The change in phototactic behaviour of a Daphnia magna clone in the presence of fish kairomones: the effect of exposure time

Using a clone that responds to the presence of fishkairomones by a pronounced change in phototacticbehaviour, we determined how fast a change to morenegatively phototactic behaviour occurs in Daphnia magnaadults that are exposed to a highconcentration of fish kairomones. Kairomone exposedanimals showed an approximately linear decrease in thevalue of the phototactic index with time. Though theresponse was almost immediate, it took two hoursbefore the difference between fish-induced and controlanimals was significant. Extrapolation of the observedresponse indicates that a maximal change inphototactic behaviour, equivalent to animals that havebeen cultured in the presence of fish kairomones sincebirth, occurs after about 13 hours exposure. Weconclude that the predator-induced change in dielvertical migration of zooplankton is fast, and isfully developed in less than a day. The response timeto fish kairomones of Daphnia is shorter forphototactic behaviour than for life history traits,which may have important consequences with respect tothe evolution of trait-dependence in induced defenceresponses.     

浮游动物昼夜垂直迁移机理的主要假说及其研究进展

对有关浮游动物昼夜垂直迁移(DVM)机理的实验、假说以及理论模型方面的研究进.展进行了综述。昼夜垂直迁移通常指常规迁移(傍晚上升,拂晓下降),其行为过程不仅影响浮游动物的垂直分布,而且也间接地影响其水平分布及生活史特征,对浮游动物在一定水域的种群维持和补充具有重要的意义。与垂直迁移机理有关的假说主要有光驱动假说、逃避捕食者假说、能量和资源利用假说等,其中逃避捕食者假说已得到大量的实验证实。其理论模型研究一般在两个时间尺度上进行,一个是短期的行为机制研究,另一个从长期的生活史策略的角度考虑。随着实验技术的进步和理论及建模工具的发展,这两个时间尺度的研究正逐渐统一到一个框架下进行。     

Vertical, lateral and longitudinal movement of zooplankton in a large river

1. The spatial distribution and movement patterns of zooplankton in large rivers are little known compared with those in lake environments. We conducted a series of studies in the Ohio River (U.S.A.) during the low flow period to assess diel vertical (DVM), longitudinal and lateral movement of crustacean zooplankton. 2. The dominant large zooplankter, the copepod Eurytemora affinis, showed a consistent vertical migration pattern of daytime ascent and night‐time descent during all sampling periods – the reverse of the most common migratory pattern of zooplankton in lakes. The cladoceran Bosmina migrated in a similar way in two of the three sampling periods. Surveys taken longitudinally in the river showed similar trends for both taxa. 3. During the lateral surveys, E. affinis was significantly more abundant in the shallow littoral zone during the night than in the daytime. The combination of vertical and lateral movement patterns along with the diel distribution of zooplanktivorous fish suggest that these movements are a predator‐avoidance mechanism. 4. Sampling programmes in large rivers should consider that larger zooplankton such as E. affinis may not be randomly distributed in the river channel and behaviours such as diel vertical migration may be just as evident in river habitats as in lakes.     

Growth and survival of Daphnia in epilimnetic and metalimnetic water from oligotrophic lakes: the effects of food and temperature

SUMMARY 1. In oligotrophic lakes, phytoplankton and bacteria growing in the deep chlorophyll maximum in the cool metalimnion of lakes often dominate biomass and production, but the importance of this source of food for zooplankton is unknown.
2. During much of the day, Daphnia rosea in two mountain lakes inhabited deep chlorophyll layers where food availability was at least equal to that in the epilimnion.
3. To determine the importance of the two strata (epilimnion and metalimnion) for Daphnia , we used a cross-classified factorial experiment to measure how epilimnetic and metalimnetic food and temperature (10 and 16 °C) influenced survival, growth and reproduction.
4. Daphnia survived and grew better when fed seston from the epilimnion of one lake, although chlorophyll, particulate nitrogen and particulate carbon were 2–2.5 times greater in the metalimnion.
5. Temperature had no significant influence on Daphnia survival or growth. Similar results were obtained with food from the second lake, with Daphnia surviving and reproducing better when provided with epilimnetic, rather than metalimnetic food, although the quantities of chlorophyll and carbon in the two strata were similar.
6. Food quality, rather than quantity or temperature, appeared to be the most important determinant influencing survival, growth and reproduction, and the greater food quantity in the metalimnia was not used effectively by the Daphnia .     

On the combined analysis of proximate and ultimate aspects in diel vertical migration (DVM) research

Although evolutionary ecologists agree that proximate and ultimate aspects are two sides of one coin, they are seldom interested in studies on physiological and behavioural mechanisms at the base of ecological phenomena. Nevertheless, these mechanisms are objects of selection and evolved to realise adaptive significances. This paper is a plea to bring both fields closer together, and, by means of an example of Diel Vertical Migration of Daphnia, some proximate and ultimate aspects are discussed. It is argued that light changes, not fish kairomone, is the primary cause for an individual to swim downwards at dawn and upwards at dusk. However, what is called a causal factor might differ when ecosystems or individuals are studied. In addition, causality in ecology is not simple, and has the character of a `set of necessary conditions'. To illustrate the importance of proximate analyses in DVM, two basic response mechanisms are discussed: Photobehaviour system 1 and 2. The physiological character of these systems leads to a fixed type of migration or to a phenotypically induced DVM, respectively. The adaptive significance of the first might be a reduction of the hazardous effects of UV radiation and of the second a lowering of mortality due to visually hunting predators.     

The photobehaviour of Daphnia spp. as a model to explain diel vertical migration in zooplankton

Many pelagic animal species in the marine environment and in lakes migrate to deeper water layers before sunrise and return around sunset. The amplitude of these diel vertical migrations (DVM) varies from several hundreds of metres in the oceans to approx. 5–20 m in lakes. DVM can be studied from a proximate and an ultimate point of view. A proximate analysis is intended to reveal the underlying behavioural mechanism and the factors that cause the daily displacements. The ultimate analysis deals with the adaptive significance of DVM and the driving forces that were responsible for the selection of the traits essential to the behavioural mechanism. The freshwater cladoceran Daphnia is the best studied species and results can be used to model migration behaviour in general. Phototaxis in Daphnia spp., which is defined as a light-oriented swimming towards (positive phototaxis) or away (negative phototaxis) from a light source, is considered the most important mechanism basic to DVM. A distinction has been made between primary phototaxis which occurs when light intensity is constant, and secondary phototaxis which is caused by changes in light intensity. Both types of reaction are superimposed on normal swimming. This swimming of Daphnia spp. consists of alternating upwards and downwards displacements over small distances. An internal oscillator seems to be at the base of these alternations. Primary phototaxis is the result of a dominance of either the upwards or the downwards oscillator phase, and the direction depends on internal and external factors: for example, fish-mediated chemicals or kairomones induce a downwards drift. Adverse environmental factors may produce a persistent primary phototaxis. Rare clones of D. magna have been found that show also persistent positive or negative primary phototaxis and interbreeding of the two types produces intermediate progeny: thus a genetic component seems to be involved. Also secondary phototaxis is superimposed on normal swimming: a continuous increase in light intensity amplifies the downwards oscillator phase and decreases the upwards phase. A threshold must be succeeded which depends on the rate and the duration of the relative change in light intensity. The relation between both is given by the stimulus strength versus stimulus duration curve. An absolute threshold or rheobase exists, defined as the minimum rate of change causing a response if continued for an infinitely long time. DVM in a lake takes place during a period of 1-5-2 h when light changes are higher than the rheobase threshold. Accelerations in the rate of relative increase in light intensity strongly enhance downwards swimming in Daphnia spp. and this enhancement increases with increasing fish kairomone and food concentration. This phenomenon may represent a ‘decision-making mechanism’ to realize the adaptive goal of DVM: at high fish predator densities, thus high kairomone concentrations, and sufficiently high food concentrations, DVM is profitable but not so at low concentrations. Body axis orientation in Daphnia spp. is controlled with regard to light-dark boundaries or contrasts. Under water, contrasts are present at the boundaries of the illuminated circular window which results from the maximum angle of refraction at 48–9° with the normal (Snell's window). Contrasts are fixed by the compound eye and appropriate turning of the body axis orients the daphnid in an upwards or an obliquely downwards direction. A predisposition for a positively or negatively phototactic orientation seems to be the result of a disturbed balance of the two oscillators governing normal swimming. Some investigators have tried to study DVM at a laboratory scale during a 24 h cycle. To imitate nature, properties of a natural water column, such as a large temperature gradient, were compressed into a few cm. With appropriate light intensity changes, vertical distributions looking like DVM were obtained. The results can be explained by phototactic reactions and the artificial nature of the compressed environmental factors but do not compare with DVM in the field. A mechanistic model of DVM based on phototaxis is presented. Both, primary and secondary phototaxis is considered an extension of normal swimming. Using the light intensity changes of dawn and the differential enhancement of kairomones and food concentrations, amplitudes of DVM could be simulated comparable to those in a lake. The most important adaptive significance of DVM is avoidance of visual predators such as juvenile fish. However, in the absence of fish kairomones, small-scale DVMs are often present, which were probably evolved for UV-protection, and are realized by not enhanced phototaxis. In addition, the ‘decision-making mechanism’ was probably evolved as based on the enhanced phototactic reaction to accelerations in the rate of relative changes in light intensity and the presence of fish kairomones.     

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.     

Differential life history responses of several pelagic Daphnia clones differing in migratory behaviour

Females of the hybrid Daphnia galeata × hyalina were isolated from a natural population in Lake Maarsseveen and from these individuals clones were cultured in the laboratory. Some clones were assumed to be migrating and some non-migrating. Life history experiments were performed with these clones in the presence and absence of fish kairomones. Results show that clones differed in life history strategy in concert with their presumed migration strategies which suggests a link between life history and behaviour. However, no sharp border exists between migrating and non-migrating clones since a gradual response pattern was found for the traits investigated. In the absence of fish kairomones, the relation between length at maturity and number of eggs was found to differ between the clones of the non-migrating and the migrating group. The latter had a lower number of eggs at similar length values. In the presence of fish kairomones, the length–clutch size relation was the same. However, non-migrating clones were smaller at the age at maturity and had fewer eggs. Although clones of both groups were thus found to differ significantly, overlap existed. Age at maturity was found to be the same.     

Neutral markers, ecologically relevant traits, and the structure of genetic variation in Daphnia

Zooplankton, Daphnia in particular, are increasingly used as model organisms to investigate general evolutionary biological questions. I here discuss some recent insights into the patterns and processes determining genetic diversity within and genetic differentiation among natural populations of cyclically parthenogenetic Daphnia. I focus on three aspects: (1) the interplay of phenotypic plasticity and genetic polymorphism in explaining variability in ecologically relevant traits, (2) the patterns of genetic variation revealed by neutral markers and ecologically relevant traits, and (3) the evolutionary ecological importance of hybridization events in Daphnia. The need for studies on the evolutionary ecology of sexual reproduction and dispersal via ephippial eggs in Daphnia is stressed.     

The genetics of phototaxis in Daphnia magna: Existence of three phenotypes for vertical migration among parthenogenetic females

Using a cloning technique, we revealed the existence of three phototactically distinct types in Daphnia magna, viz. negatives, positives, and gipsies. The latter migrate continuously between a low and a high light intensity. The expression of this behaviour is genetically determined, although positives and negatives can reversibly switch into gipsies.It is proposed that two opposite genotypes exist, with the gipsy behaviour epigenetically induced. All juveniles behave more or less uniformly, irrespective of their origin. The phototactic responses develop rather late during ontogenesis.     

Acoustic observation of diel vertical migration and shoaling behaviour in Atlantic redfishes

Acoustic methods were used to study Atlantic redfishes Sebastes spp. vertical migration and shoaling behaviour in Newfoundland waters. Redfishes exhibited consistent patterns of vertical migration in winter, spring and summer, but pelagic shoals were not observed in winter. Pelagic daytime aggregations were generally in close proximity to dense patches of redfishes along the sea floor. Pelagic shoals exhibited high degrees of variability in size, shape and density. Attempts to explain variations in shoal density and area with features of shoal position and structure were unsuccessful. Nearest neighbour distance between fish in shoals had a lower limit near one body length. During the night, fishes were dispersed in the water column and distributions were more homogenous. Diel vertical migration appeared to be a foraging strategy, in which redfishes followed the migration of their euphausiid prey.     

Diverse Responses of Planktonic Crustaceans to Fish Predation by Shifts in Depth Selection and Size at Maturity

We investigated the behaviour and life histories of large zooplankton in the Esch-sur-Sûre reservoir (Luxembourg). We found that the decrease in size at maturity, as well as diurnal refuge in deep waters, were the adaptive responses (concurrently or alternatively) adopted by large zooplankters to cope with the increasing predation risk throughout the summer. Daphnia galeata initiated a more severe trade-off to cope with high summer predation relative to other cladoceran species. Diaphanosoma brachyurum and Daphnia cucullata seem less susceptible to fish predation as indicated by the low alteration of their size structure and their vertical distribution. The copepod Eudiaptomus gracilis took refuge in deep waters and achieved important modifications of its mature size.     

Effects of aquatic insect predators on zooplankton in fishless ponds

We removed the surface-orienting aquatic insects from a fishless pond to determine their predation effects on zooplankton behavior and size structure. A second fishless pond served as the unmanipulated reference system in this two year study. In the reference pond and the treatment pond prior to manipulation, daphnids exhibited pronounced diel vertical migrations. Following the removal of surface-orienting aquatic insects from the treatment pond, daphnid migration changed to a reverse migration strategy that was significantly different from that observed in the reference system. Average daphnid body size increased significantly following predator removal in the treatment system. Our data indicate that predation by aquatic insect predators, such as notonectids and dytiscids, may affect daphnid migration behavior in fishless systems. Vertical migration by daphnids may allow coexistence with surface-orienting insects in ponds that are deep enough to provide a spatial refuge from these predators.     

Life history characteristics of Daphnia magna clones differing in phototactic behaviour

In an analysis of a life table experiment involving positively, intermediately and negatively phototactic Daphnia magna clones, life history traits such as the average duration of the adult instar, neonate and adult body size were found to be correlated with phototactic behaviour. The size of the eggs and neonates was positively correlated with adult body size, and with egg development time. Adult body size was positively correlated with the size of the second and subsequent clutches. I argue that the intrinsic positive correlation between offspring size and egg development time is a key factor structuring the differences in life history patterns observed between the positively and intermediately phototactic Daphnia genotypes, and that the two life history patterns are to be considered alternatives suited for different environmental conditions (e.g. habitats with and without strong predation pressure on adults).     

Two hundred years of zooplankton vertical migration research

Vertical migration is a geographically and taxonomically widespread behaviour among zooplankton that spans across diel and seasonal timescales. The shorter-term diel vertical migration (DVM) has a periodicity of up to 1 day and was first described by the French naturalist Georges Cuvier in 1817. In 1888, the German marine biologist Carl Chun described the longer-term seasonal vertical migration (SVM), which has a periodicity of ca. 1 year. The proximate control and adaptive significance of DVM have been extensively studied and are well understood. DVM is generally a behaviour controlled by ambient irradiance, which allows herbivorous zooplankton to feed in food-rich shallower waters during the night when light-dependent (visual) predation risk is minimal and take refuge in deeper, darker waters during daytime. However, DVMs of herbivorous zooplankton are followed by their predators, producing complex predator–prey patterns that may be traced across multiple trophic levels. In contrast to DVM, SVM research is relatively young and its causes and consequences are less well understood. During periods of seasonal environmental deterioration, SVM allows zooplankton to evacuate shallower waters seasonally and take refuge in deeper waters often in a state of dormancy. Both DVM and SVM play a significant role in the vertical transport of organic carbon to deeper waters (biological carbon sequestration), and hence in the buffering of global climate change. Although many animal migrations are expected to change under future climate scenarios, little is known about the potential implications of global climate change on zooplankton vertical migrations and its impact on the biological carbon sequestration process. Further, the combined influence of DVM and SVM in determining zooplankton fitness and maintenance of their horizontal (geographic) distributions is not well understood. The contrasting spatial (deep versus shallow) and temporal (diel versus seasonal) scales over which these two migrations occur lead to challenges in studying them at higher spatial, temporal and biological resolution and coverage. Extending the largely population-based vertical migration knowledge base to individual-based studies will be an important way forward. While tracking individual zooplankton in their natural habitats remains a major challenge, conducting trophic-scale, high-resolution, year-round studies that utilise emerging field sampling and observation techniques, molecular genetic tools and computational hardware and software will be the best solution to improve our understanding of zooplankton vertical migrations.     

An analysis of the phototactic behaviour of Daphnia magna clones and their sexual descendants

Daphnia magna clones, isolated from different natural populations, were inbred and crossbred. Some aspects of the heredity of the phototactic behaviour, quantified by an index, were analysed. Heritability in the broad sense was determined for several assemblages of clones through calculation of the clonal repeatability. Heritability sensu strictu was determined by offspring-parent regressions. Frequency distributions of a phototactic index of several inbred and crossbred families are given.The results indicate a significant contribution of additive genetic variance to the total phenotypic variance. Comparison of heritability estimates suggests an important genetic interaction component.Some implications of these results on the variability of vertical migration patterns in natural populations are discussed.     

Light intensity controls anti-predator defences in Daphnia: the suppression of life-history changes

A huge variety of organisms respond to the presence of predators with inducible defences, each of which is associated with costs. Many genotypes have the potential to respond with more than one defence, and it has been argued that it would be maladaptive to exhibit all possible responses at the same time. Here, we test how a well-known anti-fish defence in Daphnia, life-history changes (LHC), is controlled by light. We show that the kairomone-mediated reduction in size at first reproduction is inversely coupled to the light intensity. A similar effect was found for the kairomone-mediated expression of candidate genes in Daphnia. We argue that the light intensity an individual is exposed to determines the degree of LHC, which allows for plastic adjustment to fluctuating environments and simultaneously minimizes the associated costs of multiple alternately deployable defences. It is hypothesized that this allows for a coupling of multiple defences, i.e. LHC and diel vertical migration.     

Vertical distribution and diel migration of flagellated phytoplankton in a small humic lake

The vertical distributions and migrations are described of the most abundant flagellated phytoplankton species from the summer community of a small forest lake in southern Finland. The lake showed a steep and stable thermal stratification with a shallow oxygenated epilimnion. Horizontal variation of phytoplankton distribution within the lake was tested on two scales and found to be statistically significant only in the case of Mallomonas reginae. The vertical distribution of flagellated phytoplankton was assessed by reference to the distribution of a non-motile, neutrally buoyant species Ankyra judayi. Statistically significant, active vertical positioning was demonstrated for all the flagellates examined with the exception of Spiniferomonas bourrellyi. Diel vertical migrations were apparent for all species showing active positioning and the pattern of an evening descent and a morning ascent was ubiquitous. The extent and timing of diel migrations varied between species. The most extensive migrations were by Cryptomonas marssonii which crossed a temperature gradient of 14 °C and penetrated far into the anoxic hypolimnion. Several categories of competitive advantage can be gained by species undertaking such diel vertical migrations.     

Distribution and onshore migration behaviour of burbot larvae in Lake Constance, Germany

Larval abundance of burbot Lota lota in the pelagic zone of Lake Constance, Germany, peaked during April and remained at a constant but lower level until mid‐June. From the end of May onwards a significant diel vertical migration pattern was observed: while burbot larvae were distributed above as well as below the thermocline in the daytime with the highest percentages of abundance at water depths of 30 and 50 m (below the thermocline) on 5 and 25 June, they were concentrated from 2 to 15 m (above the thermocline) during the night. This migration pattern coincided with a significant decline in the food items preferred by burbot at this life stage, cyclopoid copepods. This phase of diel vertical migration lasted for c . 4 weeks until the burbot larvae suddenly disappeared from the pelagic zone. This indicated a short phase, lasting only a few days, of larval settlement into profundal benthic habitats. This was supported by a significant, abrupt decrease in the absolute growth rates of the larvae at day 56 after hatching. The day–night pattern of vertical migration observed could be assumed to be a transition phase from a pelagic to a benthic lifestyle, as reported for juveniles of several other, marine gadoid species.