren einige Gynopare sowohl Virginopare wie Gynopare, nachdem sie einige Ovipare abgelegt hatten. Bei 22,5° wurden auch einige Männchen von einigen Gynoparen erzeugt. Gynopare erzeugten demnach geflügelte und ungeflügelte Virginopare, Männchen, Gynopare und Ovipare unter Bedingungen, welche die Oviparenproduktion begünstigten. Geflügelte Virginopare erzeugten bei 23,5° auch einige Gynopare.Alle Larven, die von Ungeflügelten nach Gedrängebehandlung bei 17,5° erzeugt wurden, entwickelten sich, soweit sie geflügelt wurden, zu Gynoparen, auch wenn ihre ganze postnatale Entwicklung bei 28,5° ablief (bei welcher Temperatur keine Gynopare erzeugt werden). Dagegen entwickelten sich nur wenige der präsumptiv geflügelten Nachkommen von Ungeflügelten mit Gedrängebehandlung zu Geflügelten (und dementsprechend wurden nur wenige Gynopare erzeugt), wenn die Larven innerhalb der ersten zwei Stadien in 28,5° überführt wurden.Die ökologische Bedeutung der Erzeugung der verschiedenen Morphen in Beziehung zur Temperatur wird diskutiert.

     

The influence of changing temperature on the life history of Daphniopsis ephemeralis

We present evidence which suggests that for Daphniopsis ephemeralischanges in water temperature may directly cue changes in sexratio, ephippial and parthenogenetic egg production and indirectlydetermine female body size. Field data suggested that over anannual cycle, a population of D. ephemeralis comprised animalswith three distinct life history phases. The first was madeup of exephippial females which hatched in the fall. They produceda second group made up of large parthenogenetic females whichcould produce more than one overwintering generation. In thespring these parthenogenetic females gave rise to a third lifehistory phase which comprised males and small ephippial females.Field enclosure experiments suggested that the small size ofspring females was not related to predation. Laboratory experimentssuggested that ephippial egg production at small body sizeswas associated with ‘increasing’ temperature. Theseexperiments also suggested that the fall reproductive pattern(parthenogenetic eggs and large body sizes) was associated with‘decreasing’ temperatures. We conclude that directionalityof seasonal temperature change may be the prime factor responsiblefor D. ephemeralis life history changes observed in the field.