Viewing DVM via general behaviors of zooplankton: a way bridging the success of individual and population

In this paper, we viewed the diel vertical migration (DVM) of copepod in the context of the animal's immediate behaviors of everyday concerns and constructed an instantaneous behavioral criterion effective for DVM and non-DVM behaviors. This criterion employed the function of 'venturous revenue' (VR), which is the product of the food intake and probability of the survival, to evaluate the gains and losses of the behaviors that the copepod could trade-off. The optimal behaviors are to find the optimal habitats to maximize VR. Two types of VRs are formulated and tested by the theoretical analysis and simulations. The sensed VR, monitoring the real-time changes of trade-offs and thereby determining the optimum habitat, is validated to be the effective objective function for the optimization of the behavior; whereas, the realized VR, quantifying the actual profit obtained by an optimal copepod in the sensed-VR-determined habitat, defines the life history of a specific age cohort. The achievement of a robust copepod overwintering stock through integrating the dynamics of the constituent age cohorts subjected to the instantaneous behavioral criterion for DVM clearly exemplified a possible way bridging the immediate pursuit of an individual and the end success of the population.     

Modeling patterns of zooplankton diel vertical migration

Realized predation pressure, defined as the product of predationpressure and light intensity, expresses the mortality pressuredue to visual predation. The part of realized predation pressurewhich is sensed by organisms is here considered to be relatedto food level and temperature. This partly realized predationpressure is referred to as sensed predation pressure. We proposea possible control mechanism of diel vertical migration (DVM):organisms move vertically following the minimum change in sensedpredation pressure. To investigate this assumption, we presenta math ematical model of DVM. We assume that when predatorsare present, the food level is above a minimal level, and temperatureis higher than the tolerance of organisms to growth, prey organismsundertake DVM following the minimum change in sensed predationpressure. We examine how patterns of migration may be affectedby changes in water clarity, predation pressure, food leveland temperature. This work supports the assumption that minimizingchanges in sensed predation pressure can explain the wide variationin the vertical profile of zooplankton.     

Impact of food concentration on diel vertical migration behaviour of <Emphasis Type="Italic">Daphnia pulex</Emphasis> under fish predation risk

Vertical migration of Daphnia represents the best-studied predator-avoidance behaviour known; yet the mechanisms underlying the choice to migrate require further investigation to understand the role of environmental context. To investigate the optimal habitat choice of Daphnia under fish predation pressure, first, we selected the individuals exhibiting strong migration behaviour. The animals collected from the hypolimnion during the daytime were significantly larger, being more conspicuous, and in turn performed stronger diel vertical migration (DVM) when exposed to fish cue. We called them strong migrants. Second, we provided the strong migrant D. pulex with food at high and intermediate (1 and 0.4 mg C l⁻¹, respectively) levels, which were well above the incipient limiting level and of high quality. They traded the benefits of staying in the warm water layer and moved down to the cold water in response to fish cue indicating fish predation. The availability of food allowed the animals to stay in the cold hypolimnion. However, at the low food level (0.1 mg C l⁻¹), which is an additional constraint on fitness, Daphnia moved away from the cold hypolimnion. Poor food condition resulted in strong migrant Daphnia to cease migration and remain in the upper warmer water layer. Although temperature is known to be a more important cost factor of DVM than food, our results clearly show that this is only true as long as food is available. It becomes clear that food availability is controlling the direction of vertical positioning when daphnids experience a dilemma between optimising temperature and food condition while being exposed to fish cue. Then they overlook the predation risk. Thus, the optimal habitat choice of Daphnia appears to be a function of several variables including temperature, food levels and fish predation. Handling editor: S. I. Dodson     

Sampling and analysis of gut contents in relation to environmental variability and diel vertical migration by herbivorous zooplankton

The accuracy of standard sampling and analysis procedures forestimating ingestion by herbivorous zooplankton was assessedusing models. Artificial environments were created in a computermodel, allowing for depth-dependent variability in temperature,chlorophyll and primary production. Model zooplankton were simulatedwithin these artificial environments using individual-basedmodels. The model zooplankton feed and defaecate at rates determinedby temperature and food concentrations, and also exhibit dielvertical migration (DVM) according to a variety of migrationmodels. The computer model was run for different combinationsof these nine environmental and five DVM models. Data were ‘sampled’from the model output, similar to field sampling of mesozooplanktongrazing. Daily ingestion was calculated from the gut ‘samples’using standard procedures for analysing gut fluorescence. Thesample results were compared with the actual ingestion valuesin the model, and some causes of discrepancies were noted. (i)If incorrect temperatures were assumed when calculating thegut evacuation rate (K), then estimates of ingestion were wrongby up to 40%. (ii) Non-uniform food environments gave errorsof up to 30% because of the large variability of measured gutcontents among individuals. (iii) Sampling from only part ofthe total depth range (e.g. at the chlorophyll maximum) resultedin estimates of ingestion being only 5% of the real value. Thissampling practice should be discouraged, because the sampleis not random. (iv) If sampling is not frequent enough, errorscan be as large as 45%, but more usually were 10% for realisticsampling frequencies. We describe an analysis procedure thatuses Monte Carlo-type simulations in a computer spreadsheetto estimate population consumption. These calculations takeinto account natural variability due to populations, samplesand assumptions. We urge that results should be presented asranges of possible values, rather than as single ‘mean’values, to allow for easier recognition of meaningful differencesamong samples and systems.     

Diel vertical migration arising in a habitat selection game

Predator and prey react to each other, adjusting their behavior to maximize their fitness and optimizing their food intake while keeping their predation risk as low as possible. In a pelagic environment, prey reduce their predation mortality by adopting a diel vertical migration (DVM) strategy, avoiding their predator during their peak performance by finding refuge in deep layers during daylight hours and feeding at the surface during the night. Due to the duality of the interaction between prey and predator, we used a game theory approach to investigate whether DVM can be a suitable strategy for the predator as well as the prey. We formulated three scenarios in plankton ecology in order to address this question. A novel finding is that mixed strategies emerge as optimal over a range of the parameter space, where part of the predator or prey population adopts a DVM while the rest adopt one or other “sit and wait” strategies.     

Small-scale spatial distribution of the euphausiid Euphausia pacifica and overlap with planktivorous fishes

The spatial distribution of zooplankton and planktivorous fishin Saanich Inlet, British Columbia was characterized with a445 kHz multibeam sonar capable of localizing individual animalsin three dimensions. Numerical simulation of data processingprocedures indicates that this instrument has sufficient resolutionto characterize zooplankton spatial distributions using Lloyd’sindex of patchiness and nearest neighbour distance (NND) measures.Zooplankters at this site were dominated by the euphausiid Euphausiapacifica which underwent diel vertical migration (DVM). Fish(mainly herring and walleye pollock) were only abundant at thisdeep-water station at night. Analysis of 4 m³ volumes over scalesof     

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.     

Trade-offs inDaphnia vertical migration strategies

Summary Planktonic animals performing diel vertical migration (DVM) experience a tradeoff between reduced mortality and reduced reproductive output due to lower food availability in their refuge. Models of DVM as an evolutionarily stable strategy predict that, under certain conditions, strategies of both migration and non-migration can coexist. Vertical profiles of animal abundances during day and night, however, do not allow any discrimination between the behaviour of individuals or subpopulations. We used length-body protein regressions as a measure of the nutritional state ofDaphnia to distinguish possible sub-populations differing in their migration strategy. An overwhelming part of the population migrated downwards during the day. However, the few daphnids in the epilimnion during the day had significantly higher protein content than the animals in the deep water, indicating that these daphnids did not migrate randomly but remained in the surface food-rich water all day. This shows that migrating animals gain no metabolic advantage over non-migrating ones.Supported by a F.P.U. grant (Spanish Goverment)     

Diel vertical migration of zooplankton: optimum migrating schedule based on energy accumulation

Zooplankton perform diel vertical migration (DVM) to avoid predators at the upper water layer, but often stay in the upper water layer throughout the day seeking food in spite of the presence of predators. This difference in migrating behavior has been explained by differences in environmental conditions or genetic differences. We examined theoretically how nutritious conditions of zooplankton individuals relate to determining different migrating behavior. A simple optimization model, maximizing the population growth rate, demonstrates that zooplankton individuals change their migrating behavior depending on the amount of accumulated energy. Such energy accumulation and its investment in reproduction are repeated every reproductive cycle. Therefore, unless the reproductive cycle is synchronized among individuals, different migrating behaviors will be observed within a population even if no genetic differences exist. Our model demonstrates that such coexistence of the two migrating behaviors is possible in natural Daphnia populations, and suggests that internal conditions of zooplankton individuals may be important as a factor for determining migrating behavior of zooplankton. This revised version was published online in July 2006 with corrections to the Cover Date.     

Daphnia magna trade‐off safety from UV radiation for food

Research on diel vertical migration (DVM) is generally conducted at the population level, whereas few studies have focused on how individual animals behaviorally respond to threats when also having access to foraging opportunities. We utilized a 3D tracking platform to record the swimming behavior of Daphnia magna exposed to ultraviolet radiation (UVR) in the presence or absence of a food patch. We analyzed the vertical position of individuals before and during UVR exposure and found that the presence of food reduced the average swimming depth during both sections of the trial. Since UVR is a strong driver of zooplankton behavior, our results highlight that biotic factors, such as food patches, have profound effects on both the amplitude and the frequency of avoidance behavior. In a broader context, the trade‐off between threats and food adds to our understanding of the strength and variance of behavioral responses to threats, including DVM.     

Control mechanisms of diel vertical migration: theoretical assumptions

We explore control mechanisms underlying the vertical migration of zooplankton in the water column under the predator-avoidance hypothesis. Two groups of assumptions in which the organisms are assumed to migrate vertically in order to minimize realized or effective predation pressure (type-I) and to minimize changes in realized or effective predation pressure (type-II), respectively, are investigated. Realized predation pressure is defined as the product of light intensity and relative predation abundance and the part of realized predation pressure that really affects organisms is termed as effective predation pressure. Although both types of assumptions can lead to the migration of zooplankton to avoid the mortality from predators, only the mechanisms based on type-II assumptions permit zooplankton to undergo a normal diel vertical migration (morning descent and evening ascent). The assumption of minimizing changes in realized predation pressure is based on consideration of DVM induction only by light intensity and predators. The assumption of minimizing changes in effective predation pressure takes into account, apart from light and predators also the effects of food and temperature. The latter assumption results in the same expression of migration velocity as the former one when both food and temperature are constant over water depth. A significant characteristic of the two type-II assumptions is that the relative change in light intensity plays a primary role in determining the migration velocity. The photoresponse is modified by other environmental variables: predation pressure, food and temperature. Both light and predation pressure are necessary for organisms to undertake DVM. We analyse the effect of each single variable. The modification of the phototaxis of migratory organisms depends on the vertical distribution of these variables.     

Temperature selection in Brook Charr: lab experiments,field studies,and matching the Fry curve

Zooplankton diel vertical migration (DVM) is an ecologically important process, affecting nutrient transport and trophic interactions. Available measurements of zooplankton displacement velocity during the DVM in the field are rare; therefore, it is not known which factors are key in driving this velocity. We measured the velocity of the migrating layer at sunset (upward bulk velocity) and sunrise (downwards velocity) in summer 2015 and 2016 in a lake using the backscatter strength (VBS) from an acoustic Doppler current profiler. We collected time series of temperature, relative change in light intensity chlorophyll-a concentration and zooplankton concentration. Our data show that upward velocities increased during the summer and were not enhanced by food, light intensity or by VBS, which is a proxy for zooplankton concentration and size. Upward velocities were strongly correlated with the water temperature in the migrating layer, suggesting that temperature could be a key factor controlling swimming activity. Downward velocities were constant, likely because Daphnia passively sink at sunrise, as suggested by our model of Daphnia sinking rate. Zooplankton migrations mediate trophic interactions and web food structure in pelagic ecosystems. An understanding of the potential environmental determinants of this behaviour is therefore essential to our knowledge of ecosystem functioning.

     

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.     

Diet changes in the carbon and nitrogen content of the copepod Metridia lucens

Diel changes in the near-surface (0–50 m) abundance, prosomelength, and carbon and nitrogen content of the copepod Metridialucens were measured in Deep Cove, Doubtful Sound, New Zealand(45°27'S, 167°9'E) between 3 and 6 September 1996. Metridialucens showed maximal abundance a night, suggesting a patternof normal diel vertical migration (DVM). The change in abundancesuggested that the descent of the population occurred –1h prior to dawn and the ascent –1 h after dusk. However,a proportion of the population remained near the surface duringthe day. Although there was no diel pattern in the prosome lengthof M.lucens collected near the surface, there was a marked dielcycle in the measured carbon and nitrogen contents, with maximalvalues being measured towards the end of the night prior tothe downward migration. We suggest that this diet cycle in themeasured elemental content was caused by DVM occurring morestrongly in those animals which had a better body condition,i.e. a higher elemental content per unit length.     

Coexistence of two similar copepod species, <Emphasis Type="Italic">Eudiaptomus gracilis</Emphasis> and <Emphasis Type="Italic">E. graciloides</Emphasis>: the role of differential predator avoidance

Habitat choice in relation to environmental factors of two coexisting calanoid copepod species, Eudiaptomus gracilis and E. graciloides, was studied in a mesotrophic lake and in large indoor mesocosms. Both species and sexes showed pronounced diel vertical migration (DVM) in the field. In 12 m deep mesocosms with free ranging fish DVM was observed and species increased day depth over time. No changes were observed in copepod day depth over time in experiments with fish kairomone. It is hypothesized that fish kairomone acts as an early warning system to copepods which respond by moving deeper, but only as far as the thermocline. For full DVM, a nearby mechanical stimulus is necessary. Thus, as fish go deeper to feed, copepods retreat. The response of copepods to fish predation, in the presence of low and high numbers of Daphnia,shows that copepods effectively use Daphniaas living shields to avoid predation. The two species adopt different vertical migration strategies depending on whether there are high or low numbers of Daphniapresent. A dominant feature of mesocosm experiments was the night time aggregating (lekking) of E. gracilis males at the surface. When the spring and autumn percentages of risk takers in the epilimnion were compared, E. gracilis, particularly males, suffered the greatest cost.     

Morphological analyses allow to separate <Emphasis Type="Italic">Branchipus</Emphasis> species (Branchiopoda,Anostraca) from different geographic regions

Daphnia perform diel vertical migration (DVM), a predator-avoidance strategy to migrate towards deeper and colder layers in the water column in the morning and movement to the algae-rich surface layers in the evening. However, individuals performing DVM incur several trade-offs since they might suffer from resource limitation and a slower instantaneous birth rate in deeper depths. DVM patterns may be modified by abiotic factors such as temperature, food concentration, or pH and vary among different Daphnia species and genotypes. Furthermore, Daphnia host a variety of microparasites that might pose an additional factor influencing DVM behaviour. For infected individuals, migration into cooler temperature layers might slow down parasite growth. Moreover, parasites can increase opacity of their hosts. Non-migrating individuals might then be selectively purged from the upper layers by visually hunting predators. With these premises we asked, whether epidemics of the ichthyosporean parasite Caullerya mesnili affect or are affected by the DVM behaviour of Daphnia in Lake Greifensee, Switzerland by analysing the vertical distribution of Daphnia during day and night on two dates. Furthermore, we were interested whether a potential interaction depends on host genotype. We therefore studied the genotypic composition of the integrated population in regular sampling intervals over the course of one year and on a fine-grained vertical resolution during the Caullerya epidemic in late summer. Since Caullerya-infected Daphnia migrated equally well as uninfected ones, the findings of this study suggest that Caullerya epidemics neither affected nor were affected by the DVM behaviour of Daphnia. We observed clonal succession in the lake but could not link this succession to the Caullerya epidemic; all except one of the common multilocus genotypes were under-infected. In addition, outbreak and course of this Caullerya epidemic seemed to rely mainly on environmental cues. Because this first study only provides a snapshot of time, we hope that further studies will be done to verify our results.     

Diel vertical migration and feeding rhythm of Daphnia longispina and Bosmina corexoni in Lake Toya, Hokkaido, Japan

Diel vertical migration (DVM) and diel feeding rhythm of two cladocerans, Daphnia longispina and Bosmina coregoni were investigated at the pelagic area of Lake Toya (Hokkaido, Japan) in May, August and October 1992. Both species performed nocturnal DVM. The amplitude of DVM, however, became smaller from May to October. Such seasonal variations in DVM could not be explained by light penetration and/or water temperature. The two species had a clear feeding rhythm; they fed at night in May and October but also after sunrise in August. These feeding rhythms appeared to be related to the light-dark cycle, but were not necessarily associated with their DVM. We suggest that the diel feeding rhythm and DVM are regulated independently by light cues.     

Behavioural responses of two cladocerans and two copepods exposed to fish kairomones

In natural predator–prey interactions, chemical communication is one of the most advantageous strategies for prey organisms because they can anticipate possible harm by means of phenotypic changes. This study compares the changes in the behaviour of four freshwater zooplankton species in the presence and absence of infochemicals from the same predator. The studied organisms are two copepods and two cladocerans living in highly variable freshwater environments. The analysis is focused on two predator defensive behaviours: a pre-encounter and a post-encounter response. First, we analysed the diel vertical migration (DVM) of the organisms inside 150?cm long transparent plastic tubes. Second, we used a novel hydraulic apparatus to quantify their ability to escape from a potential predator. The results revealed that the species have different behavioural patterns in the absence of infochemical. The differences were mainly in the way DVM developed and reflect their life histories and adaptive strategies relative to their natural environment. When faced with kairomones, the escape ability of the organisms was enhanced in all cases and DVM changed, although not always in agreement with the expected patterns. The interaction between each species and the multiple environmental components is discussed.     

Ontogenetic vertical distribution and diel migration of the copepod Eucalanus inermis in the oxygen minimum zone off northern Chile (20-21{degrees} S)

The vertical and ontogenetic distribution, and diel verticalmigration (DVM), of Eucalanus inermis in relation to the strongvertical gradient in oxygen concentration associated with anintense oxygen minimum zone (OMZ) were studied at a coastalarea off northern Chile (20–21° S). A close relationshipbetween the abundance of the whole copepod population and lowoxygen waters was found, with most developmental stages remainingnear the base of the oxycline (30–80 m) and within theupper zone of the OMZ (30–200 m). All stages performedDVM but not at all the stations, mainly between the 30–60and 60–200 m strata; a small fraction (<20%) appearedin the surface layer (0–30 m) mostly at night. This strategyof movement would result in a better utilization of food resourcessince the strong physical and chemical gradients at the baseof the oxycline and upper OMZ boundary might serve as a siteof particle accumulation. A secondary fluorescence peak was,in fact, found at all the stations, coinciding with minimaldissolved oxygen (DO, <1 mL O₂ L^–1) at the base ofthe oxycline or in the upper OMZ boundary. The relevance ofthe biogeochemical flux involved in this diel migration patternwas assessed by calculating the potential active input of carbonand nitrogen from the upper layers into deeper the OMZ.