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.     

Trophic dynamics in a whole lake experiment: size-structured interactions and recruitment variation

Horizontal and vertical heterogeneity as a result of size‐structured processes are important factors influencing indirect effects in food webs. In a whole‐lake experiment covering 5 years, we added the intermediate consumer roach (Rutilus rutilus) to two out of four lakes previously inhabited by the omnivorous top predator perch (Perca fluviatilis). We focused our study on the direct consumption effect of roach presence on zooplankton (and indirectly phytoplankton) versus the indirect effect of roach on zooplankton (and phytoplankton) mediated via effects on perch reproductive performance. The patterns in zooplankton and phytoplankton abundances were examined in relation to population density of roach and perch including young‐of‐the‐year (YOY) perch in the light of non‐equilibrium dynamics. The presence of roach resulted in changed seasonal dynamics of zooplankton with generally lower biomasses in May–June and higher biomasses in July–August in roach lakes compared to control lakes. Roach presence affected perch recruitment negatively and densities of YOY perch were on average higher in control lakes than in treatment lakes. In years when perch recruitment did not differ between lakes as a result of experimental addition of perch eggs, total zooplankton biomass was lower in treatment lakes than in control lakes. Phytoplankton biomass showed a tendency to increase in roach lakes compared to control lakes. Within treatment variation in response variables was related to differences in lake morphometry in treatment lakes. Analyses of the trophic dynamics of each lake separately showed strong cascading effects of both roach and YOY perch abundance on zooplankton and phytoplankton dynamics. Consideration of the long transients in the dynamics of top predators (fish) in aquatic systems that are related to their long life span involving ontogenetic niche shifts is essential for making relevant interpretations of experimental perturbations. This conclusion is further reinforced by the circumstance that the intrinsic dynamics of fish populations may in many cases involve high amplitude dynamics with long time lags.     

Intraspecific variation in a predator drives cascading variation in primary producer community composition

Predation has important cascading impacts on primary producer biomass and community composition in many ecosystems. While most studies have focused on the consequences of interspecific or density differences in predators, it is recognized that phenotypic variation within species can have strong and cascading community and ecosystem consequences at lower trophic levels. In coastal New England lakes, both the presence and life history form of the zooplanktivorous fish alewife, Alosa pseudoharengus, have strong influence on the biomass, size structure and community composition of crustacean zooplankton communities. Here we test the hypothesis that alewife presence and life history will have cascading impacts on phytoplankton biomass and community composition in a mesocosm experiment that previously reported strong biomass and compositional differences of crustacean zooplankton communities among alewife treatments. We show that alewife life history led to small but statistically significant differences in phytoplankton community composition among treatments. This compositional difference was driven primarily by an increase in the density of two edible phytoplankton genera associated with lower zooplankton biomass in the anadromous alewife treatment. Our results show that intraspecific variation in a predator can have cascading effects on primary producer communities. However we did not observe significant differences in total algal biomass.     

Towards resolving the paradox of enrichment: the impact of zooplankton vertical migrations on plankton systems stability

Eutrophication, often resulting from human activity, is a serious threat to aquatic communities. Theoretical analysis of this phenomenon, based on conceptual mathematical models, leads to controversial predictions known as Rosenzweig's paradox of enrichment. At the same time, field observations demonstrate that real plankton communities exhibit various mechanisms of self-regulation which can buffer negative effects of enrichment. In this paper, we study potential effects of zooplankton vertical migration on stability of plankton systems functioning. We consider an intrinsically unstable plankton model, which is characterized by an unlimited phytoplankton multiplication and population oscillations of increasing amplitude, and investigate whether vertical migrations of zooplankton can stabilize such a system at low plankton densities. By means of developing two different models accounting for different ecological situations, e.g. deep waters and shallow waters, we show that vertical migrations of zooplankton can result in stabilization of eutrophic plankton systems. Thus, we show that this mechanism, rarely taken into account in models of plankton dynamics, may be important for resolving the paradox of enrichment in plankton communities.     

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).     

Cascading effects of generalist fish introduction in oligotrophic lakes

Introduction of strictly planktivorous fish to lakes can alter plankton communities via cascading interactions in food webs. Less is known about the large-scale and long-term effects resulting from the introduction of fish with more generalist feeding habits, and the extent to which these effects depend on lake trophic status. Paleolimnological records of three oligotrophic lakes in Maine, USA were used to analyze the response of plankton communities to the introduction of white perch (Morone americana), a fish that often numerically dominates fish assemblages and switches from strict planktivory to a more generalist diet during ontogeny. After white perch introduction, cladoceran ephippia size increased up to 50 %, suggesting that the most important role of this generalist fish, with respect to water quality, is as a piscivorous trophic link. Algal standing crop declined by a quarter to over a half of pre-introduction levels, suggesting that top-down effects of white perch reduced phytoplankton biomass. In comparing these oligotrophic lakes to prior work in a eutrophic system, white perch introduction had similar effects on zooplankton body size; however, cascading effects to phytoplankton were only observed in low productivity lakes.     

Interplay between temperature,fish partial migration and trophic dynamics

Whereas many studies have addressed the mechanisms driving partial migration, few have focused on the consequences of partial migration on trophic dynamics, and integrated studies combining the two approaches are virtually nonexistent. Here we show that temperature affects seasonal partial migration of cyprinid fish from lakes to predation refuges in streams during winter and that this migration in combination with temperature affects the characteristics and phenology of lower trophic levels in the lake ecosystem. Specifically, our six‐year study showed that the proportion of fish migrating was positively related to lake temperature during the pre‐migration growth period, i.e. during summer. Migration from the lake occurred later when autumn water temperatures were high, and timing of return migration to the lake occurred earlier at higher spring water temperatures. Moreover, the winter mean size of zooplankton in the lake increased with the proportion of fish being away from the lake, likely as a consequence of decreased predation pressure. Peak biomass of phytoplankton in spring occurred earlier at higher spring water temperatures and with less fish being away from the lake. Accordingly, peak zooplankton biomass occurred earlier at higher spring water temperature, but relatively later if less fish were away from the lake. Hence, the time between phyto‐ and zooplankton peaks depended only on the amount of fish being away from the lake, and not on temperature. The intensity of fish migration thereby had a major effect on plankton spring dynamics. These results significantly contribute to our understanding of the interplay between partial migration and trophic dynamics, and suggest that ongoing climate change may significantly affect such dynamics.     

Trophic interactions in rockpool food webs: regulation of zooplankton and phytoplankton by Notonecta and Daphnia

We studied trophic interactions in experimental rockpools with three different food web structures: phytoplankton and small-bodied zooplankton; phytoplankton, small-bodied zooplankton and Daphnia ; and phytoplankton, small-bodied zooplankton, Daphnia and Notonecta . Nutrients, primary productivity, chlorophyll a and zooplankton species composition and biomass were measured over eight weeks.
2. Daphnia had a negative impact on other zooplankton and reduced the phytoplankton biomass and primary productivity. In the absence of Daphnia , small-bodied zooplankton species were abundant, in particular cyclopoid copepods. Concentrations of dissolved nutrients were lower and the standing crop of primary producers was higher when Daphnia was absent.
3. The presence of the invertebrate predator Notonecta produced a top-down effect which was similar to that reported for planktivorous fish, i.e. a selective reduction of daphnids followed by an increase of small-bodied zooplankton species and phytoplankton biomass.
4. The study showed that consumer regulation of Daphnia by Notonecta and of algae by Daphnia are important, but also demonstrated that trophic level biomasses were controlled by a combination of predation and resource limitation.     

Food-web manipulations influence grazer control of phytoplankton growth rates in Lake Michigan

Stocking piscivorous salmonids in Lake Michigan produced dramaticalterations in food-web structure, including higher numbersof large-bodied zooplankton (especially Daphnia pulicaria),lower summer chlorophyll concentrations and increased watertransparency. Experimental determinations of epilimnetic phytoplanktongrowth rates and of zooplankton grazing rates indicate thatherbivorous zooplankton controlled algal dynamics during thesummer of 1983 because grazers occupied the surface waters throughoutthe day. In 1985, however, both large- and small-bodied Daphniamade approximately equal contributions to total grazer biomass,and all grazers displayed pronounced diel vertical migrations,visiting epilimnetic waters only at night. This prohibited zooplanktonfrom controlling algal dynamics because grazing losses did notexceed phytoplankton growth rates. The changes in zooplanktoncommunity composition and behavior observed in summer 1985 probablyresulted from increased predation by visually orienting planktivorousfish, especially bloater chub (Coregonus hoyi). Effects of food-webmanipulations on phytoplankton dynamics were evident only duringJuly and August. During spring and early summer copepods dominateLake Michigan's zooplankton community. Owing to their smallbody size, copepods are less susceptible to fish predation andexhibit much lower filtering rates than Daphnia. Variabilityin zooplanktivorous fish abundance probably has little effecton phytoplankton dynamics during spring and early summer.     

Diel variation in the vertical distribution of fish and plankton in Lake Kinneret: a 24-h study of ecological overlap

Diel vertical migration (DVM) behaviour is a predator avoidance mechanism observed within many zooplankton species in the presence of zooplanktivorous fish. A 24-h survey was carried out in June 1998 to investigate diel variation in the vertical distribution of fish, zooplankton and phytoplankton (chlorophyll) in Lake Kinneret, Israel. Fish revealed diel variation in vertical distribution but had no spatial overlap with zooplankton, and consequently no apparent influence on zooplankton dispersal. Zooplankton revealed some diel variation in distribution being affected by thermocline and oxycline position and movement of the internal the internal seiche wave. Cyclopoid species closely follow the movement of the seiche wave implying that, due to their greater motility, they are following conditions that are suitable to them. The Cladocera species and small rotifers only partly, which may be part of their phototaxic behaviour. Physical forces like convection, horizontal and vertical forcing probably have a role in contributing to a homogeneous distribution of the plankton by preventing stratification or interfering with the more motile zooplankton which may be attempting to migrate.     

Substitution of top predators: effects of pike invasion in a subarctic lake

1. Invasions of top predators may have strong cascading effects in ecosystems affecting both prey species abundance and lower trophic levels. A recently discussed factor that may enhance species invasion is climate change and in this context, we studied the effects of an invasion of northern pike into a subarctic lake ecosystem formerly inhabited by the native top predator Arctic char and its prey fish, ninespined stickleback. 2. Our study demonstrated a strong change in fish community composition from a system with Arctic char as top predator and high densities of sticklebacks to a system with northern pike as top predator and very low densities of sticklebacks. A combination of both predation and competition from pike is the likely cause of the extinction of char. 3. The change in top predator species also cascaded down to primary consumers as both zooplankton and predator‐sensitive macroinvertebrates increased in abundance. 4. Although the pike invasion coincided with increasing summer temperatures in the study area we have no conclusive evidence that the temperature increase is the causal mechanism behind the pike invasion. But still, our study provides possible effects of future pike invasions in mountain lakes related to climate change. We suggest that future pike invasions will have strong effects in lake ecosystems, both by replacing native top consumers and through cascading effects on lower trophic levels.     

Vertical distribution and pigmentation of Antarctic zooplankton determined by a blend of UV radiation, predation and food availability

Selection pressure induced by simultaneously occurring environmental threats is a major evolutionary driver for organisms in terrestrial, as well as in aquatic ecosystems. For example, protection against ultraviolet radiation (UVR) and predation include both morphological and behavioral components. Here we address those selective pressures on zooplankton by performing a latitudinal monitoring, combined with mechanistic experiments in the Antarctic Southern Ocean, where the UVR-threat is extremely high. We assessed vertical distributions of zooplankton along the Antarctic coast showing that animals were most abundant at 20–80 m and tended to avoid the surface at sites with clear water. UVR-threat disappeared at between 9 and 15 m at sites with low and high water transparency, respectively. Light levels were, however, sufficient for visual fish predation down to approximately 19 and 37 m, respectively. The few zooplankton that were present in surface waters had high levels of non-pigmented UVR-protective compounds (mycosporine-like amino acids) compared to deeper dwelling zooplankton. Overall they had low levels of red pigmented UVR-protective compounds (carotenoids), suggesting high predation on pigmented individuals. In a complementary laboratory study we showed that levels of UVR-protective compounds increased considerably when zooplankton were exposed to UVR in the absence of predator cues. The recently developed transparency-regulator hypothesis predicts that UVR avoidance is an important driver to diel vertical migration in transparent waters, such as in Antarctica. We, however, conclude that copepods resided well below the level where UVR had diminished to very low levels and that predator avoidance or food availability are more likely drivers of zooplankton vertical depth distribution in transparent marine systems.     

The Impact of Nutrient State and Lake Depth on Top-down Control in the Pelagic Zone of Lakes: A Study of 466 Lakes from the Temperate Zone to the Arctic

Using empirical data from 466 temperate to arctic lakes covering a total phosphorus (TP) gradient of 2-1036 mg L-1, we describe how the relative contributions of resource supply, and predator control change along a nutrient gradient. We argue that (a) predator control on large-bodied zooplankton is unimodally related to TP and is highest in the most nutrient-rich and nutrient-poor lakes and generally higher in shallow than deep lakes, (b) the cascading effect of changes in predator control on phytoplankton decreases with increasing TP, and (c) these general patterns occur with significant variations--that is, the predation pressure can be low or high at all nutrient levels. A quantile regression revealed that the median share of the predator-sensitive Daphnia to the total cladoceran biomass was significantly related unimodally to TP, while the 10% and 90% percentiles approached 0 and 100%, respectively, at all TP levels. Moreover, deep lakes (more than 6 m) had a higher percentage of Daphnia than shallow (less than 6 m) lakes. The median percentage of Daphnia peaked at 0.15 mg L-1 in shallow lakes and 0.09 mg L-1 in deep lakes. The assumption that fish are responsible for the unimodality was supported by data on the abundance of potential planktivorous fish (catch net-1 night-1 gill nets with the different mesh sizes [CPUE]). To elucidate the potential cascading effect on phytoplankton, we examined the zooplankton phytoplankton biomass ratio. Even though this ratio was inversely related to CPUE at all TP levels, we found an overall higher ratio in oligotrophic lakes that declined toward low values (typically below 0.2) in hypertrophic lakes. These results suggest that planktivorous fish have a more limited effect on the grazing control of phytoplankton in oligotrophic lakes than in eutrophic lakes, despite similar predator control of large-bodied zooplankton. Accordingly, the phytoplankton yield, expressed as the chlorophyll a-TP ratio, did not relate to CPUE at low TP, but it increased significantly with CPUE at high TP. We conclude that the chances of implementing a successful restoration program using biomanipulation as a tool to reduce phytoplankton biomass increase progressively with increasing TP, but that success in the long term is most likely achieved at intermediate TP concentrations.     

Size‐based interactions across trophic levels in food webs of shallow Mediterranean lakes

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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.     

Differential responses of size‐based functional groups to bottom–up and top–down perturbations in pelagic food webs: a meta‐analysis

We performed a meta‐analysis of 31 lake mesocosm experiments to investigate differences in the responses of pelagic food chains and food webs to nutrient enrichment and fish presence. Trophic levels were divided into size‐based functional groups (phytoplankton into highly edible and poorly edible algae, and zooplankton into small herbivores, large herbivores and omnivorous zooplankton) in the food webs. Our meta‐analysis shows that 1) nutrient enrichment has a positive effect on phytoplankton and zooplankton, while fish presence has a positive effect on phytoplankton and a negative effect on zooplankton in the food chains; 2) nutrient enrichment has a positive effect on highly edible algae and small herbivores, but no effect on poorly edible algae, large herbivores and omnivorous zooplankton in the food webs. Planktivorous fish have a positive effect on highly edible algae and small herbivores, a negative effect on large herbivores and omnivorous zooplankton, and no effect on poorly edible algae. Our meta‐analysis confirms that nutrient enrichment and planktivorous fish affect functional groups differentially within trophic levels, revealing important changes in the functioning of food webs. The analysis of fish effects shows the well‐described trophic cascade in the food chain and reveals two trophic cascades in the food web: one transmitted by large herbivores that benefit highly edible phytoplankton, and one transmitted by omnivorous zooplankton that benefit small herbivores. Comparison between the responses of food webs and simple food chains also shows consistent biomass compensation between functional groups within trophic levels.     

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.     

Fish predation regimes modify benthic diatom community structures: Experimental evidence from an in situ mesocosm study

Diatoms are important primary producers in shallow water environments. Few studies have assessed the importance of biological interactions in structuring these communities. In the present study, benthic diatom community structure in relation to manipulated food webs was assessed using in situ mesocosms, whereby predator‐free environments and environments comprising two different fish species were assessed. Zooplankton abundance, settled algal biomass and the diatom community were monitored over a 12‐day period across each of the three trophic scenarios. Differences among treatments over time were observed in zooplankton abundances, particularly copepods. Similarly, the benthic diatom community structure changed significantly over time across the three trophic treatments. However, no differences in total algal biomass were found among treatments. This was likely the result of non‐diatom phytoplankton contributions. We propose that the benthic diatom community structure within the mesocosms was influenced by trophic cascades and potentially through direct consumption by the fish. The study highlights that not only are organisms at the base of the food web affected by predators at the top of the food web, but that predator identity is potentially an important consideration for predator–prey interaction outcomes with consequences for multiple trophic levels.     

Phytoplankton food quality control of planktonic food web processes

We developed a mechanistic model of nutrient, phytoplankton, zooplankton and fish interactions to test the effects of phytoplankton food quality for herbivorous zooplankton on planktonic food web processes. When phytoplankton food quality is high strong trophic cascades suppress phytoplankton biomass, the zooplankton can withstand intense zooplanktivory, and energy is efficiently transferred through the food web sustaining higher trophic level production. Low food quality results in trophic decoupling at the plant-animal interface, with phytoplankton biomass determined primarily by nutrient availability, zooplankton easily eliminated by fish predation, and poor energy transfer through the food web. At a given nutrient availability, food quality and zooplanktivory interact to determine zooplankton biomass which in turn determines algal biomass. High food quality resulted in intense zooplankton grazing which favored fast-growing phytoplankton taxa, whereas fish predation favored slow-growing phytoplankton. These results suggest algal food quality for herbivorous zooplankton can strongly influence the nature of aquatic food web dynamics, and can have profound effects on water quality and fisheries production. Handling editor: D. Hamilton