Melatonin signaling controls circadian swimming behavior in marine zooplankton.

Melatonin, the "hormone of darkness," is a key regulator of vertebrate circadian physiology and behavior. Despite its ubiquitous presence in Metazoa, the function of melatonin signaling outside vertebrates is poorly understood. Here, we investigate the effect of melatonin signaling on circadian swimming behavior in a zooplankton model, the marine annelid Platynereis dumerilii. We find that melatonin is produced in brain photoreceptors with a vertebrate-type opsin-based phototransduction cascade and a light-entrained clock. Melatonin released at night induces rhythmic burst firing of cholinergic neurons that innervate locomotor-ciliated cells. This establishes a nocturnal behavioral state by modulating the length and the frequency of ciliary arrests. Based on our findings, we propose that melatonin signaling plays a role in the circadian control of ciliary swimming to adjust the vertical position of zooplankton in response to ambient light.

Temperature is a poor proxy for synergistic climate forcing of plankton evolution.

Changes in biodiversity at all levels from molecules to ecosystems are often linked to climate change, which is widely represented univariately by temperature. A global environmental driving mechanism of biodiversity dynamics is thus implied by the strong correlation between temperature proxies and diversity patterns in a wide variety of fauna and flora. Yet climate consists of many interacting variables. Species probably respond to the entire climate system as opposed to its individual facets. Here, we examine ecological and morphological traits of 12 633 individuals of two species of planktonic foraminifera with similar ecologies but contrasting evolutionary outcomes. Our results show that morphological and ecological changes are correlated to the interactions between multiple environmental factors. Models including interactions between climate variables explain at least twice as much variation in size, shape and abundance changes as models assuming that climate parameters operate independently. No dominant climatic driver can be identified: temperature alone explains remarkably little variation through our highly resolved temporal sequences, implying that a multivariate approach is required to understand evolutionary response to abiotic forcing. Our results caution against the use of a 'silver bullet' environmental parameter to represent global climate while studying evolutionary responses to abiotic change, and show that more comprehensive reconstruction of palaeobiological dynamics requires multiple biotic and abiotic dimensions.

Morphology and molecular phylogeny of epizoic araphid diatoms on marine zooplankton, including Pseudofalcula hyalina gen. & comb. nov. (Fragilariophyceae, Bacillariophyta).

Some diatoms are able to colonize as epibionts on their potential zooplankton predators. Here, we report Pseudohimantidium pacificum living on the copepod Corycaeus giesbrechti and as a new finding on Oithona nana, Protoraphis atlantica living on the copepod Pontellopsis brevis, Protoraphis hustedtiana on the cypris larvae of barnacles, and Falcula hyalina on the copepod Acartia lilljeborgii. The epizoic diatoms were able to grow as free-living forms under culture conditions. Pseudohimantidium pacificum and P. atlantica appeared as the most derived species from their benthic diatom ancestors. The mucilage pad or stalk of the strains of these species showed important morphological distinction when compared with their epizoic forms. Barnacle larvae explore benthic habitats before settlement, and epibiosis on them is an example where P. hustedtiana profits from the host behavior for dispersal of its benthic populations. Molecular phylogenies based on the SSU rRNA and RuBisCO large subunit (rbcL) gene sequences revealed F. hyalina as an independent lineage within the Fragilariales (Tabularia, Catacombas, and others), consistent with its morphological distinction in the low number of rows (≤6) in the ocellulimbus, among other features. We propose the transfer of F. hyalina to the genus Pseudofalcula gen. nov. Molecular phylogeny suggests a single order for the members of the Cyclophorales and the Protoraphidales, and that the epibioses of araphid diatoms on marine zooplankton have been independently acquired several times. These clades are constituted of both epizoic and epiphytic/epilithic forms that evidence a recent acquisition of the epizoic modus vivendi.

Sheldon spectrum and the plankton paradox: two sides of the same coin-a trait-based plankton size-spectrum model.

The Sheldon spectrum describes a remarkable regularity in aquatic ecosystems: the biomass density as a function of logarithmic body mass is approximately constant over many orders of magnitude. While size-spectrum models have explained this phenomenon for assemblages of multicellular organisms, this paper introduces a species-resolved size-spectrum model to explain the phenomenon in unicellular plankton. A Sheldon spectrum spanning the cell-size range of unicellular plankton necessarily consists of a large number of coexisting species covering a wide range of characteristic sizes. The coexistence of many phytoplankton species feeding on a small number of resources is known as the Paradox of the Plankton. Our model resolves the paradox by showing that coexistence is facilitated by the allometric scaling of four physiological rates. Two of the allometries have empirical support, the remaining two emerge from predator-prey interactions exactly when the abundances follow a Sheldon spectrum. Our plankton model is a scale-invariant trait-based size-spectrum model: it describes the abundance of phyto- and zooplankton cells as a function of both size and species trait (the maximal size before cell division). It incorporates growth due to resource consumption and predation on smaller cells, death due to predation, and a flexible cell division process. We give analytic solutions at steady state for both the within-species size distributions and the relative abundances across species.

A New Phaeodarian Species Discovered from the Japan Sea Proper Water, Auloscena pleuroclada sp. nov. (Aulosphaeridae, Phaeosphaerida, Phaeodaria).

A new phaeodarian species, characterized by the presence of long developed side branches recurved proximally and distally on the surface of its radial tube, was described as Auloscena pleuroclada. This new species was only collected from the layers below the 250 m depth in the Sea of Japan. They have never been found in the shallower layers (above 250 m) of this sea or in other investigated areas. The distribution of the present new species is presumably restricted within the deep water of this area, and this species could be a specific phaeodarian adapted to the deep-sea environment.

Mechanism of phototaxis in marine zooplankton.

The simplest animal eyes are eyespots composed of two cells only: a photoreceptor and a shading pigment cell. They resemble Darwin's 'proto-eyes', considered to be the first eyes to appear in animal evolution. Eyespots cannot form images but enable the animal to sense the direction of light. They are characteristic for the zooplankton larvae of marine invertebrates and are thought to mediate larval swimming towards the light. Phototaxis of invertebrate larvae contributes to the vertical migration of marine plankton, which is thought to represent the biggest biomass transport on Earth. Yet, despite its ecological and evolutionary importance, the mechanism by which eyespots regulate phototaxis is poorly understood. Here we show how simple eyespots in marine zooplankton mediate phototactic swimming, using the marine annelid Platynereis dumerilii as a model. We find that the selective illumination of one eyespot changes the beating of adjacent cilia by direct cholinergic innervation resulting in locally reduced water flow. Computer simulations of larval swimming show that these local effects are sufficient to direct the helical swimming trajectories towards the light. The computer model also shows that axial rotation of the larval body is essential for phototaxis and that helical swimming increases the precision of navigation. These results provide, to our knowledge, the first mechanistic understanding of phototaxis in a marine zooplankton larva and show how simple eyespots regulate it. We propose that the underlying direct coupling of light sensing and ciliary locomotor control was a principal feature of the proto-eye and an important landmark in the evolution of animal eyes.

Stochastic species distributions are driven by organism size.

The strengths of environmental drivers and biotic interactions are expected to show large variability across organism groups. We tested two ideas related to the degree of ecological determinism vs. stochasticity using a large data set comprising bacterio-, phyto-, and zooplankton. We expected that (1) there are predictable, size-driven differences in the degree to which planktonic taxa respond to different drivers such as water chemistry, biotic interactions, and climatic variables; and (2) species distribution models show lowest predictive performance for the smallest taxa due to the stochastic distributions of microbes. Generalized linear models (GLMs), generalized additive models (GAMs), and generalized boosted methods (GBMs) were constructed for 84 species to model their occurrence as a function of eight predictors. Predictive performance was measured as the area under the curve (AUC) of the receiver-operating characteristic plot and true skill statistic (TSS) using independent model evaluation data. We found that the model performances were typically remarkably low for all planktonic groups. The proportion of satisfactory models (AUC > 0.7) was lowest for bacteria (11.1% of the models), followed by phyto- (24.2%) and zooplankton (38.1%). The occurrences of taxa within all planktonic groups were related to climatic variables to a certain degree, but bacteria showed the strongest associations with the climatic variables. Moreover, zooplankton occurrences were more related to biotic variables than the occurrences of smaller taxa, while phytoplankton occurrences were more related to water chemistry. We conclude that the occurrences of planktonic taxa are highly unpredictable and that stochasticity in occurrences is negatively related to the organism size perhaps due to efficient dispersal and fast population dynamics among the smallest taxa.

Ecological determinism increases with organism size.

After much debate, there is an emerging consensus that the composition of many ecological communities is determined both by species traits, as proposed by niche theory, as well as by chance events. A critical question for ecology is, therefore, which attributes of species predict the dominance of deterministic or stochastic processes. We outline two hypotheses by which organism size could determine which processes structure ecological communities, and we test these hypotheses by comparing the community structure in bromeliad phytotelmata of three groups of organisms (bacteria, zooplankton, and macroinvertebrates) that encompass a 10 000-fold gradient in body size, but live in the same habitat. Bacteria had no habitat associations, as would be expected from trait-neutral stochastic processes, but still showed exclusion among species pairs, as would be expected from niche-based processes. Macroinvertebrates had strong habitat and species associations, indicating niche-based processes. Zooplankton, with body size between bacteria and macroinvertebrates, showed intermediate habitat associations. We concluded that a key niche process, habitat filtering, strengthened with organism size, possibly because larger organisms are both less plastic in their fundamental niches and more able to be selective in dispersal. These results suggest that the relative importance of deterministic and stochastic processes may be predictable from organism size.

Coiling directions in the planktonic foraminifer Pulleniatina: A complex eco-evolutionary dynamic spanning millions of years.

Planktonic foraminifera are heterotrophic sexually reproducing marine protists with an exceptionally complete fossil record that provides unique insights into long-term patterns and processes of evolution. Populations often exhibit strong biases towards either right (dextral) or left (sinistral) shells. Deep-sea sediment cores spanning millions of years reveal that some species show large and often rapid fluctuations in their dominant coiling direction through time. This is useful for biostratigraphic correlation but further work is required to understand the population dynamical processes that drive these fluctuations. Here we address the case of coiling fluctuations in the planktonic foraminifer genus Pulleniatina based on new high-resolution counts from two recently recovered sediment cores from either side of the Indonesian through-flow in the tropical west Pacific and Indian Oceans (International Ocean Discovery Program Sites U1486 and U1483). We use single-specimen stable isotope analyses to show that dextral and sinistral shells from the same sediment samples can show significant differences in both carbon and oxygen isotopes, implying a degree of ecological separation between populations. In one case we detect a significant difference in size between dextral and sinistral specimens. We suggest that major fluctuations in coiling ratio are caused by cryptic populations replacing one another in competitive sweeps, a mode of evolution that is more often associated with asexual organisms than with the classical 'biological species concept'.

Gametogenesis in planktonic foraminifera.

Gametogenesis in Globigerinella aequilateralis and Globigerinoides sacculifer in culture is preceded by sinking of the organism and loss of its spines. Hundreds of thousands of flagellated gametes, about 5 micrometers in diameter, are produced within the parent shell and released within a period of 13 hours.

Intraspecific variation in a predator affects community structure and cascading trophic interactions.

Intraspecific phenotypic variation in ecologically important traits is widespread and important for evolutionary processes, but its effects on community and ecosystem processes are poorly understood. We use life history differences among populations of alewives, Alosa pseudoharengus, to test the effects of intraspecific phenotypic variation in a predator on pelagic zooplankton community structure and the strength of cascading trophic interactions. We focus on the effects of differences in (1) the duration of residence in fresh water (either seasonal or year-round) and (2) differences in foraging morphology, both of which may strongly influence interactions between alewives and their prey. We measured zooplankton community structure, algal biomass, and spring total phosphorus in lakes that contained landlocked, anadromous, or no alewives. Both the duration of residence and the intraspecific variation in foraging morphology strongly influenced zooplankton community structure. Lakes with landlocked alewives had small-bodied zooplankton year-round, and lakes with no alewives had large-bodied zooplankton year-round. In contrast, zooplankton communities in lakes with anadromous alewives cycled between large-bodied zooplankton in the winter and spring and small-bodied zooplankton in the summer. In summer, differences in feeding morphology of alewives caused zooplankton biomass to be lower and body size to be smaller in lakes with anadromous alewives than in lakes with landlocked alewives. Furthermore, intraspecific variation altered the strength of the trophic cascade caused by alewives. Our results demonstrate that intraspecific phenotypic variation of predators can regulate community structure and ecosystem processes by modifying the form and strength of complex trophic interactions.

Independent gradients of producer, consumer, and microbial diversity in lake plankton.

Interactions between trophic levels during food web assembly can drive positive correlations in diversity between producers, consumers, and decomposers. However, the contribution of trophic interactions relative to local environmental factors in promoting species diversity is poorly understood, with many studies only considering two trophic levels. Here we examine correlations in diversity among zooplankton, phytoplankton, and bacteria in the pelagic zone of 31 lakes in British Columbia, Canada. We sampled species diversity of zooplankton and phytoplankton through morphological identification, and bacterial genetic diversity was estimated by denaturing gradient gel electrophoresis (DGGE) of 16S rDNA polymorphisms. We looked for correlations in diversity that were independent of the abiotic environment by statistically controlling for 18 limnological variables. No significant correlations were found between the diversity of zooplankton, phytoplankton, and bacteria. In addition, the physical factors that were associated with species composition in one trophic level were independent of those that were important for another. Our results provide no support for the importance of direct feedbacks between producers, consumers, and decomposers in maintaining diversity. Zooplankton, phytoplankton, and bacterial diversity and composition are regulated independently from one another and respond to different environmental variables. These results suggest that species of lake plankton show loose trophic associations with one another due to broad diets in consumers and decomposers.

Histological approaches for high-quality imaging of zooplanktonic organisms.

The investigation of the internal organization of zooplankton communities provides important information on the plankton biology with special interest for the study of ecological processes. Zooplanktoners can play a structural function as indicators for ecosystem health or stress, but their study using histological techniques is still limited. Here we report that the internal structure of zooplanktonic organisms can be facilely observed by a histological approach that combines optimal fixation and processing with a plastic resin (glycol methacrylate) embedding, resulting in increased tissue resolution. Using copepods, organisms that can dominate zooplankton assemblages, as models, collected from a tropical ecosystem (Paraibuna river, Brazil), we showed fine histological details of their muscular, nervous and digestive systems, structure of appendages and cell features. Critical advantages of this approach are that it permits optimal preservation and adequate handling of the organisms (embedded in agar after fixation) for further histological processing and investigation. This is important because it prevents both mechanically induced artifacts and loss of these diminutive organisms during the different steps of processing. Moreover, embedding in plastic resin showed a superior imaging of copepod internal structures compared to paraffin embedding. The use of glycol methacrylate is advantageous over paraffin/paraplast embedding by avoiding heat damage, tissue retraction and allowing faster embedding procedure and better tissue resolution. The value of histological approaches in enabling high-quality imaging of the internal structure of copepods is particularly important because these organisms can be used as indicators of environmental changes.

Main predictors of periphyton species richness depend on adherence strategy and cell size.

Periphytic algae are important components of aquatic ecosystems. However, the factors driving periphyton species richness variation remain largely unexplored. Here, we used data from a subtropical floodplain (Upper Paraná River floodplain, Brazil) to quantify the influence of environmental variables (total suspended matter, temperature, conductivity, nutrient concentrations, hydrology, phytoplankton biomass, phytoplankton species richness, aquatic macrophyte species richness and zooplankton density) on overall periphytic algal species richness and on the richness of different algal groups defined by morphological traits (cell size and adherence strategy). We expected that the coefficients of determination of the models estimated for different trait-based groups would be higher than the model coefficient of determination of the entire algal community. We also expected that the relative importance of explanatory variables in predicting species richness would differ among algal groups. The coefficient of determination for the model used to predict overall periphytic algal species richness was higher than the ones obtained for models used to predict the species richness of the different groups. Thus, our first prediction was not supported. Species richness of aquatic macrophytes was the main predictor of periphyton species richness of the entire community and a significant predictor of the species richness of small mobile, large mobile and small-loosely attached algae. Abiotic variables, phytoplankton species richness, chlorophyll-a concentration, and hydrology were also significant predictors, depending on the group. These results suggest that habitat heterogeneity (as proxied by aquatic macrophytes richness) is important for maintaining periphyton species richness in floodplain environments. However, other factors played a role, suggesting that the analysis of species richness of different trait-based groups unveils relationships that were not detectable when the entire community was analysed together.

'Ancient' DNA in the resting egg bank of a microcrustacean can serve as a palaeolimnological database.

Recent work on the diapausing egg banks of zooplankton, such as Daphnia (Crustacea: Anomopoda), indicates that these eggs can remain viable for decades while, theoretically, DNA can remain intact for even longer periods (i.e. centuries or millennia). We isolated diapausing eggs of Daphnia from a 30 m long sediment core taken from a hypereutrophic, northern German lake (Belauer See), with some eggs found in dated core material as old as 4500 years. Using microsatellite markers, we analysed the genetic structure of the resting eggs dated as old as ca. 200 years, and found that, although levels of heterozygosity remained remarkably stable, significant genetic differentiation (Nei's D = 0.36; F(ST) = 0.15) between recent and 'ancient' resting eggs (including allele frequency shifts and private alleles) was detected. These shifts represent either species-level changes in this complex (i.e. species-specific characters of ephippia are not always robust), or intraspecific shifts in genetic variation, or a combination of both. This study demonstrates that the egg banks of aquatic zooplankton can serve as repositories of both genetic (intrapopulational) and ecological (interspecific) information. The use of molecular markers, such as microsatellites, on diapausing egg/seed banks may open new avenues of enquiry related to tracking the long-term genetic (and/or species) shifts that are associated with long-term environmental changes.

Lake ecosystem health assessment: indicators and methods.

A set of ecological indicators including structural, functional, and system-level aspects were proposed for a lake ecosystem health assessment, according to the structural, functional, and system-level responses of lake ecosystems to chemical stresses including acidification, eutrophication and copper, oil and pesticide contamination. The structural indicators included phytoplankton cell size and biomass, zooplankton body size and biomass, species diversity, macro- and micro-zooplankton biomass, the zooplankton phytoplankton ratio, and the macrozooplankton microzooplankton ratio. The functional indicators encompassed the algal C assimilation ratio, resource use efficiency, community production, gross production/respiration (i.e. P/R) ratio, gross production standing crop biomass (i.e. P/B) ratio, and standing crop biomass unit energy flow (i.e. B/E) ratio. The ecosystem-level indicators conisisted of ecological buffer capacities, energy, and structural energy. Based on these indicators, a direct measurement method (DMM) and an ecological modeling method (EMM) for lake ecosystem health assessment were developed. The DMM procedures were designed to: (1) identify key indicators; (2) measure directly or calculate indirectly the selected indicators; and, (3) assess ecosystem health on the basis of the indicator values. The EMM procedures were designed to: (1) determine the structure and complexity of the ecological model according to the lake's ecosystem structure; (2) establish an ecological model by designing a conceptual diagram, establishing model equations, and estimating model pararmeters; (3) compare the simulated values of important state variables and process rates with actual observations; (4) calculate ecosystem health indicators using the ecological model; and, (5) assess lake ecosystem health according to the values of the ecological indicators. The results of a case study demonstrated that both methods provided similar results which corresponded with the lake's actual trophic state.

Collection and culture techniques for gelatinous zooplankton.

Gelatinous zooplankton are the least understood of all planktonic animal groups. This is partly due to their fragility, which typically precludes the capture of intact specimens with nets or trawls. Specialized tools and techniques have been developed that allow researchers and aquarists to collect intact gelatinous animals at sea and to maintain many of these alive in the laboratory. This paper summarizes the scientific literature on the capture, collection, and culture of gelatinous zooplankton and incorporates many unpublished methods developed at the Monterey Bay Aquarium in the past 15 years.

[Spatiotemporal characteristics of zooplankton community structure and diversity in the strong temperature increment seawaters near Guohua power plant in Xiangshan Bay].

To explore the spatiotemporal characteristics of the zooplankton community structure and diversity in the strong temperature increment seawaters near a power plant, zooplankton samples were seasonally collected in duplicate by the type II net with mesh size of 160 microm at 10 stations near Guohua power plant in Xiangshan Bay in 2011. The results showed that a total of 62 species (including larvae) were identified in the samples, and the average abundance was 9 531.1 ind x m(-3). In the seawaters, zooplankton communities were mainly composed of copepods and pelagic larvae, and pelagic larvae were the dominant with an average percentage of abundance reached up to 66.6%. Analysis of similarities demonstrated that significant differences existed in zooplankton community structures among different months (P < 0.01). In these zooplankton communities, there were 18 dominant species controlling these community structures, among which the most important discriminating species were Centropages tenuiremis, Oithona similis, Oithona fallax, Acartia clausi, Clausocalanus furcatus, Paracalanus aculeatus and Paracalanus parvwus. GLM analysis indicated that diversity indices were also significantly different among different months (P < 0.01). According to the calculation results, the inflection point, where the diversity index began to decrease with increasing water temperature, fell within 20.31-22.31 degrees C. In sections, the average water temperature in the 0.2 km section (D02), away from the outfall, was 2.16: higher than that in the 2 km section. Driven by temperature, the main dominant species such as C. tenuiremis and O. similis tended to move into the 0.2 km section, while A. clause and especially large zooplankton tended to stay away from the outfall, and then gathered in the 1.2 km section. As a result, the number of species (33 species) and abundance (5 522.8 ind x m(-3)) were minimum in the section D02, while the number of species (53 species) and abundance (16 491.0 ind x m(-3)) reached the highest in the 1.2 km section. Meanwhile, diversity indices in the 0.2 km section were also obviously lower than those in other sections. Linear regression analysis showed that the diversity indices significantly decreased with increasing water temperature (P < 0.01). The zooplankton richness decreased by 12.3% when the water temperature increased by 1 degrees C.

Development of a halotolerant community in the St. Lucia Estuary (South Africa) during a hypersaline phase.

BACKGROUND: The St. Lucia Estuary, Africa's largest estuarine lake, is currently experiencing unprecedented freshwater deprivation which has resulted in a northward gradient of drought effects, with hypersaline conditions in its northern lakes. METHODOLOGY/PRINCIPAL FINDINGS: This study documents the changes that occurred in the biotic communities at False Bay from May 2010 to June 2011, in order to better understand ecosystem functioning in hypersaline habitats. Few zooplankton taxa were able to withstand the harsh environmental conditions during 2010. These were the flatworm Macrostomum sp., the harpacticoid copepod Cletocamptus confluens, the cyclopoid copepod Apocyclops cf. dengizicus and the ciliate Fabrea cf. salina. In addition to their exceptional salinity tolerance, they were involved in a remarkably simple food web. In June 2009, a bloom of an orange-pigmented cyanobacterium (Cyanothece sp.) was recorded in False Bay and persisted uninterruptedly for 18 months. Stable isotope analysis suggests that this cyanobacterium was the main prey item of F. cf. salina. This ciliate was then consumed by A. cf. dengizicus, which in turn was presumably consumed by flamingos as they flocked in the area when the copepods attained swarming densities. On the shore, cyanobacteria mats contributed to a population explosion of the staphylinid beetle Bledius pilicollis. Although zooplankton disappeared once salinities exceeded 130, many taxa are capable of producing spores or resting cysts to bridge harsh periods. The hypersaline community was disrupted by heavy summer rains in 2011, which alleviated drought conditions and resulted in a sharp increase in zooplankton stock and diversity. CONCLUSIONS/SIGNIFICANCE: Despite the current freshwater deprivation crisis, the False Bay region has shown to be resilient, harboring a unique biodiversity with species that are capable of enduring harsh environmental conditions. However, further freshwater deprivation may extend beyond the physiological thresholds of this community, as well as other unique biodiversity components which this system sustains.