Why plankton communities have no equilibrium: solutions to the paradox

In a classical paper, Hutchinson (1961) argued that the large number of species in most plankton communities is remarkable in view of the competitive exclusion principle, which suggests that in homogeneous, well-mixed environments species that compete for the same resources cannot coexist. Few ideas in aquatic ecology have evoked more research than this `paradox of the plankton'. This review is an effort to put the main solutions to the paradox that have been proposed over the years into perspective. Hutchinson himself already suggested that the explanation could be that plankton communities are not in equilibrium at all due to weather-driven fluctuations. Subsequent research confirmed that such externally imposed variability can allow many species to coexist. Another important point is that in practice the homogeneous well-mixed conditions assumed in the competitive exclusion principle hardly exist. Even the open ocean, for instance, has a spatial complexity resulting from meso-scale vortices and fronts that can facilitate coexistence of species. Perhaps most excitingly, theoretical work on species interactions has given a counter-intuitive new dimension to the understanding of diversity. Various competition and predation models suggest that even in homogeneous and constant environments plankton will never settle to equilibrium. Instead, interactions between multiple species may give rise to oscillations and chaos, with a continuous wax and wane of species within the community. Long-term laboratory experiments support this view. This chaotic behavior implies among other things that plankton dynamics are intrinsically unpredictable in the long run when viewed in detail. Nonetheless, on a higher aggregation level, indicators such as total algal biomass may show quite regular patterns.     

Towards a solution of the plankton paradox: the importance of physiology and life history

Phytoplankton communities reveal an astonishing biodiversity, whereas classical competition theory seems to suggest that only a few competing species can survive. Recently we suggested a new solution to this plankton paradox. In theory, at least, competition between multiple species can generate complex dynamics that can support a large number of species. How likely is it then, in reality, that competitive chaos indeed promotes biodiversity? To obtain some insight, we simulated multispecies competition according to five different physiological scenarios. For random species parameters, biodiversity was generally low. Assuming plausible physiological trade‐offs, the simulations revealed switches back and forth between equilibrium and nonequilibrium dynamics, and a higher biodiversity. An extremely high biodiversity, with sometimes more than 100 species on three resources, was observed in simulations that assumed a cyclic relation between competitive abilities and resource contents. We conclude that physiological and life‐history patterns have a major impact on the likelihood of nonequilibrium dynamics and on the biodiversity of plankton communities.     

Interaction among Non-toxic Phytoplankton,Toxic Phytoplankton and Zooplankton: Inferences from Field Observations

We explore the mutual dependencies and interactions among different groups of species of the plankton population, based on an analysis of the long-term field observations carried out by our group in the North–West coast of the Bay of Bengal. The plankton community is structured into three groups of species, namely, non-toxic phytoplankton (NTP), toxic phytoplankton (TPP) and zooplankton. To find the pair-wise dependencies among the three groups of plankton, Pearson and partial correlation coefficients are calculated. To explore the simultaneous interaction among all the three groups, a time series analysis is performed. Following an Expectation Maximization (E-M) algorithm, those data points which are missing due to irregularities in sampling are estimated, and with the completed data set a Vector Auto-Regressive (VAR) model is analyzed. The overall analysis demonstrates that toxin-producing phytoplankton play two distinct roles: the inhibition on consumption of toxic substances reduces the abundance of zooplankton, and the toxic materials released by TPP significantly compensate for the competitive disadvantages among phytoplankton species. Our study suggests that the presence of TPP might be a possible cause for the generation of a complex interaction among the large number of phytoplankton and zooplankton species that might be responsible for the prolonged coexistence of the plankton species in a fluctuating biomass.     

Does “supersaturated coexistence” resolve the “paradox of the plankton”?

In contradiction with field observations, theory predicts that the number of coexisting plankton species at equilibrium cannot exceed the number of limiting resources, which is called the "paradox of the plankton". Recently, Huisman & Weissing (1999 , 2000 ) showed, in a model study, that the number of coexisting species may exceed the number of limiting resources when internal system feedback induces oscillations or chaos. In this paper, we use the term "supersaturated coexistence" for this phenomenon. On the basis of these findings, they claimed that the paradox of the plankton is solved. We investigated the prerequisites for supersaturated coexistence in the same model. Our results indicate that supersaturated coexistence is a rare phenomenon in parameter space, requires a very precise parameterization of the community members and is sensitive to the introduction of new species and the removal of the present species. This raises the question of whether supersaturated coexistence is likely to occur in nature. We conclude that the claim by Huisman & Weissing (1999 , 2000 ) is premature.     

Toxic phytoplankton as a keystone species in aquatic ecosystems: stable coexistence to biodiversity

The effect of allelochemicals released by toxic species in plankton community is often taken into account to reveal plankton biodiversity. Using a minimal chemostat model we show that the interaction between toxic and non‐toxic phytoplankton species with changing competitive effects among species due to allelopathy helps to promote the stable coexistence of many species on a single resource and hence can solve the paradox of plankton. We emphasize toxic phytoplankton as a keystone species that strongly uncovers its allelochemicals on other non‐toxic phytoplankton and enhances the species persistence and diversity in aquatic ecosystems. In addition, we analyze the consistency of ecosystem functioning and species diversity using a number of approaches, such as sampling hypothesis with selection and complementarity effects, cascading extinction–reinvasion, and examining system dynamics at different enrichment levels and toxicity. Our results suggest that chemostats with one toxic and one or more nontoxic phytoplankton species can be used for the experimental verification of the stable coexistence of many species on a single resource in aquatic ecology.     

Competing Effects of Toxin-Producing Phytoplankton on Overall Plankton Populations in the Bay of Bengal

The coexistence of a large number of phytoplankton species on a seemingly limited variety of resources is a classical problem in ecology, known as ‘the paradox of the plankton’. Strong fluctuations in species abundance due to the external factors or competitive interactions leading to oscillations, chaos and short-term equilibria have been cited so far to explain multi-species coexistence and biodiversity of phytoplankton. However, none of the explanations has been universally accepted. The qualitative view and statistical analysis of our field data establish two distinct roles of toxin-producing phytoplankton (TPP): toxin allelopathy weakens the interspecific competition among phytoplankton groups and the inhibition due to ingestion of toxic substances reduces the abundance of the grazer zooplankton. Structuring the overall plankton population as a combination of nontoxic phytoplankton (NTP), toxic phytoplankton, and zooplankton, here we offer a novel solution to the plankton paradox governed by the activity of TPP. We demonstrate our findings through qualitative analysis of our sample data followed by analysis of a mathematical model.     

Resisting annihilation: relationships between functional trait dissimilarity,assemblage competitive power and allelopathy

Allelopathic species can alter biodiversity. Using simulated assemblages that are characterised by neutrality, lumpy coexistence and intransitivity, we explore relationships between within‐assemblage competitive dissimilarities and resistance to allelopathic species. An emergent behaviour from our models is that assemblages are more resistant to allelopathy when members strongly compete exploitatively (high competitive power). We found that neutral assemblages were the most vulnerable to allelopathic species, followed by lumpy and then by intransitive assemblages. We find support for our modeling in real‐world time‐series data from eight lakes of varied morphometry and trophic state. Our analysis of this data shows that a lake's history of allelopathic phytoplankton species biovolume density and dominance is related to the number of species clusters occurring in the plankton assemblages of those lakes, an emergent trend similar to that of our modeling. We suggest that an assemblage's competitive power determines its allelopathy resistance.     

Spatial Interaction Among Nontoxic Phytoplankton, Toxic Phytoplankton, and Zooplankton: Emergence in Space and Time

In homogeneous environments, by overturning the possibility of competitive exclusion among phytoplankton species, and by regulating the dynamics of overall plankton population, toxin-producing phytoplankton (TPP) potentially help in maintaining plankton diversity—a result shown recently. Here, I explore the competitive effects of TPP on phytoplankton and zooplankton species undergoing spatial movements in the subsurface water. The spatial interactions among the species are represented in the form of reaction-diffusion equations. Suitable parametric conditions under which Turing patterns may or may not evolve are investigated. Spatiotemporal distributions of species biomass are simulated using the diffusivity assumptions realistic for natural planktonic systems. The study demonstrates that spatial movements of planktonic systems in the presence of TPP generate and maintain inhomogeneous biomass distribution of competing phytoplankton, as well as grazer zooplankton, thereby ensuring the persistence of multiple species in space and time. The overall results may potentially explain the sustainability of biodiversity and the spatiotemporal emergence of phytoplankton and zooplankton species under the influence of TPP combined with their physical movement in the subsurface water.     

Towards a resolution of ‘the paradox of the plankton’: A brief overview of the proposed mechanisms

In plankton ecology, it is a fundamental question as to how a large number of competing phytoplankton species coexist in marine ecosystems under a seemingly-limited variety of resources. This ever-green question was first proposed by Hutchinson [Hutchinson, G.E., 1961. The paradox of the plankton. Am. Nat. 95, 137–145] as ‘the paradox of the plankton’. Starting from Hutchinson [Hutchinson, G.E., 1961. The paradox of the plankton. Am. Nat. 95, 137–145], over more than four decades several investigators have put forward varieties of mechanisms for the extreme diversity of phytoplankton species. In this article, within the boundary of our knowledge, we review the literature of the proposed solutions and give a brief overview of the mechanisms proposed so far. The proposed mechanisms that we discuss mainly include spatial and temporal heterogeneity in physical and biological environment, externally imposed or self-generated spatial segregation, horizontal mesoscale turbulence of ocean characterized by coherent vortices, oscillation and chaos generated by several internal and external causes, stable coexistence and compensatory dynamics under fluctuating temperature in resource competition, and finally the role of toxin-producing phytoplankton in maintaining the coexistence and biodiversity of the overall plankton population that we have proposed recently. We find that, although the different mechanisms proposed so far is potentially applicable to specific ecosystems, a universally accepted theory for explaining plankton diversity in natural waters is still an unachieved goal.     

Specific features of the feeding of larval fish of the families Blenniidae and Gobiidae in relation to changes in the coastal plankton community of the Black Sea

Data on the feeding of larvae of mass Black Sea fish species of the families Blenniidae and Gobiidae with a length of 2.2–7.0 mm from coastal waters of the Crimea (Sevastopol) are presented. Despite the tendency for an improvement in the feeding of larval fish, Mnemiopsis leidyi, in the case of a prolonged staying in the plankton in mass amounts in the absence of Beroe ovata, exerts a negative effect on the food resources and the survival of larvae. This is evidenced by the indices of food consumption and the proportion of larvae with empty intestines.     

Biological activity in the wake of an island close to a coastal upwelling

Hydrodynamic forcing plays an important role in shaping the dynamics of marine organisms, in particular of plankton. In this work we study the planktonic biological activity in the wake of an island which is close to an upwelling region. Our research is based on numerical analysis of a kinematic flow mimicking the hydrodynamics in the wake, coupled to a three-component plankton model.We use parameter values relevant for the Canary wake, and the main results for a realistic range of parameters in this area are as follows: (a) Primary production is enhanced in the region of the wake opposite to the upwelling zone. (b) There is a strong dependence of the productivity on the inflow conditions of biological material entering the wake transported by the main current. Finally (c) we show that under certain conditions the interplay between wake structures and biological growth leads to plankton blooms inside mesoscale hydrodynamic vortices that act as incubators of primary production.     

Fusing spatial resource heterogeneity with a competition–colonization trade-off in model communities

Two commonly cited mechanisms of multispecies coexistence in patchy environments are spatial heterogeneity in competitive abilities caused by variation in resources and a competition–colonization trade-off. In this paper, a model that fuses these mechanisms together is presented and analyzed. The model suggests that spatial variation in resource ratios can lead to multispecies coexistence, but this mechanism by itself is weak when the number of resources for which species compete is small. However, spatial resource heterogeneity is a powerful mechanism for multispecies coexistence when it acts synergistically with a competition–colonization trade-off. The model also shows how resource supply can control the competitive balance between species that are weak competitors but superior colonizers and strong competitors/inferior colonizers. This provides additional theoretical support for a possible explanation of empirically observed hump-shaped relationships between species diversity and ecological productivity.     

The role of predation for seasonal variability patterns among phytoplankton and ciliates

Investigating the mechanisms which underlie the biomass fluctuations of populations and communities is important to better understand the processes which buffer community biomass in a variable environment. Based on long-term data of plankton biomass in Lake Constance (Bodensee), this study aims at explaining the different degree of synchrony among populations observed within two freshwater plankton groups, phytoplankton and ciliates. Established measures of temporal variability such as the variance ratio and cross-correlation coefficients were combined with first-order autoregressive models that allow estimating species interactions from time-series data. We found that predation was an important driver of the observed seasonal variability patterns in phytoplankton and ciliates, and that competitive interactions only played a subordinate role. In Lake Constance copepods and cladocerans, two major invertebrate predator groups, focus their grazing pressure at different times of the season. Model results suggested that compensatory dynamics detected in phytoplankton originate from the differential vulnerability of species to either one of these two predator groups. For ciliates model results advocated that synchrony among species occurs because ciliates tend to be vulnerable to both predator groups. Our findings underline the necessity of extending studies of community variability to multiple trophic levels because accounting for predator-prey interactions may often be more important than accounting for competitive interactions at one trophic level.     

常熟沿江湿地物种资源现状与保护措施

为弄清常熟沿江湿地的资源现状,提供湿地保护依据,采用野外采样和室内分析方法,从区域大尺度及生境小尺度获得湿地动植物物种科属组成、分布特征和物种生物量等信息;并对物种间的相关性和浮游生物与水质间的相关性进行了分析.结果表明:观测区植被以芦苇(Phragmites australis)、菰(Zizania latifolia)、蔗草(Scirpus planiculmis)为优势种;直链藻(Melosira italica)和铜锈微囊藻(Microcystis aeruginosa)是浮游植物中的优势种;浮游生物和底栖动物多样性较低,渔业资源相对丰富;植被、浮游生物多样性指数与底栖动物栖息密度相关性显著,而长江汛期水质与浮游生物之间没有显著相关.在湿地面积逐渐减少、生物资源日益匮乏的现状下,应从恢复湿地面积、加强动态监测和建立科学开发模式3个方面保护沿江湿地.     

Estimation of the biomass of plankton

Summary A mathematical function is demonstrated in the numbers of individuals of the various species in a planktonic biocoenosis. The logarithms of the numbers form a Gauss or normal probability curve. A similar probability relation is found in the volumes of the individuals of the various species as well as in the biomass of the various populations.This relationship in the numbers is caused by the effect of the numerous ecological factors influencing the rate of proliferation of the various plankton species. The cause of this relationship concerning the volumes of the various species is not understood. The relationship between the various biomasses is the mathematical product of number and mean volume.An approximate hyperbolic function can be derived from the population volumes and with the aid of a simple equation the plankton biomass is calculated. A modus operandi is given to abbreviate the work necessary to determine the plankton biomass with Lohmann's method. Only ten or twenty of the most dominant populations out of all species present in a plankton sample, have to be counted and measured.The biomasses of the populations in various plankton samples may easily be compared using the hyperbolic or the probability relationship.The biomasses of plankton in various habitats may easily be compared in a graphic way. The logarithms of the biomasses found during the year follow a probability curve and may be plotted and compared on a cumulative logarithmic probability graph.The number of organisms of each species to be counted depends on the degree of accuracy and has to be about a hundred. A chance determined spread is always found in plankton counts.The spatial distribution of most plankters shows a very broad spread. Therefore, sampling at ten places and working with the mean of the ten samples is compulsory.Some gregariously living zooplankters form bunches in the water. A reliable mean may be calculated using the hyperbolic function which seems to describe their densities at the various places.From the existing methods of collection of plankton the rotary, electric pump is chosen. A translucent hose with a special and moving mouth is let down into the water. First the water passes through the plankton-net and after that through the pump and the water-meter. A series of 7 samples of increasing decimal volumes is drawn in this way. From these samples the plankton is concentrated and fractionated by means of two sedimentation chambers, four small plankton sieves and three plankton nets. The sieves and nets have various standardized meshes.Square counting chambers of 10 cm² area are used. These chambers have a thin glass bottom and a broad rim. The sedimentation chambers and the small plankton sieves fit on and into the chambers thus minimizing the loss of organisms.The plankton organisms are enumerated by means of an inverted microscope projecting the image on a ground glass which makes counting easier. Only those organisms seen within a measured square on the ground glass are counted.By standardization of the sample volumes, the magnifications of the microscope and the dimensions of the squares the conversion factors are so simple that only zeros or a decimal point have to be placed in the number counted to obtain the result.International standardization of the method of estimation of the biomass of plankton and the expression of the results is proposed.     

Standing out from the crowd: Spotting your targets in a mixed plankton sample

The diversity of marine organisms is staggering, and this fact is readily appreciated by microscopic examination of the contents of a plankton net after a short tow across the ocean surface. Although this diversity is beautiful, it can present a significant problem for those seeking to extract information about a single species of interest. Enumeration of the eggs and larvae of a specific target species can provide a quantitative window into reproductive dynamics that are of great use for fisheries stock assessment and management. But how do you efficiently sort through the mass of plankton and identify target species’ eggs and larvae that may be morphologically indistinguishable from those of a number of other local species? In this issue of Molecular Ecology Resources, Oxley et al. ( 2017 ) describe an innovative in situ hybridization (ISH) approach that successfully solves this important problem and opens an exciting new avenue to ichthyoplankton analysis that may be widely adopted by both fish ecologists and fisheries managers.     

Biodiversity of testate amoebae (Arcellinida and Euglyphida) in different habitats of a lake in the Upper Paraná River floodplain

This study aimed to investigate the testate amoebae (Arcellinida and Eugliphida) species diversity in plankton, macrophytes and aquatic sediment samples from a shallow lake of the Upper Paraná River floodplain. Samples were carried out from April 2007 to March 2008. We recorded 89 taxa, belonging to 10 families. Eighty-two taxa were found in the aquatic sediment, 71 in the macrophytes and 53 in the plankton. Highest values of alpha diversity were observed in the aquatic sediment. Although the plankton had the highest number of accidental species, accessory and constant species were also observed in this habitat. Most of the species classified as constant for the plankton belonged to the genus Arcella. Most of the constant species in the macrophytes and aquatic sediment belonged to the genus Difflugia. This study supports the idea that the presence of these protists in the plankton should not be attributed only to stochastic processes because (i) the species diversity recorded in this habitat was remarkably high in relation to the total biodiversity of the lake, and (ii) we also recorded frequent and constant species in the plankton.     

Relations between biological diversity in continental waterbodies and their morphometry and water mineralization

The number of phytoplankton, zooplankton, and macrobenthos species was studied in continental lakes of diverse origin, geographical position, and hydrochemical (water mineralization) and morphological (area and capacity) characteristics. It is shown that the diversity of benthos communities depends on mineralization, area, and capacity of the waterbody, the dependence on area and mineralization being stronger than the dependence on capacity. Zooplankton community diversity depends on water mineralization and, to a very small extent, on waterbody area. The number of phytoplankton species in a lake is not strictly determined by morphometric characteristics and water mineralization. This number is to a greater extent dependent on other factors (e.g., light, nutrients, etc.). The largest number of benthos and plankton species was observed in waterbodies with water mineralization around 0.4 g/l. Increase in mineralization leads not only to decrease in species number, but also to simplification of community structure in plankton and bottom organisms, which is reflected by the Shannon index of diversity decreasing accordingly. The studied relations show wide dispersal in the number of species that can result, beside other factors unaccounted for, from the uneven reliability of the identifications and recordings of plankton and benthos species due to the different proficiency level of experts in taxonomy and systematics.     

Coexistence of species competing for shared resources

In this paper we develop a mathematical model in which any number of competing species can coexist on four resources which regenerate according to an algebraic relationship. We show that previous attempts to prove that n species cannot coexist on fewer that n resources (the “competitive exclusion principle”) all make use of the very restrictive assumption that the specific growth rates of all competing species are linear functions of resource densities. When this restriction is relaxed, it becomes possible to find situations in which n species can coexist on fewer than n resources. On the basis of this and other observations we conclude that the competitive exclusion principle should be considered to apply only to coexistence at fixed densities.     

Changes in plankton and fish larvae communities across hydrographic fronts off West Greenland

The variability in plankton community structure was studiedin Disko Bay and across important fishing banks off the westcoast of Greenland. The primary goal of the study was to investigatepossible linkages between hydrographical processes and planktonstructures, hypothesizing that hydrographic fronts would bepresent in the area, and that these to a large extent determineplankton distribution, composition and productivity. We sampledalong four cross-shelf transects, one covering Disko Bay andDisko Bank, while the other three covered Store Hellefiske Bank,Lille Hellefiske Bank and Sukkertop Bank. The hydrography wasexamined by CTD profiling, the phytoplankton by fluorescenceprofiling and water bottle sampling, while mesozooplankton andichthyoplankton were sampled by vertical or oblique net hauls,respectively. We observed distinct along-shelf flowing currentsin the area (e.g. the West Greenland Current, the Polar Currentand the Irminger Current), and the physical characteristicsindicated frontogenesis at the shelf slope, in regions of 80–100m water depth. Phytoplankton and ichthyoplankton showed a cross-shelfstructuring with apparent linkages to frontal characteristics,while a more diverse pattern was observed for the mesozooplanktonwhich were dominated by Calanus finmarchicus, Calanus glacialisand Calanus hyperboreus. The relationship between hydrographiccharacteristics and plankton distribution differed among species,and apparently specific plankton communities were establishedin different areas of the shelf. For example the larvae of Boreogadussaida, Ammodytes sp., Reinhardtius hippoglossoides and Stichaeuspunctatus differed markedly in distributional characteristics.In addition to the cross-shelf structuring, marked differencesin species composition and total plankton abundance were observedin the along-shelf (north–south) direction. The latitudinaldifferences in the unicellular plankton communities are interpretedlargely within a seasonal successional framework (i.e. an earlydominance of diatoms followed by increasing importance of smallerunicellular plankton), while the ichthyo- and zooplankton communitiesalso differed by the respective dominance of species with polarversus temperate origin. Our findings suggest that the flowof major currents and the establishment of hydrographical frontsare of primary importance to the plankton communities in theWest Greenland shelf area, influencing the early life of fishand the recruitment to the important fisheries resources.