Emergence of Holling type III zooplankton functional response: Bringing together field evidence and mathematical modelling

Food-web population models are rather sensitive to parameterization of functional response in predation terms. Theoretical studies predict enhancing of ecosystems’ stability for a functional response of sigmoid type (Holling type III). The choice of a correct type of response is especially important for modelling outcome of grazing control of algal blooms by zooplankton in nutrient-rich ecosystems. Extensive experiments on zooplankton feeding in laboratories show non-sigmoid nature of response for most herbivorous zooplankton species. As a consequence, there is a strong opinion in literature that the implementation of Holling III type grazing in plankton models is biologically meaningless. I argue, however, that such an ‘evident’ claim might be wrong and sigmoid functional responses in real plankton communities would emerge more often than was suggested earlier. Especially, this concerns plankton models without vertical resolution, which ignore heterogeneity in vertical distribution of species. Having conducted extensive literature search of data on zooplankton feeding in situ, I show that vertical heterogeneity in food distribution as well as active food searching behaviour of zooplankton can modify the type of functional response. In particular, the rate of food intake by the whole zooplankton population in the column, as a function of total amount of food, often exhibits a sigmoid behaviour, instead of a non-sigmoid one postulated previously based on laboratory experiments. This conceptual discrepancy is due to the ability of zooplankton to feed mostly in layers with high algal density. I propose a generic model explaining the observed alteration of type between overall and local functional responses. I show that emergence of Holling type III in plankton systems is due to mechanisms different from those well known in the ecological literature (e.g. food search learning, existence of alternative food, refuge for prey).     

Implications of resting eggs of zooplankton for the paradox of enrichment

In this study, we numerically investigated to what extent introducing resting-egg dynamics would stabilize simple Daphnia–algae consumer–resource models. In the models, the density of viable resting eggs was explicitly expressed, and we assumed that zooplankton produced resting eggs seasonally or in response to food deficiency and that resting eggs hatched seasonally. The models predicted that, although the paradox of enrichment was not completely resolved (i.e., the system was destabilized by eutrophication), we found the following conditions under which the stabilizing effects of resting eggs would be significantly large: (1) resting eggs are produced seasonally (rather than in response to food deficiency), (2) the annual average allocation ratio to resting eggs is large, and (3) the annual average hatching rate of resting eggs is low. The results suggest that resting-egg dynamics can significantly reduce the paradox of enrichment within the biologically meaningful parameter space and contribute to the stability of plankton community dynamics.     

Towards a correct description of zooplankton feeding in models: Taking into account food-mediated unsynchronized vertical migration

Complex nature of foraging behaviour of zooplankton makes it difficult to describe adequately zooplankton grazing in models with vertical space. In mean-field models (based on systems of PDEs or coupled ODEs), zooplankton feeding at a given depth is normally computed as the product of the local functional response and the zooplankton density at this depth. Such simplification is often at odds with field observations which show the absence of clear relationship between intake rates of organisms and the ambient food density. The observed discrepancy is generic and is often caused by fast non-synchronous vertical migration of organisms with different nutrition status. In this paper, we suggest a simple way of incorporating unsynchronized short-term vertical migration of zooplankton into the mean-field modelling framework. We compute grazing of zooplankton in each layer depending on feeding activity of organisms in the layer. We take into account grazing impact of animals which are in the active phase of foraging cycle at the given moment of time but neglect the impact of animals which are in the non-active phase of the cycle (e.g. digesting food). Unsynchronized vertical migration determines the vertical distribution of actively feeding animals in layers depending on vertical distribution of food. In this paper, we compare two generic plankton models: (i) a model based on ‘classical’ grazing approach and (ii) a model incorporating food-mediated unsynchronized vertical migration of zooplankton. We show that including unsynchronized food-mediated migration would make the behaviour of a plankton model more realistic. This would imply a significant enhancement of ecosystem's stability and some additional mechanisms of regulation of algal blooms. In the system with food-mediated unsynchronized vertical migration, the control of phytoplankton by herbivorous becomes possible even for very large concentrations of nutrients in the water (formally, when the system's carrying capacity tends to infinity).     

Mathematical modeling of cascading migration in a tri-trophic food-chain system

Diel vertical migration is a behavioral antipredator defense that is shaped by a trade-off between higher predation risk in surface waters and reduced growth in deeper waters. The strength of migration of zooplankton increases with a rise in the abundance of predators and their exudates (kairomone). Recent studies span multiple trophic levels, which lead to the concept of coupled vertical migration. The migrations that occur at one trophic level can affect the vertical migration of the next lower trophic level, and so on, throughout the food chain. This is called cascading migration. In this paper, we introduce cascading migration in a well-known model (Hastings and Powell, Ecology 73:896–903, 1991). We represent the dynamics of the system as proposed by Hastings and Powell as a phytoplankton–zooplankton–fish (prey–middle predator–top predator) model where fish affect the migrations of zooplankton, which in turn affect the migrations of motile phytoplankton. The system under cascading migration enhances system stability and population coexistence. It is also observed that for a higher rate of cascading migration, the system shows chaotic behavior. We conclude that the observations of Hastings and Powell remain true if the cascading migration rate is high enough.     

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.     

Effect of the rate of phytoplankton growth on the spaced-time dynamics of plankton communities in an homogeneous environment

We use a conceptual mathematical reaction-diffusion model to investigate the mechanisms of spatial structure formation and complex temporal dynamics of plankton in a heterogeneous environment. We take into account basic trophic interactions, namely, "prey-predator" interactions between phytoplankton, zooplankton, and fish in upper layers of natural waters. We consider plankton as a passive contaminant in turbulent waters. We show that plankton structure formation can result from the difference in phytoplankton growth rate in neighboring habitats. Phytoplankton and zooplankton biomass is shown to undergo both regular and chaotic oscillations. The fish predation rate substantially affects the spatial and temporal dynamics of plankton in a heterogeneous environment.     

Competition patterns among phytoplankton functional groups: How useful are the complex mathematical models?

Simple models have significant contribution to the development of ecological theory. However, these minimalistic modeling approaches usually focus on a small subset of the causes of a phenomenon and neglect important aspects of system dynamics. In this study, we use a complex aquatic biogeochemical model to examine competition patterns and structural shifts in the phytoplankton community under nutrient enrichment conditions. Our model simulates multiple elemental cycles (org. C, N, P, Si, O), multiple functional phytoplankton (diatoms, green algae and cyanobacteria) and zooplankton (copepods and cladocerans) groups. It also takes into account recent advances in stoichiometric nutrient recycling theory, and the zooplankton grazing term is reformulated to include algal food quality effects on zooplankton assimilation efficiency. The model provided a realistic platform to examine the functional properties (e.g., kinetics, growth strategies, intracellular storage capacity) and the abiotic conditions (temperature, nutrient loading) under which the different phytoplankton groups can dominate or can be competitively excluded in oligo, meso and eutrophic environments. Based on the results of our analysis, the intergroup variability in the minimum cell quota and maximum transport rate at the cell surface for phosphorus along with the group-specific metabolic losses can shape the structure of plankton communities. We also use classification tree analysis to elucidate aspects (e.g., relative differences in the functional group properties, critical values of the abiotic conditions, levels of the other plankton community residents) of the complex interplay among physical, chemical and biological factors that drive epilimnetic plankton dynamics. Finally, our study highlights the importance of improving the mathematical representation of phytoplankton adaptive strategies for resources procurement (e.g., regulation of transport kinetics, effects of transport kinetics on the kinetics of assimilation, relationship between assimilation and growth) to effectively link variability at the organismal level with ecosystem-scale patterns.     

The structure and diurnal variations of the zooplankton of the Prince Edward Islands: Implications for the biomass build-up of higher trophic levels

Summary Short-term variations in the micro-, meso- and macrozooplankton communities at shelf and offshore stations in the vicinity of the Price Edward Islands were examined during April/May 1985 and 1986. Microzooplankton was dominated by copepod nauplii. Other holoplanktonic groups were represented in large numbers, while meroplanktonic larvae of benthic invertebrates were very scarce despite the large benthic population of the island shelf. Copepods dominated in terms of numerical abundance the meso- and macrozooplankton assemblage but cuphausiids were also very important in terms of biomass contribution. Dirunal vertical migrations were most pronounced for the euphausiids and the copepod Metridia gerlachei. The copepods Eucalanus longipes, Rhincalanus gigas and Microsetella sp. showed significant, but lesser, diurnal vertical migrations. A daylight decrease in zooplankton biomass was observed consistently on the island shelf, compared to the pattern found in deep-water. Data from daytime tows collected during April/May 1983 show that zooplankton biomass in the area increases with depth up to a stability level of about 50 mg/m³ (dry weight). It is suggested that an interaction between vertical migrations, surface Ekman drift and bottom topography results in zooplankton mass depletion by visual predators during daytime and replenishment during the night. The nocturnal advection of allochtonous zooplankton into the area may represent an input of food supply equivalent to as much as 2.2 times the local maximum phytoplankton production.     

Chemical interactions between planktonic crustaceans

Three levels of chemical communications involved plankton Crustacea are considered: 1) Influence of zooplankton excretion on phytoplankton; 2) Influence of zooplankton excretion on the individuals of the same or other species of the same trophic level; 3) Influence of chemical cues released by predatory zooplankton and fish on herbivorous zooplankton. The data on the influence of excreted cues on some physiological (growth, reproduction, feeding, etc.) and behavioural (vertical and horizontal migrations) characters of planktonic crustaceans are presented. Ecological role and chemistry cues responsible for the interactions of different trophic levels can be different. It is considered that chemical communications in aquatic ecosystems can be provided with: 1) Species-specific cues that strictly influence particular biological functions (communication system of feromone type); 2) Non-specific cues that strictly influence particular functions (system of regulator, that act at the whole ecosystem as the hormonal system of an organism). 3) Non-specific substances with broad (non-specidic) influence--toxic substances of "biocondition substances" according to classification of Novikov and Kharlamova (2000).     

Inducible defences and the paradox of enrichment

In order to evaluate the effects of inducible defences on community stability and persistence, we analyzed models of bitrophic and tritrophic food chains that incorporate consumer-induced polymorphisms. These models predict that intra-specific heterogeneity in defence levels resolves the paradox of enrichment for a range of top-down effects that affect consumer death rates and for all possible levels of primary productivity. We show analytically that this stability can be understood in terms of differences in handling times on the different prey types. Our predictions still hold when defences also affect consumer attack rates. The predicted stability occurs in both bitrophic and tritrophic food chains.
Inducible defences may promote population persistence in tritrophic food chains. Here the minimum densities of cycling populations remain bound away from zero, thus decreasing the risk of population extinctions. However, the reverse can be true for the equivalent bitrophic predator–prey model. This shows that theoretical extrapolations from simple to complex communities should be made with caution. Our results show that inducible defences are among the ecological factors that promote stability in multitrophic communities.     

The effects of mysid grazing on kelp zoospore survival and settlement

Recent studies have indicated that long‐distance dispersal by kelp zoospores may play an important role in the colonization of newly exposed rocky habitats and in the recovery of recently disturbed kelp forests. This may be facilitated by the vertical transport of zoospores into the shallower portions of the water column where they are exposed to greater alongshore currents that increase their dispersal potential. However, this vertical transport can also expose them to elevated irradiances and enhanced grazing by zooplankton, both of which negatively impact zoospore survival and settlement. In this study, we used plankton tows to show that zooplankton (mysids) were at least seven times more abundant in the surface waters than near the benthos along the edge of a large kelp forest at the time of our spring sampling. We then used feeding experiments and epifluorescence microscopy to verify that these mysids grazed on kelp zoospores. Finally, we conducted laboratory experiments to show that grazing by these mysids over a 12 h period reduced kelp zoospore settlement by at least 50% relative to treatments without grazing. Together with previous studies that have revealed the impacts of high irradiance on zoospore survival and settlement, our study indicates that the vertical transport of kelp zoospores into the shallower portions of the water can also expose them to significantly increased mortality from mysid grazing. Thus, if these patterns are consistent over broader temporal and geographic scales, vertical transport may not be a viable method for sustained long‐distance zoospore dispersal.     

青藏高原柴达木盆地尕海盐湖浮游生物群落多样性特征的初步研究

青海尕海是青藏高原柴达木盆地比较典型的高盐度且具有丰富卤虫资源的盐湖 ,海拔高程 2 849.6m。 1997年夏季我们对尕海盐湖浮游生物主要类群群落多样性特征进行了初步调查。调查期间在内湖主要水体 5个断面2 2个采样站共发现浮游藻类 46种 ,平均密度为 5 4.39× 10 4 Cells/L ;浮游动物 12种 ,全湖平均密度为 8.2 2个 /L ,平均生物量 0 .2 9mg/L。通过盐度含量较高 (119g/L)的内湖主要水体采样断面与盐度含量较低 (1.8g/L)的湖西北岸小水面采样断面比较 ,浮游生物不论是在种类组成特征、群落的多样性还是其个体丰度都存在十分明显的差异。结果表明 :在盐湖生态系统中 ,盐度是决定生物物种多样性及其个体丰度的关键因素之一。     

Diel vertical movements of zooplankton in lake La Cruz (Cuenca, Spain)

The study of diel vertical movements of zooplankton in a smallmeromictic karstic lake (lake La Cruz), presenting highly stratifiedwaters, was performed using two different methodologies: (i)samples were taken along the vertical profile and were comparedat different hours in a diel cycle; (ii) some plankton trapswere located at different depths, covering different periodsof time, to catch organisms going upwards and downwards. Themain subject of this study has been the vertical movements affectingrotifers since they were dominant in the zooplankton of thislake, but we have also included the results obtained for otherzooplankton groups. The results indicate an almost general movementin epilimnetic waters corresponding to the ‘normal’pattern of migration (ascent at dusk and descent at dawn); inmetalimnetic and hypolimnetic waters, vertical movements weregreatly reduced and were more independent of the diel cycle.The results also confirm that the dense populations at theselevels of the oxic–anoxic boundary are made up of activeanimals. Among the causes accounting for our results, the cyclesof activity (mainly feeding) connected with the diel cycle couldbe important in explaining vertical movements of filter-feederrotifers. In larger zooplankters, visual predation might bethe main reason for such behavior.     

Effects of omnivorous filter‐feeding fish and nutrient enrichment on the plankton community and water transparency of a tropical reservoir

1. The major aim of this study was to test the hypothesis that nutrient enrichment and the introduction of the Nile tilapia (Oreochromis niloticus), an exotic omnivorous filter‐feeding fish, operate interdependently to regulate plankton communities and water transparency of a tropical reservoir in the semi‐arid northeastern Brazil. 2. A field experiment was performed for 5 weeks in 20 enclosures (9.8 m³) to which four treatments were randomly allocated: tilapia addition (F), nutrient addition (N), tilapia and nutrient addition (F + N) and a control treatment with no tilapia or nutrient addition (C). A two‐way repeated measures anova was undertaken to test for time, tilapia and nutrient effects and their interactions on water transparency, total phosphorus and total nitrogen concentrations, phytoplankton biovolume and zooplankton biomass. 3. Nutrient addition had no effect except on rotifer biomass, but there were significant fish effects on the biomass of total zooplankton, copepod nauplii, rotifers, cladocerans and calanoid copepods and on the biovolume of total phytoplankton, large algae (GALD ≥ 50 μm), Bacillariophyta and Zygnemaphyceae and on Secchi depth. In addition, we found significant interaction effects between tilapia and nutrients on Secchi depth and rotifers. Overall, tilapia decreased the biomass of most zooplankton taxa and large algae (diatoms) and decreased water transparency, while nutrient enrichment increased the biomass of rotifers, but only in the absence of tilapia. 4. In conclusion, the influence of fish on the reservoir plankton community and water transparency was significant and even greater than that of nutrient loading. This suggests that biomanipulation of filter‐feeding tilapias may be of importance for water quality management of eutrophic reservoirs in tropical semi‐arid regions.     

Qualitative assessment of the diet of European eel larvae in the Sargasso Sea resolved by DNA barcoding

European eels (Anguilla anguilla) undertake spawning migrations of more than 5000 km from continental Europe and North Africa to frontal zones in the Sargasso Sea. Subsequently, the larval offspring are advected by large-scale eastward ocean currents towards continental waters. However, the Sargasso Sea is oligotrophic, with generally low plankton biomass, and the feeding biology of eel larvae has so far remained a mystery, hampering understanding of this peculiar life history. DNA barcoding of gut contents of 61 genetically identified A. anguilla larvae caught in the Sargasso Sea showed that even the smallest larvae feed on a striking variety of plankton organisms, and that gelatinous zooplankton is of fundamental dietary importance. Hence, the specific plankton composition seems essential for eel larval feeding and growth, suggesting a linkage between eel survival and regional plankton productivity. These novel insights into the prey of Atlantic eels may furthermore facilitate eel larval rearing in aquaculture, which ultimately may replace the unsustainable use of wild-caught glass eels.     

How internal waves influence the vertical distribution of zooplankton

1. We present data with a high spatio‐temporal resolution from a 72‐h field survey in Bautzen Reservoir (Saxony, Germany). The aims of this survey were to observe hydrophysical processes during a period of unstable stratification in spring and investigate the effect of wind‐induced internal waves on the vertical distribution of zooplankton. 2. Wind velocities up to 10 m s⁻¹ caused a strong downwelling event of warm water at the sampling site and led to the generation of internal waves with an amplitude of 4 m. 3. The zooplankton community, which was dominated by Daphnia galeata, inhabited epilimnetic waters. Downwelling enlarged the thickness of the epilimnetic layer and, hence, led to high zooplankton abundances down to relatively deep water strata indicating lateral transport of zooplankton. As a consequence, area‐specific zooplankton abundances increased considerably (max. fourfold) during downwelling. 4. We conclude that classical limnological field sampling, such as for monitoring purposes, can lead to severely biased estimates of zooplankton abundance due to the interfering effects of hydrophysical processes like internal waves. 5. Backscattering strengths measured by a simultaneously deployed Acoustic Doppler Current Profiler (600 kHz) were found to be correlated with estimated zooplankton abundances based on plankton samples.     

Vertiquant: A Device for Automatically Recording Vertical Migration of Plankton

Vertical migration is a key subject in understanding zooplankton ecology and its influence on aquatic ecosystems. This paper introduces a device for automatically recording vertical plankton migrations to study proximate factors regulating the stimulus, timing and amplitude of these movements under controlled laboratory conditions. The instrument records the light scattered by organisms at their respective depths and processes the signals in real time to a graphic representation of the organisms vertical distribution. Organisms of different taxa from a size of <40 μ, to > 10 000 μm were used for these experiments. Daphnia migrations in response to UV light are used to demonstrate the basic functions of the instrument.     

Eat and run? The hunger/satiation hypothesis in vertical migration: history,evidence and consequences

The study of vertical migrations in aquatic organisms has a long and colourful history, much of it to do with the effects of changing sampling technology on our understanding of the phenomenon. However, the overwhelming majority of such studies carried out today still depend on detecting differences in vertical distribution profiles during some course of time, or acoustic echoes of migrating bands of organisms. These can not distinguish migratory activity of individual organisms, but can only assess net results of mass transfers of populations, which may integrate many individual migrations. This is an important distinction, for without knowing the actual movements of individuals it seems unlikely that we will be able to understand their causes, nor the effects of vertical migrations on the environment or on the migrators themselves. This review examines evidence for individual vertical movements gathered from 'tracers', mainly gut contents, and reviews the evidence for the hypothesis that such movements are in fact driven by hunger and satiation. The more recently appreciated vertical migrations of phytoplankters and their similarities in form and driving forces to those of zooplankton and nekton are also discussed. Finally, the role of vertical migrators in vertical fluxes of materials is discussed, along with the consequences of satiation-driven descent for such estimates.     

Water level and fish-mediated cascading effects on the microbial community in eutrophic warm shallow lakes: a mesocosm experiment

Information on the effects of water level changes on microbial planktonic communities in lakes is limited but vital for understanding ecosystem dynamics in Mediterranean lakes subjected to major intra- and inter-annual variations in water level. We performed an in situ mesocosm experiment in an eutrophic Turkish lake at two different depths crossed with presence/absence of fish in order to explore the effects of water level variations and the role of top-down regulation at contrasting depths. Strong effects of fish were found on zooplankton, weakening through the food chain to ciliates, HNF and bacterioplankton, whereas the effect of water level variations was overall modest. Presence of fish resulted in lower biomass of zooplankton and higher biomasses of phytoplankton, ciliates and total plankton. The cascading effects of fish were strongest in the shallow mesocosms as evidenced by a lower zooplankton contribution to total plankton biomass and lower zooplankton:ciliate and HNF:bacteria biomass ratios. Our results suggest that a lowering of the water level in warm shallow lakes will enhance the contribution of bacteria, HNF and ciliates to the plankton biomass, likely due to increased density of submerged macrophytes (less phytoplankton); this effect will, however, be less pronounced in the presence of fish.     

Plankton Community Succession in Artificial Systems Subjected to Cyanobacterial Blooms Removal using Chitosan-Modified Soils

Using artificial systems to simulate natural lake environments with cyanobacterial blooms, we investigated plankton community succession by polymerase chain reaction–denaturing gradient gel electrophoresis (PCR-DGGE) fingerprinting and morphological method. With this approach, we explored potential ecological effects of a newly developed cyanobacterial blooms removal method using chitosan-modified soils. Results of PCR-DGGE and morphological identification showed that plankton communities in the four test systems were nearly identical at the beginning of the experiment. After applying the newly developed and standard removal methods, there was a shift in community composition, but neither chemical conditions nor plankton succession were significantly affected by the cyanobacteria removal process. The planted Vallisneria natans successfully recovered after cyanobacteria removal, whereas that in the box without removal process did not. Additionally, canonical correspondence analysis indicated that other than for zooplankton abundance, total phosphorus was the most important environmental predictor of planktonic composition. The present study and others suggest that dealing with cyanobacteria removal using chitosan-modified soils can play an important role in controlling cyanobacterial blooms in eutrophicated freshwater systems.