The aim of the study was to measure copepod reproduction, mortality and sex ratio in the field before, during and after a cyanobacteria bloom during the summer in the western Gulf of Finland. Environment and zooplankton samples were collected every fortnight, and the copepod Acartia spp. was incubated in the laboratory for reproductive output, i.e. egg production and egg hatching success. Other responses monitored were female: male ratio, mortality and body condition. In addition, molecular analyses of the nodularin-producing cyanobacterium Nodularia in Acartia gut contents (GCs) were assessed. Egg production and body condition decreased with increasing Nodularia GCs. During the bloom, hatching decreased as a response to Nodularia in the copepod gut. Although not related to cyanobacteria variables, male mortality was higher than female mortality, resulting in a female-biased sex ratio over most of the summer. The study demonstrates that Acartia reproductive output is constrained by cyanobacteria blooms in the Baltic Sea, and more generally that copepod population dynamics may be negatively affected by such blooms. This is especially significant considering that toxin-producing blooms are predicted to increase due to warming.
Aquatic ecosystems experience large natural variation in elemental composition of carbon (C), nitrogen (N) and phosphorus (P), which is further enhanced by human activities. Primary producers typically reflect the nutrient ratios of their resource, whose stoichiometric composition can vary widely in conformity to environmental conditions. In contrast, C to nutrient ratios in consumers are largely constrained within a narrow range, termed homeostasis. In comparison to crustacean zooplankton, less is known about the ability of protozoan grazers and rotifer species to maintain stoichiometric balance. In this study, we used laboratory experiments with a primary producer (Nannochloropsis sp.), three different species of protozoan grazers and one mesozooplankton species: two heterotrophic dinoflagellates (Gyrodinium dominans and Oxyrrhis marina), a ciliate (Euplotes sp.) and a rotifer (Brachionus plicatilis) to test the stoichiometric response to five nutrient treatments. We showed that the dependency of zooplankton C: N: P ratios on C: nutrient ratios of their food source varies among species. Similar to the photoautotroph, the two heterotrophic dinoflagellates weakly regulated their internal stoichiometry. In contrast, the strength of stoichiometric regulation increased to strict homeostasis in both the ciliate and the rotifer, similar to crustacean zooplankton. Our study further shows that ciliate and rotifer growth can be constrained by imbalanced resource supply. It also indicates that these key primary consumers have the potential to trophically upgrade poor stoichiometric autotrophic food quality for higher trophic levels.
The size structure of a zooplankton community is frequently used as a trait reflecting functional properties, including biochemical composition. Therefore, a shift in zooplankton body size can reflect shifts in the nutritional quality of zooplankton. In dominant Baltic copepods and cladocerans, neutral to polar lipid ratio (NL/PL ratio), a proxy for the mass-normalized lipid storage, was determined and related to individual body weight. A significant relationship between the NL/PL ratio and body weight was found; the latter was the strongest and the most significant predictor of the lipid storage capacity across different species and developmental stages. These findings provide support for using mean body weight in zooplankton community as a proxy for lipid storage capacity of zooplankton prey and justify applicability of zooplankton mean size as an indicator of nutritional conditions for Baltic zooplanktivores.
The ecological role of nodularin in cyanobacterium Nodularia spumigena is still largely unknown, as are the conditions that promote toxin production. We report a modulating effect of mesozooplankton grazing on cellular nodularin content in N. spumigena expressed as a decrease in cell-bound toxin concentration in the presence of copepods compared with the cyanobacterium in similar assemblages without copepods. In our experiments, N. spumigena was incubated in an ambient plankton (< 90 mu m) assemblage (Expt I) or in 0.2-mu m filtered seawater (Expt II), with and without the copepod Eurytemora affinis. Following similar to 28-h incubation, we measured the changes in N. spumigena abundance and nodularin concentration, frequency of Nodularia DNA occurrence in copepods as a proxy for grazing pressure on the cyanobacterium and individual RNA content in E. affinis as a proxy for copepod growth response. In all copepod-free treatments, intracellular nodularin concentrations were up to four times higher than in the treatments containing copepods. In Experiment I, the copepods also has a positive effect on the cyanobacterium growth, presumably due to a selective removal of more edible algal species and thus decreased competition for nutrients. Nodularia DNA was detected with high frequencies, 18-80%, increase in treatments with no alternative food or high copepod densities. Simultaneously, no noxious effects of N. spumigena on the copepods were detected as indicated by higher RNA content in copepods exposed to N. spumigena with or without ambient plankton organisms compared with started controls. These findings stress the need to understand the importance of intra-specific interactions for nodularin production in relation to population dynamics of N. spumigena.
Plankton succession was studied in a hyper-eutrophic stratified estuary, Mariager Fjord, Denmark. Above the pycnocline (15 m) pH increased from 8.5 to 9.2 and the oxygen increased to super saturation after 5 d of sunny weather due to high primary production. The protistan grazers were dominated by heterotrophic dinoflagellates and mixotrophic and heterotrophic ciliates. Metazooplankton was dominated by meroplankton, rotifers and the copepod, Acartia tonsa, all with a relatively low biomass. Cirriped nauplii occupied the upper strata while polychaete larvae populated the whole water column. Bivalve larvae occurred occasionally above the pycnocline even at very high pH. In pH challenge experiments, the mixotrophic ciliate Mesodinium rubrum was the least pH tolerant species, followed by Strombidium spp., which did not cope well with seawater pH > 8.5. Some heterotrophic dinoflagellates were more tolerant with net growth at pH > 9. The predominant rotifer Synchaeta sp. tolerated up to pH 9.5 and the copepod survived pH 10 but stopped producing eggs at pH 9.5 with unaffected egg hatching success. The polychaete and cirriped larvae tolerated pH 9.5, but bivalve larvae showed decreased survival already at pH 8.5. In situ distribution patterns and pH challenge experiments suggest that pH indeed contribute to structuring zooplankton distribution.
Biomarkers are very useful for in situ assessments of zooplankton growth. In particular, RNA-based methods have been developed to estimate egg production in copepods. However, RNA-growth relationships can potentially depend on a variety of factors, such as egg quality. This study shows that in Acartia tonsa, female RNA-content reflects egg production irrespective of egg viability, implying that this growth proxy is not applicable for recruitment studies if the proportion of viable eggs fluctuates widely.
In marine food webs, copepods are the major producers of a carotenoid pigment astaxanthin, which is an important antioxidant. The availability of astaxanthin for higher trophic levels can be affected by changes in phytoplankton stocks and copepod feeding; however, the functional relationship between food availability and astaxanthin production is poorly understood. We hypothesized that with a given food type and quality, astaxanthin content in copepods is positively related to feeding and egg production rates. The hypothesis was tested by measuring astaxanthin accumulation in concert with ingestion and egg production rates in the copepod Acartia bifilosa exposed to different algal concentrations (Tetraselmis suecica; 0 to 1200 μg C L−1). Egg production and ingestion rates increased with increasing food availability and reached a plateau at ≥400–600 μg C L−1. In contrast, increasing accumulation of astaxanthin with increasing food availability was observed only at concentrations ≤150 μg C L−1. Contrary to our hypothesis, at 600–1200 μg C L−1 copepods had maximal ingestion and egg production rates, but low astaxanthin contents. It is suggested that this low accumulation of astaxanthin at high food concentrations results from a food-dependant decrease in assimilation efficiency. These findings are important for the understanding of astaxanthin dynamics within marine food webs, where increases in phytoplankton biomass may translate to a trade-off between zooplankton quantity and its nutritional quality for zooplanktivores.
We studied diel vertical migration (DVM) of the six copepodite stages of two of the most abundant crustacean zooplankton in the Baltic Sea, the calanoid copepods Eurytemora affinis and Acartia spp. The study was conducted monthly from May through October in a bay in the northwestern Baltic proper. Fish biomass, phytoplankton abundance and temperature were obtained in conjunction with the zooplankton sampling. Both copepod species performed DVM. With the exception of females, all E. affinis copepodite stages performed migrations of over 10 m with only a slight increase with the copepodite stage. Adult female E. affinis remained at depth with only slight upward movement at night. In Acartia spp., DVM amplitude increased with stage and size, suggesting an ontogenetic shift in behaviour; although they had a less pronounced DVM than E. affinis. Although DVM amplitude increased with size, indicative of visual predation, fish biomass did not correlate with the amplitude of DVM. However, fish were present throughout the study period. We surmise that these ontogenetic shifts in behaviour are due to size increase and therefore visibility to predators and that the difference in DVM between the species may well be a result of physiological differences and reproductive strategy.
In the Baltic Sea, the predatory cladoceran Cercopagis pengoi is a non-indigenous species that has potential to compete for mesozooplankton with pelagic zooplanktivorous fish. To understand the extent of diet overlap with these fishes in a coastal area of the northern Baltic proper, we studied the feeding of C. pengoi using stable C-13 and N-15 isotope signatures of the predator and possible prey. Feasible combinations of sources were estimated in two ways: (i) with the IsoSource mixing model, and (ii) temporal-tracking analysis. Further, contribution of different prey was related to ambient zooplankton composition to gauge selectivity. The modelling results indicate that C. pengoi is an opportunistic generalist predator with a positive selection towards older copepodites (CIVVI) of Acartia spp. and Eurytemora affinis, which also have the greatest contribution to its diet. Positive selection towards podonid Cladocera is also likely. In contrast, evidence for extensive feeding on microzooplankton was inconclusive, and bosminids were not found to be an important prey in the zooplankton assemblages studied. As the derived diet of C. pengoi overlaps greatly with that of zooplanktivorous fish, food competition between these zooplanktivores is possible.
Calanoid copepods of the genus Pseudocalanus are key species in temperate-boreal marine pelagic ecosystems. Pseudocalanus species are difficult to distinguish morphologically and there is uncertainty regarding the species present in the Baltic Sea. In this study, we investigated the species composition of Pseudocalanus in the Baltic proper and the Gulf of Finland using a restriction fragment length polymorphism approach. Screening of 888 individuals from 13 different stations, sampled during various seasons on a total of 22 different occasions stretching from November 2006 until July 2008, confirmed that P. acuspes is the only Pseudocalanus species normally present in the Baltic Sea. Mitochondrial diversity is exceptionally low in Baltic Sea populations of P. acuspes, as only two cytochrome oxidase I haplotypes were observed in samples ranging from the Gulf of Finland in the north to the Arkona Basin in the south (83 individuals). This unusually low level of genetic diversity indicates that planktonic organisms may experience loss of genetic diversity in marginal Baltic Sea populations, despite large population sizes. Low genetic diversity may negatively impact the species' capacity for adaptation to environmental change.
Since its first reported appearance in the Baltic Sea in 2007, there has been a little research on the role of the Arctic ctenophore Mertensia ovum in this ecosystem. We provide results from the first feeding experiments of M. ovum from the northern Baltic Sea. Experiments were conducted with various prey types; picocyanobacteria Synechococcus bacillaris, ciliates Mesodinium rubrum, nauplii of mixed copepod species and copepodites of Eurytemora affinis. Molecular gut content analyses were also used to measure in situ feeding of M. ovum on the picocyanobacteria. The observed clearance rates on M. rubrum (< 9.0 mL predator(-1) h(-1)), and S. bacillaris (<7.5 mL predator(-1) h(-1)) were lower than those reported for similar-sized ctenophore species feeding on similar prey. Similarly, clearance rates of M. ovum on copepodites and copepod nauplii were close to zero, implying significantly lower predation on crustacean prey compared with other ctenophores. Overall, M. ovum predation rates were relatively low with a maximum daily consumption of 0.95 mu g C ind.(-1) day(-1) (similar to 15.8% of estimated predator carbon content). In addition, we examined the vertical distribution of M. ovum in relation to that of micro- and mesozooplankton and found greater overlap with potential microplankton prey than with mesozooplankton. Taken together, these results imply that in the Baltic Sea, M. ovum feed mainly on bacterio-and microplankton, thus potentially contributing to the coupling between the microbial loop and higher consumers in the pelagic food web.
The mysid shrimp Praunus flexuosus is common in littoral habitats in the Baltic Sea and other marine areas, but its bioenergetic characteristics have not been studied. We present the first model of its routine respiration rate as a function of size and a natural temperature range. The model explained 87% of the variance in respiration, indicating that it could be useful in a larger modeling framework. Specific respiration rates and temperature dependence were consistent with previous reports for this and other littoral mysids at low-to-moderate temperatures. Respiration at higher temperatures was lower, indicating that previous reports may have been biased by residual SDA (specific dynamic action) effects. Increased respiration due to SDA was detectable over a longer period than previously reported, ∼30 h.
Mysids are known for benthic-pelagic diel vertical migration (DVM), where the population is benthic by day and pelagic by night. However, historical and recent observations in members of the Mysis relicta complex suggests populations exhibit partial DVM, with some remaining benthic at night. We used pelagic net and benthic sled tows to assess diel habitat use by Mysis diluviana at two stations (60 and 100 m deep) in Lake Champlain, USA, during June-November 2015. At both stations, mysids were on the bottom both day and night, but the extent of pelagic habitat use by Mysis varied by site depth. At 60-m, pelagic densities were an order of magnitude lower during the day compared to at night, indicative of benthic-pelagic DVM. Contrary to expectations, we found no diel difference between pelagic and benthic sled density estimates at 100-m, suggesting an equal number of Mysis are benthic day and night, and an equal number are pelagic-day and night at deeper sites. Mean body length of benthic-caught mysids was greater than pelagic-caught individuals, a pattern that was evident both day and night at 100-m. Our findings indicate Mysis partial DVM is common across seasons and influenced by body size and depth.
The plankton community consists of diverse interacting species. The estimation of species interactions in nature is challenging. There is limited knowledge on how plankton interactions are influenced by environmental conditions because of limited understanding of zooplankton feeding strategies and factors affecting trophic interactions. In this study, we used DNA-metabarcoding to investigate trophic interactions in mesozooplankton predators and the influence of prey availability on their feeding behavior. We found that mesozooplankton feeding strategies vary within species across an environmental gradient. Some species, such as Temora longicornis consistently used a selective strategy, while diets of Centropages hamatus and Acartia spp. varied between stations, showing a trophic plasticity with the prey community. We found a dominance of Synechococcales reads in Temora’s gut content and a high prey diversity for the cladoceran Evadne nordmanni. Our study shows the wide range of prey species that supports mesozooplankton community and helps to understand the spatial and temporal complexity of plankton species interactions and discriminate the selectivity ability of four zooplankton key species. Due to the central role of plankton in marine waters, a better comprehension of the spatiotemporal variability in species interactions helps to estimate fluxes to benthic and pelagic predators.
Heterocyst frequencies in Baltic Sea Aphanizomenon sp. were similar along a strong nutrient gradient from the discharge point of a sewage treatment plant at the head of the Himmerfjarden bay to the open sea. Filaments lacked heterocysts in winter and for over a month after the spring bloom had depleted combined nitrogen in the surface layer. Heterocyst-free filaments in spring contained granulate structures that decreased in abundance simultaneously as colony nitrogen content decreased, but delta N-15 remained unchanged, indicative of storage of fixed nitrogen in over-wintering Aphanizomenon sp. filaments. Heterocyst formation was initiated when water temperature was sufficient to form a shallow seasonal pycnocline that allowed filaments to be exposed to enough light to initiate growth and a subsequent intracellular shortage of nitrogen. During the growth season, heterocyst frequency varied significantly with maximum values in early summer (May), lower values in mid-August that coincided with maximum temperatures and an increase in late summer. Heterocyst frequencies decreased with increased temperatures, suggesting a more efficiently functioning nitrogenase enzyme. Based on data from three seasons, filament C: P ratios did not correlate with heterocyst frequencies, neither did reduced heterocyst frequencies coincide with high dissolved inorganic nitrogen concentrations. Increased heterocyst frequencies, however, resulted in decreased C:N ratios, probably as more heterocysts likely increase nitrogen fixation.
We used nitrogen stable isotopes to study the regulation of nitrogen fixation by filamentous cyanobacteria. Nitrogen fixation was found to be almost insensitive to combined nitrogen, along a gradient from the Himmerfjarden sewage treatment plant discharge to the open sea. We found similarly low cyanobacterial (mostly Aphanizomenon sp.) delta N-15-values at all stations, despite significant differences along the bay in both total nitrogen concentrations in water and delta N-15 in seston (particles <10 mu m), the latter used as a proxy for algae growing on combined nitrogen alone. Only late in the productive season, when cyanobacterial biomass was declining or already low, did elevated delta N-15 suggest uptake of combined nitrogen. However, this coincided with an increase in the contribution of Dolichospermum spp. to overall diazotrophic biomass and may indicate uptake of combined nitrogen by this species. These results indicate that almost all nitrogen used for growth by nitrogen-fixing cyanobacteria in the study area comes from nitrogen fixation, and very little from uptake of dissolved combined nitrogen. This study was part of a whole ecosystem experiment analyzing the effects of nitrogen removal in a sewage treatment plant discharging to the Himmerfjarden Bay, northern Baltic Sea Proper.