Evaluating zooplankton indicators using signal detection theory

Indicators are used to help managers to conserve biodiversity and guarantee the sustainable use of marine resources. Good indicators are scientifically valid, ecologically relevant, respond to pressures, and it is possible to set target levels for them. Zooplankton is an important link in the food web as it transfers energy from primary producers (phytoplankton) to planktivorous fish, including the commercially important herring in the Baltic Sea. Eutrophication is known to increase zooplankton abundance and decrease the mean size of zooplankton individuals, while particularly herring prefers larger zooplankton as prey. Therefore, both the abundance/biomass and the size structure of the zooplankton community are highly relevant for the functioning of the pelagic food web, and their combination has been proposed as an indicator of the status of the pelagic food web. In this study, we evaluated the indicator performance of zooplankton abundance and mean size in the northern Baltic Sea using signal detection theory and annual zooplankton monitoring data from years 1979–2014. Herring weight-at-age and chlorophyll a levels were used to estimate the reference periods or “gold standard” of the food web status. The sensitivity and specificity of the indicator was evaluated using ROC curves. Thresholds were set and evaluated with positive and negative predictive values for the zooplankton mean size in three sub-basins of the Baltic Sea. The results suggest that zooplankton mean size is able to reflect the state of the food web in the Baltic Sea. Our study also confirms that signal detection theory is useful in evaluating ecological indicators with clear pressures. However, with parameters that are affected by multiple contrary pressures, such as zooplankton abundance, ROC curves cannot offer enough information about the performance of an indicator parameter.     

Long-term dynamics of zooplankton in the southeastern Baltic Sea

Long-term research in the Baltic Sea revealed the basic trends of zooplankton community variations depending on oceanographic processes. Alternation of the periods of increase and decrease in salinity of the Baltic Sea against the background of climate changes (temperature increase) and eutrophication affect the state of the entire Baltic ecosystem, including zooplankton. For these periods, the dynamics of zooplankton in the Baltic Sea were analyzed based on literature data and results of regular research in the southeastern Baltic Sea during 1998–2007. The changes in the hydrological situation were accompanied by significant changes in the zooplankton community. In the 1990s–2000s, the abundance and biomass of brackish-water and thermophilous species primarily of Cladocera and Copepoda increased markedly. The role of the previously dominant marine copepod Pseudocalanus elongatus decreased due to salinity reduction in the deep-water part of the Baltic Sea. Maximum development of zooplankton occurred in years of the greatest warming-up of the water (2001, 2005–2007) against the background of a general positive trend of zooplankton abundance in the last decade.     

Structure,Dynamics and Production of Mesozooplankton Community in the Bothnian Bay,Related to Environmental Factors

Studies on the zooplankton community of the Bothnian Bay (BB), the northernmost basin of the Baltic Sea, were carried out in 1976–78. Only 8–14 taxa dominated in the zooplankton community. The highest abundances and biomasses occurred during the warmest period or immediately afterwards, in July–September. The production of zooplankton was estimated to be 3.1–7.8 g C · m⁻². a⁻¹ in the coastal area and 2.5–3.6 g C · m⁻² · a⁻¹ in the open sea. During the short growing season (June–September) the biomass turnover took place in about 11 days. The productivity of zooplankton is discussed in relation to available food of both autochthonous and allochthonous origin and compared with the other parts of the Baltic Sea.     

Studies on the zooplankton community of a shallow lagoon of the Southern Baltic Sea: long-term trends,seasonal changes,and relations with physical and chemical parameters

The Darß-Zingst Lagoon, a coastal inlet of the southern Baltic Sea, was subject to extended monitoring. The biomass data of zooplankton from 1969 to 2001 were used to analyze long-term trends and to correlate zooplankton biomass with abiotic factors. The dominant species in the lagoon were the calanoid copepods Eurytemora affinis and Acartia tonsa, and the rotifer Keratella cochlearis f. tecta. In the long-term trend, two pronounced changes in zooplankton biomass and species composition were observed. They are discussed in connection with a shift in dominance from macrophytes to phytoplankton and the invasion of a polychaet species into the lagoon. Significant relations between zooplankton data and abiotic parameters were found. While temperature, precipitation and NAO winter index correlated positively with copepods and negatively with rotifers, the relationships were inversely for pH-value and duration of ice cover.     

Responses of Phyto- and Zooplankton Communities to Prymnesium polylepis (Prymnesiales) Bloom in the Baltic Sea

A large bloom of Prymnesium polylepis occurred in the Baltic Sea during the winter 2007 – spring 2008. Based on numerous reports of strong allelopathic effects on phytoplankton exerted by P. polylepis and its toxicity to grazers, we hypothesized that during this period negative correlations will be observed between P. polylepis and (1) main phytoplankton groups contributing to the spring bloom (i.e., diatoms and dinoflagellates), and (2) zooplankton growth and abundance. To test these hypotheses, we analyzed inter-annual variability in phytoplankton and zooplankton dynamics as well as growth indices (RNA∶DNA ratio) in dominant zooplankton in relation to the Prymnesium abundance and biomass. Contrary to the hypothesized relationships, no measurable negative responses to P. polylepis were observed for either the total phytoplankton stocks or the zooplankton community. The only negative response, possibly associated with P. polylepis occurrence, was significantly lower abundance of dinoflagellates both during and after the bloom in 2008. Moreover, contrary to the expected negative effects, there were significantly higher total phytoplankton abundance as well as significantly higher winter abundance and winter-spring RNA∶DNA ratio in dominant zooplankton species in 2008, indicating that P. polylepis bloom coincided with favourable feeding conditions for zooplankton. Thus, primary consumers, and consequently also zooplanktivores (e.g., larval fish and mysids), may benefit from haptophyte blooms, particularly in winter, when phytoplankton is scarce.     

Effects of the Distribution of a Toxic Microcystis Bloom on the Small Scale Patchiness of Zooplankton

Toxic cyanobacterial blooms can strongly affect freshwater food web structures. However, little is known about how the patchy occurrence of blooms within systems affects the spatial distribution of zooplankton communities. We studied this by analysing zooplankton community structures in comparison with the spatially distinct distribution of a toxic Microcystis bloom in a small, shallow, eutrophic lake. While toxic Microcystis was present at all sites, there were large spatial differences in the level of cyanobacterial biomass and in the zooplankton communities; sites with persistently low cyanobacterial biomass displayed a higher biomass of adult Daphnia and higher zooplankton diversity than sites with persistently high cyanobacterial biomass. While wind was the most likely reason for the spatially distinct occurrence of the bloom, our data indicate that it was the differences in cyanobacterial biomass that caused spatial differences in the zooplankton community structures. Overall, our study suggests that even in small systems with extensive blooms ‘refuge sites’ exist that allow large grazers to persist, which can be an important mechanism for a successful re-establishment of the biodiversity in an ecosystem after periods of cyanobacterial blooms.     

Zooplankton response to climate warming: a mesocosm experiment at contrasting temperatures and nutrient levels

Zooplankton community response to the combined effects of nutrients and fish (hereafter N + F) at contrasting temperatures was studied in a long-term experiment conducted in 24 shallow lake mesocosms with low and high nutrient levels. We found a positive effect of N + F on zooplankton biomass, chlorophyll-a and turbidity. In contrast, zooplankton species and size diversity decreased with added N + F, as did submerged macrophyte plant volume inhabited (PVI). The community composition of zooplankton in high N + F mesocosms was related to chlorophyll-a and turbidity and to macrophyte PVI in the low N + F mesocosms. Macrophytes can protect zooplankton from fish predation. Compared to N + F effects, temperature appeared to have little effect on the zooplankton community. Yet analysis of community heterogeneity among treatments indicated a significant temperature effect at high N + F levels. The results indicate an indirect temperature effect at high N + F levels that can be attributed to temperature-dependent variation in fish density and/or chlorophyll-a concentration.     

Fading bioluminescence of the tropical Atlantic Ocean

Bioluminescence intensity acts as the indicator of the functional state of a plankton community. Data on bioluminescence intensity, zooplankton biomass, and chlorophyll a from the expeditions to the tropical and subtropical Atlantic Ocean were analyzed. The regression models implied a ~10-fold decline of bioluminescence intensity [bioluminescence potential (BP)] and zooplankton biomass for the 46 year time range from 1970 to 2016. The correlation was low between chlorophyll a (the indicator of phytoplankton biomass) and BP, but it was significant for the zooplankton biomass BP annual time series. The decline of BP was associated with the decreasing abundance of bioluminescent zooplankton, and increasing global warming-driven temperature.     

Mesozooplankton Grazing on Picocyanobacteria in the Baltic Sea as Inferred from Molecular Diet Analysis

Our current knowledge on the microbial component of zooplankton diet is limited, and it is generally assumed that bacteria-sized prey is not directly consumed by most mesozooplankton grazers in the marine food webs. We questioned this assumption and conducted field and laboratory studies to examine picocyanobacteria contribution to the diets of Baltic Sea zooplankton, including copepods. First, qPCR targeting ITS-1 rDNA sequence of the picocyanobacteria Synechococcus spp. was used to examine picocyanobacterial DNA occurrence in the guts of Baltic zooplankton (copepods, cladocerans and rotifers). All field-collected zooplankton were found to consume picocyanobacteria in substantial quantities. In terms of Synechococcus quantity, the individual gut content was highest in cladocerans, whereas biomass-specific gut content was highest in rotifers and copepod nauplii. Moreover, the gut content in copepods was positively related to the picocyanobacteria abundance and negatively to the total phytoplankton abundance in the water column at the time of sampling. This indicates that increased availability of picocyanobacteria resulted in the increased intake of this prey and that copepods may rely more on picoplankton when food in the preferred size range declines. Second, a feeding experiments with a laboratory reared copepod Acartia tonsa fed a mixture of the picocyanobacterium Synechococcus bacillaris and microalga Rhodomonas salina confirmed that copepods ingested Synechococcus, even when the alternative food was plentiful. Finally, palatability of the picocyanobacteria for A. tonsa was demonstrated using uptake of ¹³C by the copepods as a proxy for carbon uptake in feeding experiment with ¹³C-labeled S. bacillaris. These findings suggest that, if abundant, picoplankton may become an important component of mesozooplankton diet, which needs to be accounted for in food web models and productivity assessments.     

浙江饮用水源地浮游动物群落特征及环境响应

2010年1月至2011年10月,对浙江省16个饮用水源地(H1—H8为河网型,K1—K8为水库型)的浮游动物群落进行季节调查。共记录浮游动物优势种(属)21种(轮虫8种、枝角类5种、剑水蚤5种和哲水蚤3种),各类群第一优势种分别为针簇多肢轮虫(Polyarthra trigla)、长额象鼻溞(Bosmina longirostris)、粗壮温剑水蚤(Thermocyclops dybowskii)和汤匙华哲水蚤(Sinocalanus dorrii)。2年间,河网和水库浮游动物平均密度分别为345.2 L-1和199.4 L-1,生物量分别为0.667 mg/L和0.421mg/L。各类群密度百分比例均以轮虫和桡足类无节幼体为主,甲壳动物以剑水蚤为主。经逐步回归分析表明,浮游动物群落密度(生物量)与河网水质因子(P0.01)之间相关性比水库(P0.05)更密切,总磷和氨氮分别入选了河网和水库所有有效的回归方程中。通径分析和决策系统分析表明,河网的总磷和叶绿素a含量对浮游动物群落变动具有正效应,溶解氧具有负效应;总磷含量是影响河网群落变动的最重要因子,叶绿素a含量则是影响群落增长最主要的限制因子。河网剑水蚤、无节幼体和轮虫群落的密度(生物量)与水体综合营养指数TLIc密度(TLIc生物量)之间有显著的线性回归关系(P0.001),无节幼体密度构成了TLIc密度变动的限制因子,轮虫生物量成为TLIc生物量变动的限制因子,而剑水蚤是一类最重要、稳定的水质指示群落,这对于筛选浮游动物群落的一些拓展性监测指标具有重要的参考作用。     

The Native Bacterioplankton Community in the Central Baltic Sea Is Influenced by Freshwater Bacterial Species

The Baltic Sea is one of the largest brackish environments on Earth. Despite extensive knowledge about food web interactions and pelagic ecosystem functioning, information about the bacterial community composition in the Baltic Sea is scarce. We hypothesized that due to the eutrophic low-salinity environment and the long water residence time (>5 years), the bacterioplankton community from the Baltic proper shows a native “brackish” composition influenced by both freshwater and marine phylotypes. The bacterial community composition in surface water (3-m depth) was examined at a single station throughout a full year. Denaturing gradient gel electrophoresis (DGGE) showed that the community composition changed over the year. Further, it indicated that at the four extensive samplings (16S rRNA gene clone libraries and bacterial isolates from low- and high-nutrient agar plates and seawater cultures), different bacterial assemblages associated with different environmental conditions were present. Overall, the sequencing of 26 DGGE bands, 160 clones, 209 plate isolates, and 9 dilution culture isolates showed that the bacterial assemblage in surface waters of the central Baltic Sea was dominated by Bacteroidetes but exhibited a pronounced influence of typical freshwater phylogenetic groups within Actinobacteria, Verrucomicrobia, and Betaproteobacteria and a lack of typical marine taxa. This first comprehensive analysis of bacterial community composition in the central Baltic Sea points to the existence of an autochthonous estuarine community uniquely adapted to the environmental conditions prevailing in this brackish environment.     

Zooplankton and environmental factors of a recovering eutrophic lake (Lysimachia Lake, Western Greece)

The present study investigates the zooplankton community dynamics and the abiotic environment in the eutrophic Lake Lysimachia (western Greece). The lake is considered to be recovering from eutrophication after the termination of an urban sewage inflow in 2000, and its waters are replenished constantly from the nearby oligotrophic Lake Trichonis. The results show that, although a decrease in nutrient concentrations was observed compared to the past, the lake still has eutrophic characteristics. This was reflected in the zooplankton community which is typical of those found in eutrophic lakes where rotifers prevail. Similarities among this lake and other nearby lakes were found considering the zooplankton community composition and seasonal variation. However, Lake Lysimachia is inhabited also by a number of different and even unique species (e.g., Moina micrura), suggesting that this ecosystem may be an important biodiversity refuge. Most of the zooplankton species were correlated with water temperature and, to a lesser extent, eutrophication key-water quality variables. Although there are few available data on the zooplankton of the lake, the abundance and composition of the community presenting characteristics indicative of intermediate trophic conditions and suggesting that the lake is probably under a kind of “biological” recovery.     

The use of medium point density LiDAR elevation data to determine plant community types in Baltic coastal wetlands

This study investigates the use of medium point density LiDAR (light detection and ranging) elevation data for identifying and locating plant community types in Baltic coastal wetlands. Ground-surveyed micro-topography data obtained using real-time kinematic differential GPS were used to analyse and correct the accuracy of LiDAR sourced elevation values in Matlab R2010a. Following the application of elevation corrections, 3 interpolation techniques were applied: Inverse Distance Weighting (IDW), Ordinary Kriging (OK) and the Delaunay Triangulated Irregular Network (TIN) interpolation. Analysis showed that the TIN method produced a more robust model that adequately represented the micro-topographical variation across the wetland. The TIN elevation interpolation was then used to characterise the extent and distribution of the plant communities using known elevation preferences in one coastal wetland site, Tahu. The plant community model developed from the TIN elevation interpolation was then further ground-truthed in two separate Baltic coastal wetland sites, Matsalu and Kudani, in order to test model validity.The results showed that the accuracy of the LiDAR data varied dependent upon plant community type. In 5 of the 6 studied community types, the LiDAR data gave a mean elevation difference of 0.177 m (0.016 SD) above the dGPS elevations. With dGPS elevation corrections, the LiDAR data produced an accurate model of the location of the different plant community types, Kappa coefficient (κ) 0.63, at the initial site, Tahu. The model was found to be very accurate in one of the subsequent ground-truthed sites, κ 0.81, with a similar management history, but less accurate, κ 0.53, in a wetland more exposed to wave action and with a longer history of vegetation management.The inclusion of dGPS ground survey data was shown to considerably improve the accuracy of the LiDAR elevation data to facilitate the identification of plant community types on the basis of elevation. The approach developed in this study of Baltic coastal wetlands may provide a transferable method for rapidly and accurately mapping plant communities in other open environments.     

Trend Analysis of Biological Parameters in the Baltic (1976-1988)

Eutrophication of the nature is one of the most relevant problems for the human society today. In comparison to terrestrial and limnological ecosystems, however, the marine environment is affected with some exceptions of coastal waters in a minor degree. On the basis of data from 1976–1988 trend analysis for chlorophyll, primary production, zooplankton biomass and water transparency have been carried out for the Mecklenburg Bight and different areas of the Baltic proper. As expected from the longterm increase in the nutrient levels, also for some pelagic biological variables increasing trends could be observed. At least for chlorophyll they are significant in the 95% probability level for all investigated areas. Primary production shows also an increase, however, not significant for each subarea. For zooplankton nearly no changes could be observed. All data reflect a high interannual variability, which can partly be explained by meteorological and oceanological conditions. The results are discussed from an ecological point of view. The increase in phytoplankton variables is considered to be at least partly related to the eutrophication of the Baltic.     

Characteristics of Zooplankton in Syamozero Lake (South Karelia) Based on the Results of Long-Term Monitoring

The results of long-term studies on zooplankton from Syamozero Lake, South Karelia, have been analyzed. The relationship between the quantitative indices of the zooplankton community and the value and dynamics of the biogenic load on the lake is established. The redistribution of the ratio of the major groups and dominant zooplankton species, the decrease in the Shannon diversity index, the increase in the Mäemets trophic state index, and with the increase in the abundance of indicator species of higher nutrient supply have been determined. The effect of anthropogenic factors on the population characteristics of the zooplankton community and changes in the trophic status of the lake with a high resource potential have been found.     

基于宏基因组的保安湖浮游动物多样性研究

研究于2019年春、夏、秋、冬四季对保安湖进行了水样采集, 基于宏基因组测序, 在优化物种鉴定和丰度计算方法的基础上, 考察了保安湖浮游动物的多样性、群落结构及其影响因素。共鉴定到浮游动物OTU 374种, 其中原生动物282个; 枝角类45个; 桡足类26个; 轮虫21个。从季节来看, 夏、秋季保安湖的浮游动物多样性高; 从湖区来看, 肖四海和主湖区浮游动物多样性高。季节因素对保安湖浮游动物群落结构的影响高于湖区影响。保安湖营养状态为中营养型, 水体温度、叶绿素a是影响保安湖浮游动物群落结构的主要环境因子, 不同类群与环境因子相关性不同, 总体可分为5类。其中原生动物优势类群为混合营养的纤毛虫和丝足虫, 同硝氮、化学需氧量、温度有明显的相关性, 而枝角类和桡足类同环境因子的关系较为相似, 与溶氧、叶绿素a、正磷酸盐存在明显相关。研究利用宏基因组方法对保安湖浮游动物多样性开展了研究, 为从浮游动物这一角度来理解保安湖这一江湖阻隔型湖泊的生物多样性的变化提供了支撑。     

Multi-level trophic cascades in a heavily exploited open marine ecosystem

Anthropogenic disturbances intertwined with climatic changes can have a large impact on the upper trophic levels of marine ecosystems, which may cascade down the food web. So far it has been difficult to demonstrate multi-level trophic cascades in pelagic marine environments. Using field data collected during a 33-year period, we show for the first time a four-level community-wide trophic cascade in the open Baltic Sea. The dramatic reduction of the cod (Gadus morhua) population directly affected its main prey, the zooplanktivorous sprat (Sprattus sprattus), and indirectly the summer biomass of zooplankton and phytoplankton (top-down processes). Bottom-up processes and climate-hydrological forces had a weaker influence on sprat and zooplankton, whereas phytoplankton variation was explained solely by top-down mechanisms. Our results suggest that in order to dampen the occasionally harmful algal blooms of the Baltic, effort should be addressed not only to control anthropogenic nutrient inputs but also to preserve structure and functioning of higher trophic levels.     

Structure of the zooplankton community in a subtropical shallow lake (Itapeva Lake – South of Brazil) and its relationship to hydrodynamic aspects

The structure of the zooplankton community in Itapeva Lake was formed by four groups and more than 127 zooplankton species, in which microplankton was the predominant size structure. The largest richness recorded was of the protists group and in autumn seasonal campaign. Protists were characteristic of the lake, regarding density, except during spring at the Center point (copepods) and autumn at the South point (rotifers). The seasonal distribution revealed that during summer, mean density increased in the zooplankton community, exactly the opposite of phytoplankton (that blooms during the cold season). However, the maximum density was recorded during autumn. High density was recorded for the ciliate Codonella sp. at all points and during all seasons. The abundance of the tecamoeba Difflugia tuberculata was strongly associated with the maximum effects of fetch in the lake. Rotifers were generally the second most representative groups in terms of density. Rotifers and Cladocera were more abundant in summer, whereas copepods were in spring and winter/98. The Shannon–Wiener index showed that the smallest zooplankton diversity average occurred during the winter/98 (H=1.44), while in autumn the largest zooplankton diversity average (H=2.36) was observed. Correlations (r-Pearson, p<0.05) with wind velocity were significant for zooplankton density (groups and/or abundant species), diversity, and richness. The analysis of variance (ANOVA) showed a seasonally significant spatial-temporal variation for the factors sampling point, day and shift (p<0.01). Temporal alterations in density, diversity and richness were closely dependent on the hydrodynamic action induced by the wind on the spatial distribution of the zooplankton community in the Itapeva Lake.     

<Emphasis Type="Italic">Bythotrephes</Emphasis> invasion elevates trophic position of zooplankton and fish: implications for contaminant biomagnification

We estimated the effects of Bythotrephes longimanus invasion on the trophic position (TP) of zooplankton communities and lake herring, Coregonus artedi. Temporal changes in lacustrine zooplankton communities following Bythotrephes invasion were contrasted with non-invaded reference lakes, and along with published information on zooplankton and herring diets, formed the basis of estimated changes in TP. The TP of zooplankton communities and lake herring increased significantly following the invasion of Bythotrephes, whereas TP in reference lakes decreased (zooplankton) or did not change significantly (lake herring) over a similar time frame. Elevated TP following Bythotrephes invasion was most prominent in lakes that also supported the glacial relict, Mysis diluvania, suggesting a possible synergistic interaction between these two species on zooplankton community composition. Our analysis indicated that elevated TPs of zooplankton communities and lake herring are not simply due to the presence of Bythotrephes, but rather reflect changes in the zooplankton community induced by Bythotrephes; namely, a major reduction in the proportion of herbivorous cladoceran biomass and a concomitant increase in the proportion of omnivorous and/or predatory copepod biomass in invaded lakes. We demonstrated that increases in TP of the magnitude reported here can lead to substantial increases in fish contaminant concentrations. In light of these results, we discuss potential mechanisms that may be responsible for the disconnect between empirical and theoretical evidence that mid-trophic level species invasions (e.g., Bythotrephes) elevate contaminant burdens of consumer species, and provide testable hypotheses to evaluate these mechanisms.     

Pelagic fish and zooplankton species assemblages in relation to water mass characteristics in the northern Bering and southeast Chukchi seas

This research explores the distributions and community composition of pelagic species in the sub-Arctic and Arctic waters of the northern Bering and central and southern Chukchi seas during September 2007 by linking pelagic zooplankton and fish assemblages to water masses. Juvenile saffron cod (Eleginus gracilis), polar cod (Boreogadus saida), and shorthorn sculpin (Myoxocephalus scorpius) were most abundant in warm, low salinity Alaska Coastal Water (ACW) of the central Chukchi Sea, characterized by low chlorophyll, low nutrients, and small zooplankton taxa. Adult Pacific herring (Clupea pallasii) were more abundant in the less stratified Bering Strait waters and in the colder, saltier Bering Shelf Water of the northern Bering and southern Chukchi seas, characterized by high chlorophyll, high nutrients, and larger zooplankton taxa. Juvenile pink (Oncorhynchus gorbuscha) and chum (O. keta) salmon were most abundant in the less stratified ACW in the central Chukchi Sea and Bering Strait. Abundances of large zooplankton were dominated by copepods (Eucalanus bungii, Calanus glacialis/marshallae, Metridia pacifica) followed by euphausiids (juvenile Thysanoessa raschii and unidentified taxa), whereas small zooplankton were dominated by bivalve larvae and copepods (Centropages abdominalis, Oithona similis, Pseudocalanus sp.). Pelagic community composition was related to environmental factors, with highest correlations between bottom salinity and large zooplankton taxa, and latitude and fish species. These data were collected in a year with strong northward retreat of summer sea ice and therefore provide a baseline for assessing the effects of future climate warming on pelagic ecosystems in sub-Arctic and Arctic regions.