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).     

Role of infochemical mediated zooplankton grazing in a phytoplankton competition model

Infochemicals released by marine phytoplankton play important roles in food web interactions by influencing the feeding behavior and selectivity of zooplanktonic predators. Recent modeling efforts have focused on the role of such chemicals as toxic grazing deterrents in phytoplankton competition. However, infochemicals may also be utilized as grazing cues, leading predators to profitable foraging patches. Here we investigate the role of infochemical mediated zooplankton grazing in a standard 3-species phytoplankton competition model, with the aim of further elucidating the ecological role of phytoplankton derived infochemicals. We then extend this to consider a more realistic 4-species model. The models produce a range of solutions depending on the strength of competition and microzooplankton grazing selectivity. Our key result is that infochemical chemoattractants, which increase the susceptibility of the producer to grazing, can provide a refuge for both competing phytoplankton species by attracting carnivorous copepods to consume microzooplankton grazers in a multi-trophic interaction. Our results indicate that infochemicals potentially have important consequences for the dynamics of marine food webs.     

Day/night differences in the grazing impact of marine copepods

Day/night differences in the removal rate of phytoplankton can occur as a result of increased copepod grazing rates at certain times of the day and diel vertical migration of animals. We conducted shipboard grazing experiments and fine-scale vertical zooplankton sampling to resolve these behaviors. Day/night feeding differences were compared in the center of several warm-core Gulf Stream rings, under conditions of no lateral water mass exchange, in the mesohaline portion of Chesapeake Bay and when following drogues in the Chesapeake Bay plume. Day/night variations in copepod biomass in the surface mixed layer were greater in neritic waters as compared to the open ocean stations. Day/night differences in weight-specific copepod filtration rates varied less than biomass. At the neritic stations copepod grazing was often higher at night, whereas at the oceanic stations day/night grazing rates were similar or daytime grazing rates were highest. The night/day ratio of zooplankton grazing impact on the phytoplankton community (the product of zooplankton biomass and their weight-specific grazing rate) averaged 4.8 in the Chesapeake Bay plume and 1.6 in warm-core Gulf Stream rings. Our results suggest that at lower food levels, there often are less day/night differences in the removal rate of phytoplankton by the copepod community.     

Learning to forage in a regenerating patchy environment: Can it fail to be optimal?

The behaviour of animals foraging along closed traplines of regenerating patches of food has been simulated using a learning rule that determines when an animal should leave the patch at which it is currently feeding to search for another one. The rule causes the animal to stay at the patch as long as it is feeding faster than it remembers doing. The foraging behaviour of one animal, and of two or more animals together, feeding in traplines containing patches of the same and of differing types has been simulated, and in all cases the foraging behaviour generated by the rule allowed the animals to exploit the food very efficiently. The learning model is also responsible for indirect social interactions among animals sharing the same trapline because the feeding of each animal reduces the availability of food for the others. This causes a population of animals to disperse themselves, on average, among patches of food according to the ideal free distribution. The relationship between the learning model and conventional optimal foraging models is examined and it is shown that it is pointless to try to account for learned behaviour in the context of optimal foraging theory.     

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.     

The role of highly unsaturated fatty acids in aquatic foodweb processes

1. Polyunsaturated fatty acids (PUFA) are almost exclusively synthesized by plants. Animals can convert from one form of PUFA to another through elongation and desaturation, but very few can synthesize PUFA de novo. PUFA play an important role in regulating cell membrane properties, serve as precursors for important animal hormones and are essential for animals. 2. In aquaculture studies, highly unsaturated fatty acids (HUFA), a subset of PUFA, have been found to be critical for maintaining high growth, survival and reproductive rates and high food conversion efficiencies for a wide variety of marine and freshwater organisms. 3. The plankton literature suggests high food-quality algae species are rich in HUFA and low food-quality algae are poor in HUFA. Adding semi-pure emulsions of HUFA to algae monocultures can markedly increase the growth rates of zooplankton feeding on these mixtures. 4. A study measuring zooplankton biomass accrual when feeding on natural phytoplankton found a strong correlation between phytoplankton HUFA (specifically eicosapentaenoic acid) content and herbivorous zooplankton production. 5. The aquatic ecology literature suggests that planktonic foodwebs with high HUFA content phytoplankton have high zooplankton to phytoplankton biomass ratios, while systems with low HUFA phytoplankton have low zooplankton biomass. Also, the seasonal succession of plankton in many temperate lakes follows patterns tied to phytoplankton HUFA content, with intense zooplankton grazing and ‘clear-water-phases’ characteristic of periods when the phytoplankton is dominated by HUFA-rich species. 6. Herbivorous zooplankton production is constrained by the zooplankton’s ability to ingest and digest phytoplankton. It is becoming increasingly clear, however, that much of the phytoplankton which is assimilated may be nutritionally inadequate. HUFA may be key nutritional constituents of zooplankton diets, and may determine energetic efficiency across the plant–animal interface, secondary production and the strength of trophic coupling in aquatic pelagic foodwebs.     

Effects of food type on diel behaviours of common carp Cyprinus carpio in simulated aquaculture pond conditions

In order to better understand behaviour patterns of common carp Cyprinus carpio in aquaculture ponds, their diel grazing, swimming, resting and schooling behaviours were observed in six 1 m² tanks under simulated pond conditions. Each tank was fertilized to stimulate natural food production before starting experiments, and then stocked with three C. carpio . Fish behaviours were compared among three treatments: (1) tanks with plankton only, (2) tanks with plankton and benthic macroinvertebrates and (3) tanks with plankton, benthic macroinvertebrates and artificial feed. Overall C. carpio grazed more frequently during daytime than at night and exhibited the reverse pattern for non-feeding swimming behaviour. A significant negative relationship ( r ² = 0·99, P < 0·01, n = 48) was observed between total per cent grazing time and total per cent swimming time. Fish dispersed to graze individually during daytime but schooled at night and did not display any agonistic behaviours. Diel variations in the vertical swimming behaviour of C. carpio were related to food types available. In tanks containing plankton only, fish grazed in the water column, whereas when benthic macroinvertebrates were present, they spent more time near the tank bottom. Resting behaviour was only seen in tanks with artificial feed and even then was rare (2–5% of total time). Results suggest that C. carpio growth and feed utilization efficiency in semi-intensive aquaculture systems could be optimized by using a combination of plankton, benthic macroinvertebrates and artificial feed, and feeding fish twice per day (at c . 0730 and c . 1630 hours).     

Planktonic food chains of a highly humic lake

The development and metabolism of epilimnetic plankton from a highly humic lake was followed in late summer, when the predominant zooplankton species, Daphnia longispina, was very abundant (ca. 200 ind. l^?1). The experiment was made in two tanks: one with an unaltered plankton assemblage and one with larger zooplankton removed. The scarce phytoplankton community was also simple, consisting mainly of one Cryptomonas and two Mallomonas species. The abundance and species composition of smaller plankton was heavily influenced by grazing of Daphnia. In particular, the biomass, of heterotrophic flagellates increased after the removal of Daphnia. The biomass and production of bacterioplankton were not affected, and remained several times higher than that of phytoplankton. Bacterial production and grazing on bacteria were balanced, and when Daphnia was removed its grazing activity was compensated by flagellates. The removal of Daphnia did not affect the respiration or community net production of plankton. Among organisms smaller than zooplankton, bacteria seemed to be responsible for most of the respiration. The community net production was consistently negative even at the water surface, indicating an allochthonous carbon source. The results suggest that phytoplankton primary production was insufficient for the secondary production in the epilimnetic water of the study lake. The food requirements of bacteria and zooplankton, as well as of flagellates, each exceeded that supplied by phytoplankton primary production. The simple food chains in this experiment made it possible to reveal the functioning of the community so completely that dissolved organic matter is certainly comparable to or exceeds the importance of phytoplankton primary production as an energy and carbon source for food webs in this humic lake.     

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.     

Day‐Night Vertical Distribution and Feeding Patterns of Fourth Instar ofChaoborus Larvae in a Neotropical Reservoir (Socuy Reservoir,Venezuela)

The day‐night vertical distribution, diel feeding activity and diet of fourth instar of Chaoborus larvae were analyzed in lacustrine zone of a neotropical reservoir which shows seasonally contrasting hypolimnetic oxygen conditions. Larvae stayed in sediment and water bottom during day and ascended to surface during night. Results indicate that feeding activity is limited mainly to the plankton population. Phytoplankton, rotifers or remains of Chaoborus larvae were not found in crops. With the exception of ostracods, all crustacean prey available in the zooplankton occurred in the guts. Ceriodaphnia cornuta and Moina micrura were the most frequent food items (about 75% of occurrence frequency) and were positively selected. The remainder crustacean zooplankton taxa were negatively selected by larvae. The most intense feeding activity in larvae occurred near midnight and sunrise, in dates when the hypolimnion was anoxic. When oxygen was available on the bottom, a higher and not changing diel feeding activity was detected. Our results indicate that vertical migration may promote a spatial separation between larvae and zooplankton, and feeding activity of larvae occurred only when both overlapped. (© 2005 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

Zooplankton grazing on Phaeocystis: a quantitative review and future challenges

The worldwide colony-forming haptophyte phytoplankton Phaeocystis spp. are key organisms in trophic and biogeochemical processes in the ocean. Many organisms from protists to fish ingest cells and/or colonies of Phaeocystis. Reports on specific mortality of Phaeocystis in natural plankton or mixed prey due to grazing by zooplankton, especially protozooplankton, are still limited. Reported feeding rates vary widely for both crustaceans and protists feeding on even the same Phaeocystis types and sizes. Quantitative analysis of available data showed that: (1) laboratory-derived crustacean grazing rates on monocultures of Phaeocystis may have been overestimated compared to feeding in natural plankton communities, and should be treated with caution; (2) formation of colonies by P. globosa appeared to reduce predation by small copepods (e.g., Acartia, Pseudocalanus, Temora and Centropages), whereas large copepods (e.g., Calanus spp.) were able to feed on colonies of Phaeocystis pouchetii; (3) physiological differences between different growth states, species, strains, cell types, and laboratory culture versus natural assemblages may explain most of the variations in reported feeding rates; (4) chemical signaling between predator and prey may be a major factor controlling grazing on Phaeocystis; (5) it is unclear to what extent different zooplankton, especially protozooplankton, feed on the different life forms of Phaeocystis in situ. To better understand the mechanisms controlling zooplankton grazing in situ, future studies should aim at quantifying specific feeding rates on different Phaeocystis species, strains, cell types, prey sizes and growth states, and account for chemical signaling between the predator and prey. Recently developed molecular tools are promising approaches to achieve this goal in the future.     

A review of planktivorous fishes: Their evolution,feeding behaviours,selectivities, and impacts

The classical approach of limnologists has been to consider the interactions between lake ecosystem components as an unidirectional flow of influence from nutrients to the phytoplankton, to the zooplankton, and finally to the fish, through successive controls by physical, chemical, and biological processes (Strakraba, 1967). The effect of planktivorous fishes on zooplankton and phytoplankton communities was not recognized until the studies of Hrbáek et al. (1961), Hrbáek (1962), Brooks & Dodson (1965) and Strakraba (1965). They showed that (1) in ponds and lakes in the presence of planktivorous fishes the zooplankton communities were composed of smaller bodied species than in those lacking planktivores, and (2) the resulting small-bodied zooplankton communities affected the phytoplankton communities. Although the variability of the phytoplankton response to fish predation showed the importance of other factors (such as nutrient limitation and interspecific competition of algae), these studies emphasized that zooplankton and phytoplankton communities can be affected by the feeding selectivity of planktivorous fishes. During the last two decades, many limnological studies have focused on this dramatic impact of fish on plankton communities. The direct response of zooplankton communities to visual fish predation (i.e. particulate feeding) has been of major interest, whereas the multilevel effects of filter-feeding fish (predation on zooplankton plus grazing on phytoplankton) have been neglected. The objectives of this review are to document fish-plankton interrelationships in order to (1) provide insights into the impact of fish on plankton communities, and (2) outline mechanistic models of planktivory according to the feeding repertory and the selectivity of the fish, the adaptive responses of the plankton, and the environmental conditions.The approach adopted here is based on field and laboratory experimental results derived from the literature on tropical and temperate freshwater (occasionally marine) systems. Four types of planktivorous fish are distinguished: the gape-limited larvae and small fish species, the particulate feeders, the pump filter feeders, and the tow-net filter feeders. For each type of planktivore, the mechanisms of prey selection are analyzed from the point of view of both the predator and the prey. To investigate the main determinants of the predator feeding selectivity, and to discuss its potential effects on prey communities, the predation-act is divided into a sequence of successive events (Holling, 1966): detection, pursuit, capture, retention, and digestion for particulate feeders; and capture, retention, and digestion for filter feeders. The strengths and weaknesses of various measures of selectivity (i.e. electivity indices), as well as their appropriate usages are considered. Available prey selection models and optimal foraging theories are analyzed for the different planktivore feeding modes. Mechanistic models based on Holling's (loc. cit.) approach are proposed for each feeding mode to determine differential prey vulnerabilities and optimal diet breadth.This review has application to several fields, including general ecology, limnology, fisheries management (for example, utilization of planktonic resources, stocking, introduction, or maintenance of natural fish populations), and biological control of the eutrophication processes (biomanipulation approaches). It emphasizes the real need for more knowledge of the feeding selectivity and food utilization of planktivores. It concludes that predator and prey are mutually adapted. Thus, in most cases, study of plankton dynamics and water quality should include the assessment of fish predation and grazing pressures.     

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.     

Toxic phytoplankton-induced spatiotemporal patterns

Here we consider a reaction diffusion system of three plankton populations, a zooplankton feeding on two phytoplankton populations, in two different settings. Firstly, the two phytoplanktons are both non-toxic and both enhance the growth of the grazing zooplankton. Secondly, we assume that one of the phytoplankton releases toxin and thereby inhibits the growth of the zooplankton. Our analytic and numerical study shows that the spatiotemporal distribution of the plankton species is uniform when both phytoplankton populations are non-toxic. However, in the presence of toxin-producing phytoplankton, the biomass distribution of all the plankton populations becomes inhomogeneous.     

Relationships between individual- and population-based plankton models

Two simulations of plankton dynamics are combined: an N/P/Zmodel and an optimal foraging strategy dependent on variablevertical migration. We show that there is no optimal individualstrategy consistent with a copepod population that has two generationsand is a significant grazer on its limiting food supply. Alternativeroles for did vertical migration are considered.     

The effect of different zooplankton grazing patterns resulting from diel vertical migration on phytoplankton growth and composition: a laboratory experiment

Diel vertical migration (DVM) of herbivorous zooplankton is a widespread behavioural phenomenon in freshwater ecosystems. So far only little attention has been paid to the impact of DVM on the phytoplankton community in the epilimnion. Some theoretical models predict that algal population growth in the epilimnion should depend on the herbivores migration and grazing patterns: even if migrating zooplankton consume the same total amount of algae per day in the epilimnion as non-migrating zooplankton, nocturnal grazing should result in enhanced algal growth and favour algal species with high intrinsic growth rates over species with lower intrinsic growth rates. To test these hypotheses we performed experiments in which several algal species were confronted with different feeding regimes of Daphnia. In the experiments algal growth did not only depend on the absolute time of grazing but was comparatively higher when grazing took place only during the night, even when the grazing pressure was the same. Furthermore, algal species with higher intrinsic growth rates had higher advantages when being grazed upon only discontinuously during the night than algal species with a smaller intrinsic growth rate. The grazing pattern itself was an important factor for relative algal performance.     

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.     

The influence of diet on foraging habitat models: a case study using nursing Antarctic fur seals

Predictable sources of food underpin lifetime reproductive output in long lived animals. The most important foraging areas of top marine predators are therefore likely to be related to environmental features that enhance productivity in predictable spatial and temporal patterns. Even so, although productive areas within the marine environment are distributed patchily in space and time, most studies assess the relationships between feeding activity and proximate, not long term, environmental characteristics. In addition, individuals within a population may exploit different prey types, and these are often associated with different hydrographic features. Until now, models attempting to associate core foraging areas (CFAs) of marine predators with the environmental characteristics of those areas have not considered the diet of individual animals, despite the influence this could have on these relationships. We used bathymetry and multi‐year (n=24) mean sea surface temperature and variability as predictors of CFAs of lactating Antarctic fur seals Arctocephalus gazella at Heard Island. The effect of prey types on the predictability of these models was explored by matching diet and foraging trip data of individual seals (n=40 seals, n=1 trip each). Differences in diet between seals were mirrored by their spatial behaviour. Foraging strategies differed both between and within groups of seals consuming different diets. Long‐term environmental parameters were useful for predicting the foraging activity of seals that consumed a single prey type with relatively specific habitat preferences, but not for those that consumed single or multiple prey types associated with more varied habitats. Ignoring individual variation in predator diet probably contributes to the poor performance of foraging habitat models. These findings highlight the importance of incorporating individual specialization in foraging behaviour into ecological models and management of predator populations.     

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.