Experimental evolution reveals the synergistic genomic mechanisms of adaptation to ocean warming and acidification in a marine copepod.

Metazoan adaptation to global change relies on selection of standing genetic variation. Determining the extent to which this variation exists in natural populations, particularly for responses to simultaneous stressors, is essential to make accurate predictions for persistence in future conditions. Here, we identified the genetic variation enabling the copepod Acartia tonsa to adapt to experimental ocean warming, acidification, and combined ocean warming and acidification (OWA) over 25 generations of continual selection. Replicate populations showed a consistent polygenic response to each condition, targeting an array of adaptive mechanisms including cellular homeostasis, development, and stress response. We used a genome-wide covariance approach to partition the allelic changes into three categories: selection, drift and replicate-specific selection, and laboratory adaptation responses. The majority of allele frequency change in warming (57%) and OWA (63%) was driven by shared selection pressures across replicates, but this effect was weaker under acidification alone (20%). OWA and warming shared 37% of their response to selection but OWA and acidification shared just 1%, indicating that warming is the dominant driver of selection in OWA. Despite the dominance of warming, the interaction with acidification was still critical as the OWA selection response was highly synergistic with 47% of the allelic selection response unique from either individual treatment. These results disentangle how genomic targets of selection differ between single and multiple stressors and demonstrate the complexity that nonadditive multiple stressors will contribute to predictions of adaptation to complex environmental shifts caused by global change.

The role of fish predators and their foraging traits in shaping zooplankton community structure.

Differentiation of foraging traits among predator populations may help explain observed variation in the structure of prey communities. However, few studies have investigated the phenotypic effects of predators on their prey in natural communities. Here, we use a comparative analysis of 78 Greenlandic lakes to examine how foraging trait variation among threespine stickleback populations can help explain variation in zooplankton community composition among lakes. We find that landscape-scale variation in zooplankton composition was jointly explained by lake properties, such as size and water chemistry, and the presence and absence of both stickleback and arctic char. Additional variation in zooplankton community structure can be explained by stickleback jaw protrusion, a trait with known utility for foraging on zooplankton, but only in lakes where stickleback co-occur with arctic char. Overall, our results illustrate how trait variation of predators, alongside other ecosystem properties, can influence the composition of prey communities in nature.

Regional and fine-scale local adaptation in salinity tolerance in Daphnia inhabiting contrasting clusters of inland saline waters.

Understanding the spatial scales at which organisms can adapt to strong natural and human-induced environmental gradients is important. Salinization is a key threat to biodiversity, ecosystem functioning and the provision of ecosystem services of freshwater systems. Clusters of naturally saline habitats represent ideal test cases to study the extent and scale of local adaptation to salinization. We studied local adaptation of the water flea Daphnia magna, a key component of pond food webs, to salinity in two contrasting landscapes-a dense cluster of sodic bomb crater ponds and a larger-scale cluster of soda pans. We show regional differentiation in salinity tolerance reflecting the higher salinity levels of soda pans versus bomb crater ponds. We found local adaptation to differences in salinity levels at the scale of tens of metres among bomb crater pond populations but not among geographically more distant soda pan populations. More saline bomb crater ponds showed an upward shift of the minimum salt tolerance observed across clones and a consequent gradual loss of less tolerant clones in a nested pattern. Our results show evolutionary adaptation to salinity gradients at different spatial scales, including fine-tuned local adaptation in neighbouring habitat patches in a natural landscape.

Comparative analysis of the molecular starvation response of Southern Ocean copepods.

Large lipid-storing copepods dominate mesozooplankton biomass in the polar oceans and form a critical link between primary production and higher trophic levels. The ecological success of these species depends on their ability to survive periods of food deprivation in a highly seasonal environment, but the molecular changes that mediate starvation tolerance in these taxa are unknown. We conducted starvation experiments for two dominant Southern Ocean copepods, Calanoides acutus and Calanus propinquus, allowing us to compare the molecular starvation response between species. These species differ in life history, diet and metabolic traits, and expressed overlapping but distinct transcriptomic responses to starvation. Most starvation-response genes were species-specific, but we identified a conserved core set of starvation-response genes related to RNA and protein metabolism. We used phylotranscriptomics to place these results in the context of copepod evolution and found that starvation-response genes are under strong purifying selection at the sequence level and stabilizing selection at the expression level, consistent with their role in mediating essential biological functions. Selection on starvation-response genes was especially strong in our focal lipid-storing lineage relative to other copepod taxa, underscoring the significance of starvation tolerance for these species. We also found that certain key lipid enzymes (elongases and desaturases) have experienced diversification and positive selection in lipid-storing lineages, reflecting the unique lipid storage needs of these animals. Our results shed light on the molecular adaptations of high-latitude zooplankton to variable food conditions and suggest that starvation-response genes are under particularly strong sequence and expression constraints.

Revealing the profound influence of diapause on gene expression: Insights from the annual transcriptome of the copepod Calanus finmarchicus.

Annual rhythms are observed in living organisms with numerous ecological implications. In the zooplanktonic copepod Calanus finmarchicus, such rhythms are crucial regarding its phenology, body lipid accumulation, and global carbon storage. Climate change drives annual biological rhythms out of phase with the prevailing environmental conditions with yet unknown but potentially catastrophic consequences. However, the molecular dynamics underlying phenology are still poorly described. In a rhythmic analysis of C. finmarchicus annual gene expression, results reveal that more than 90% of the transcriptome shows significant annual rhythms, with abrupt and dramatic upheaval between the active and diapause life cycle states. This work explores the implication of the circadian clock in the annual timing, which may control epigenetic mechanisms to profoundly modulate gene expression in response to calendar time. Results also suggest an increased light sensitivity during diapause that would ensure the photoperiodic entrainment of the endogenous annual clock.

Global mesozooplankton communities show lower connectivity in deep oceanic layers.

Mesozooplankton is a key component of the ocean, regulating global processes such as the carbon pump, and ensuring energy transfer from lower to higher trophic levels. Yet, knowledge on mesozooplankton diversity, distribution and connectivity at global scale is still fragmented. To fill this gap, we applied DNA metabarcoding to mesozooplankton samples collected during the Malaspina-2010 circumnavigation expedition across the Atlantic, Indian and Pacific oceans from the surface to bathypelagic depths. We highlight the still scarce knowledge on global mesozooplankton diversity and identify the Indian Ocean and the deep sea as the oceanic regions with the highest proportion of hidden diversity. We report no consistent alpha-diversity patterns for mesozooplankton at a global scale, neither across vertical nor horizontal gradients. However, beta-diversity analysis suggests horizontal and vertical structuring of mesozooplankton communities mostly attributed to turnover and reveals an increase in mesozooplankton beta-diversity with depth, indicating reduced connectivity at deeper layers. Additionally, we identify a water mass type-mediated structuring of mesozooplankton bathypelagic communities instead of an oceanic basin-mediated as observed at upper layers. This suggests limited dispersal at deep ocean layers, most likely due to weaker currents and lower mixing of water mass types, thus reinforcing the importance of oceanic currents and barriers to dispersal in shaping global plankton communities.

The appendicularian Oikopleura dioica can enhance carbon export in a high CO2 ocean.

Gelatinous zooplankton are increasingly recognized to play a key role in the ocean's biological carbon pump. Appendicularians, a class of pelagic tunicates, are among the most abundant gelatinous plankton in the ocean, but it is an open question how their contribution to carbon export might change in the future. Here, we conducted an experiment with large volume in situ mesocosms (~55-60 m3 and 21 m depth) to investigate how ocean acidification (OA) extreme events affect food web structure and carbon export in a natural plankton community, particularly focusing on the keystone species Oikopleura dioica, a globally abundant appendicularian. We found a profound influence of O. dioica on vertical carbon fluxes, particularly during a short but intense bloom period in the high CO2 treatment, during which carbon export was 42%-64% higher than under ambient conditions. This elevated flux was mostly driven by an almost twofold increase in O. dioica biomass under high CO2 . This rapid population increase was linked to enhanced fecundity (+20%) that likely resulted from physiological benefits of low pH conditions. The resulting competitive advantage of O. dioica resulted in enhanced grazing on phytoplankton and transfer of this consumed biomass into sinking particles. Using a simple carbon flux model for O. dioica, we estimate that high CO2 doubled the carbon flux of discarded mucous houses and fecal pellets, accounting for up to 39% of total carbon export from the ecosystem during the bloom. Considering the wide geographic distribution of O. dioica, our findings suggest that appendicularians may become an increasingly important vector of carbon export with ongoing OA.

Declining calcium concentration drives shifts toward smaller and less nutritious zooplankton in northern lakes.

Zooplankton community composition of northern lakes is changing due to the interactive effects of climate change and recovery from acidification, yet limited data are available to assess these changes combined. Here, we built a database using archives of temperature, water chemistry and zooplankton data from 60 Scandinavian lakes that represent broad spatial and temporal gradients in key parameters: temperature, calcium (Ca), total phosphorus (TP), total organic carbon (TOC), and pH. Using machine learning techniques, we found that Ca was the most important determinant of the relative abundance of all zooplankton groups studied, while pH was second, and TOC third in importance. Further, we found that Ca is declining in almost all lakes, and we detected a critical Ca threshold in lake water of 1.3 mg L-1 , below which the relative abundance of zooplankton shifts toward dominance of Holopedium gibberum and small cladocerans at the expense of Daphnia and copepods. Our findings suggest that low Ca concentrations may shape zooplankton communities, and that current trajectories of Ca decline could promote widespread changes in pelagic food webs as zooplankton are important trophic links from phytoplankton to fish and different zooplankton species play different roles in this context.

Dynamics of Gut Bacteria Across Different Zooplankton Genera in the Baltic Sea.

In aquatic ecosystems, zooplankton-associated bacteria potentially have a great impact on the structure of ecosystems and trophic networks by providing various metabolic pathways and altering the ecological niche of host species. To understand the composition and drivers of zooplankton gut microbiota, we investigated the associated microbial communities of four zooplankton genera from different seasons in the Baltic Sea using the 16S rRNA gene. Among the 143 ASVs (amplified sequence variants) observed belonging to heterotrophic bacteria, 28 ASVs were shared across all zooplankton hosts over the season, and these shared core ASVs represented more than 25% and up to 60% of relative abundance in zooplankton hosts but were present at low relative abundance in the filtered water. Zooplankton host identity had stronger effects on bacterial composition than seasonal variation, with the composition of gut bacterial communities showing host-specific clustering patterns. Although bacterial compositions and dominating core bacteria were different between zooplankton hosts, higher gut bacteria diversity and more bacteria contributing to the temporal variation were found in Temora and Pseudocalanus, compared to Acartia and Synchaeta. Diet diatom and filamentous cyanobacteria negatively correlated with gut bacteria diversity, but the difference in diet composition did not explain the dissimilarity of gut bacteria composition, suggesting a general effect of diet on the inner conditions in the zooplankton gut. Synchaeta maintained high stability of gut bacterial communities with unexpectedly low bacteria-bacteria interactions as compared to the copepods, indicating host-specific regulation traits. Our results suggest that the patterns of gut bacteria dynamics are host-specific and the variability of gut bacteria is not only related to host taxonomy but also related to host behavior and life history traits.

Silica Nanoparticle Size Determines the Mechanisms Underlying the Inhibition of Iron Oxide Nanoparticle Uptake by Daphnia magna.

Aquatic environments are complicated systems that contain different types of nanoparticles (NPs). Nevertheless, recent studies of NP toxicity, and especially those that have focused on bioaccumulation have mostly investigated only a single type of NPs. Assessments of the environmental risks of NPs that do not consider co-exposure regimes may lead to inaccurate conclusions and ineffective environmental regulation. Thus, the present study examined the effects of differently sized silica NPs (SiO2 NPs) on the uptake of iron oxide NPs (Fe2O3 NPs) by the zooplankton Daphnia magna. Both SiO2 NPs and Fe2O3 NPs were well dispersed in the experimental medium without significant heteroaggregation. Although all three sizes of SiO2 NPs inhibited the uptake of Fe2O3 NPs, the underlying mechanisms differed. SiO2 NPs smaller than the average mesh size (∼200 nm) of the filtering apparatus of D. magna reduced the accumulation of Fe2O3 NPs through uptake competition, whereas larger SiO2 NPs inhibited the uptake of Fe2O3 NPs mainly by reducing the water filtration rate of the daphnids. Overall, in evaluations of the risks of NPs in the natural environment, the different mechanisms underlying the effects of NPs of different sizes on the uptake of dissimilar NPs should be considered.

Reducing Gut Dissolution of Zinc Oxide Nanoparticles by Secondary Microplastics with Consequent Impacts on Barnacle Larvae.

The environmental impact of sunscreen is a growing concern, yet the combined effects of its components on marine animals are poorly understood. In this study, we investigated the combined effects of sunscreen-extracted zinc oxide nanoparticles (nZnO) and microplastics (MPs) on the development of barnacle larvae, focusing on the different roles played by primary microplastics (PMPs) and secondary microplastics (SMPs) generated through the phototransformation of PMPs. Our findings revealed that a lower concentration of nZnO (50 µg/L) enhanced molting and eye development in barnacle larvae, while a higher concentration (500 µg/L) inhibited larval growth. Co-exposure to PMPs had no significant effect on larval development, whereas SMPs mitigated the impact of nZnO by restricting the in vivo transformation to ionic Zn. Accumulated SMPs reduced gut dissolution of nZnO by up to 40%, lowering gut acidity by 85% and buffering the in vivo dissolution of nZnO. We further identified a rough-surfaced Si-5 fragment in SMPs that damaged larval guts, resulting in decreased acidity. Another Si-32 resisted phototransformation and had no discernible effects. Our study presented compelling evidence of the impacts of SMPs on the bioeffect of nZnO, highlighting the complex interactions between sunscreen components and their combined effects on marine organisms.

Concordance among lacustrine communities are low and inconsistent in the conterminous United States.

Concordance occurs when two or more biological groups are correlated to each other. Examining the degree of concordance between communities has been a central goal in ecology. However, few studies have assessed the levels of community concordance at large spatial scales. We used a dataset obtained by the National Lakes Assessment (United States Environmental Protection Agency) to evaluate whether (i) the levels of concordance between aquatic communities were higher at the continental scale than within individual ecoregions of the United States and (ii) whether the levels of concordance between phytoplankton and zooplankton were higher than those between the plankton and macroinvertebrates communities. At the continental scale, the levels of concordance between different pairs of aquatic communities were low and did not exceed those within the ecoregions. Furthermore, levels of concordance varied considerably among ecoregions. Our results suggest that interactions between aquatic communities likely determined concordance patterns; however, the expectation of higher levels of concordance between the phytoplankton and zooplankton communities than between them and the macroinvertebrates community was not supported. The consistently low and variable levels of concordance suggest that using surrogate groups is not recommendable for monitoring lakes in the United States, both at the continental and regional scales. According to our results, the prospect of using the surrogacy approach was low even for aquatic communities that are highly interactive or driven by similar environmental factors.

Compound-specific stable isotope analyses of fatty acids indicate feeding zones of zooplankton across the water column of a subalpine lake.

Spatial and temporal zooplankton feeding dynamics across the water column of lakes are key for understanding site-specific acquisition of diet sources. During this 6-week lake study, we examined stable carbon (δ13C) and nitrogen (δ15N) isotopes and conducted compound-specific fatty acid (FA) stable isotope analysis (CSIA) of edible seston in the epi-, meta-, and hypolimnion, and zooplankton of Lake Lunz, Austria. We predicted that CSIA of essential FA can discern the foraging grounds of zooplankton more accurately than the commonly used bulk stable isotopes. The δ13C and δ15N values of seston from different lake strata were similar, whereas a dual CSIA approach using stable carbon and hydrogen isotopes of FA (δ13CFA and δ2HFA) provided sufficient isotopic difference in essential FA to discern different lake strata-specific diet sources throughout the study period. We present a CSIA model that suggests strata-specific foraging grounds for different zooplankton groups, indicating higher preference of cladocerans for feeding on epilimnetic diet sources, while calanoid copepods retained more hypolimnetic resources. The CSIA approach thus yields strata-specific information on foraging strategies of different zooplankton taxa and provides more details on the spatial and temporal trophodynamics of planktonic food webs than commonly used bulk stable isotopes.

A circumpolar study of surface zooplankton biodiversity of the Southern Ocean based on eDNA metabarcoding.

Under pressure from climate change and fishing, the Southern Ocean ecosystems have been changing. Zooplankton plays a vital role in the food web of the Southern Ocean and is crucial for maintaining ecosystem stability. Investigating the circumpolar-scale species composition and biodiversity of zooplankton is crucial for ensuring ecosystem-based conservation and management of the Southern Ocean in a changing climate. Here, we utilized eDNA metabarcoding to assess the biodiversity of zooplankton in the surface seawater surrounding the Antarctica based on samples collected during two expeditions spanning from 2021 to 2022. The main purpose of this paper is to provide more baseline information about circumpolar zooplankton biodiversity based on the emerging eDNA metabarcoding tool. This comprehensive approach led to the identification of over 300 distinct zooplankton species, forming a diverse community dominated by Jellyfish, Mollusca and Polychaete. Surprisingly, common dominant taxonomic groups such as krill and copepods in the Southern Ocean did not show high relative abundance (reads) in surface seawater. The results of redundancy analysis (RDA) and correlation analysis highlighted that water temperature and chlorophyll a had the most significant impact on the reads and diversity of zooplankton. Notably, the influence of water temperature on zooplankton seemed to be primarily indirect, potentially mediated by its effects on primary productivity. Increasing in primary production might lead to lower zooplankton biodiversity in the Southern Ocean in future. This research underscores the effectiveness of eDNA metabarcoding as a valuable tool for monitoring zooplankton diversity in open seas. Given the ongoing changes in temperature, sea ice extent and their impact on primary production, our findings lay a crucial foundation for using eDNA techniques to establish long-term biodiversity monitoring programs across extensive marine ecosystems in the future.

Zooplankton-based adverse outcome pathways: A tool for assessing endocrine disrupting compounds in aquatic environments.

Endocrine disrupting compounds (EDCs) pose a significant ecological risk, particularly in aquatic ecosystems. EDCs have become a focal point in ecotoxicology, and their identification and regulation have become a priority. Zooplankton have gained global recognition as bioindicators, benefiting from rigorous standardization and regulatory validation processes. This review aims to provide a comprehensive summary of zooplankton-based adverse outcome pathways (AOPs) with a focus on EDCs as toxicants and the utilisation of freshwater zooplankton as bioindicators in ecotoxicological assessments. This review presents case studies in which zooplankton have been used in the development of AOPs, emphasizing the identification of molecular initiating events (MIEs) and key events (KEs) specific to zooplankton exposed to EDCs. Zooplankton-based AOPs may become an important resource for understanding the intricate processes by which EDCs impair the endocrine system. Furthermore, the data sources, experimental approaches, advantages, and challenges associated with zooplankton-based AOPs are discussed. Zooplankton-based AOPs framework can provide vital tools for consolidating toxicological knowledge into a structured toxicity pathway of EDCs, offering a transformative platform for facilitating enhanced risk assessment and chemical regulation.

Phytoplankton-chytrid-zooplankton dynamics via a reaction-diffusion-advection mycoloop model.

Mycoloop is an important aquatic food web composed of phytoplankton, chytrids (one dominant group of parasites in aquatic ecosystems), and zooplankton. Chytrids infect phytoplankton and fragment them for easy consumption by zooplankton. The free-living chytrid zoospores are also a food resource for zooplankton. A dynamic reaction-diffusion-advection mycoloop model is proposed to describe the Phytoplankton-chytrid-zooplankton interactions in a poorly mixed aquatic environment. We analyze the dynamics of the mycoloop model to obtain dissipativity, steady state solutions, and persistence. We rigorously derive several critical thresholds for phytoplankton or zooplankton invasion and chytrid transmission among phytoplankton. Numerical diagrams show that varying ecological factors affect the formation and breakup of the mycoloop, and zooplankton can inhibit chytrid transmission among phytoplankton. Furthermore, this study suggests that mycoloop may either control or cause phytoplankton blooms.

Cloud shadows drive vertical migrations of deep-dwelling marine life.

Many zooplankton and fishes vertically migrate on a diel cycle to avoid predation, moving from their daytime residence in darker, deep waters to prey-rich surface waters to feed at dusk and returning to depth before dawn. Vertical migrations also occur in response to other processes that modify local light intensity, such as storms, eclipses, and full moons. We observed rapid, high-frequency migrations, spanning up to 60 m, of a diel vertically migrating acoustic scattering layer with a daytime depth of 300 m in the subpolar Northeastern Pacific Ocean. The depth of the layer was significantly correlated, with an ∼5-min lag, to cloud-driven variability in surface photosynthetically available radiation. A model of isolume-following swimming behavior reproduces the observed layer depth and suggests that the high-frequency migration is a phototactic response to absolute light level. Overall, the cumulative distance traveled per day in response to clouds was at least 36% of the round-trip diel migration distance. This previously undescribed phenomenon has implications for the metabolic requirements of migrating animals while at depth and highlights the powerful evolutionary adaptation for visual predator avoidance.

Invasion genomics uncover contrasting scenarios of genetic diversity in a widespread marine invader.

Invasion rates have increased in the past 100 y irrespective of international conventions. What characterizes a successful invasion event? And how does genetic diversity translate into invasion success? Employing a whole-genome perspective using one of the most successful marine invasive species world-wide as a model, we resolve temporal invasion dynamics during independent invasion events in Eurasia. We reveal complex regionally independent invasion histories including cases of recurrent translocations, time-limited translocations, and stepping-stone range expansions with severe bottlenecks within the same species. Irrespective of these different invasion dynamics, which lead to contrasting patterns of genetic diversity, all nonindigenous populations are similarly successful. This illustrates that genetic diversity, per se, is not necessarily the driving force behind invasion success. Other factors such as propagule pressure and repeated introductions are an important contribution to facilitate successful invasions. This calls into question the dominant paradigm of the genetic paradox of invasions, i.e., the successful establishment of nonindigenous populations with low levels of genetic diversity.

Effects of dilution and pretreatment on nutrient removal and biomass production of Chlorella vulgaris in kitchen wastewater.

This research investigated the effect of kitchen wastewater (KWW) concentrations and pretreatment methods on Chlorella vulgaris biomass production, lipid content and nutrient removal. This study was divided into two separate experiments. The first experiment determined the appropriate dilution rate of KWW for the growth of microalgae, sterilized KWW was varied between 25%, 50%, 75%, and 100%(v/v). The result indicated that 50%(v/v) showed the highest nutrient removal by 90.23%, 85.87%, and 80.64% of sCOD, TKN, and TP, respectively. The highest biomass and lipid content were obtained with 50%(v/v) (1.447 g/L, 37.9%). The second experiment was to find an effective physical pretreatment method, which separated the biotic contaminant, non-sterilized KWW was diluted 50%(v/v) and filtered with different mesh size filters (150 µm, 50 µm, and 30 µm) compared with sterilized KWW as a control sample. The result indicated that pretreatment with 50 µm filtration was found highest nutrient removal by 90.51%, 84.74%, and 77.50% of sCOD, TKN, and TP, respectively. The highest biomass and lipid content were obtained with 50 µm filtration (1.496 g/L, 39.4%). Our results support the hypothesis that the optimal dilution and proper filtration of KWW helps create more favorable environment for microalgal growth.

The application of microalgae in actual wastewater treatment was the improper amount of nutrients and the presence of biotic contaminant in the non-sterilized wastewater, which is inhibit the microalgae growth. Hence, it is necessary to develop the technique for controlling biotic contamination and appropriately diluting wastewater to enable full-scale microalgae cultivation in the future.

We need to talk about the role of zooplankton in marine food webs.

Zooplankton are the key intermediary between primary production and the fish community and a cornerstone of marine food webs, but they are often poorly represented in models that tend to focus on fish, charismatic top predators, or ocean biogeochemistry. In this study, we use an intermediate complexity end-to-end food web model of the North Sea with explicit two-way coupling of zooplankton to phytoplankton and higher trophic levels to ask whether this matters. We vary the metabolic rate of omnivorous zooplankton (OZ) as a proxy for uncertainties in our understanding and modeling of zooplankton form and function, and moving beyond previous studies we look at the impacts on the food web in concert with climate warming and fishing. We consider impacts on food web state and time to recover the relevant unfished state after fishing ceases. We also consider potential impacts on pelagic and demersal fishing fleets if we assume that they are constrained by the requirement to allow recovery to an unfished state within a certain period of time as a way of ensuring consistency with Good Environmental Status as required by EU and UK legislation. We find that all three aspects considered are highly sensitive to changes in the treatment of zooplankton, with impacts being larger than for warming of 2 or 4°C across most food web functional groups, particularly for apex predators. We call for a programme of research aimed at improving our understanding of zooplankton ecology and its relationship to the wider food web, and we recommend that improved representations of zooplankton are incorporated in future modeling studies as a priority.