Mediterranean Copepods Research Articles

Transcriptomic analysis reveals responses to a polluted sediment in the Mediterranean copepod Acartia clausi

Marine sediments are regarded as sinks for several classes of contaminants. Characterization and effects of sediments on marine biota now require a multidisciplinary approach, which includes chemical and ecotoxicological analyses and molecular biomarkers. Here, a gene expression study was performed to measure the response of adult females of the Mediterranean copepod Acartia clausi to elutriates of polluted sediments (containing high concentrations of polycyclic aromatic hydrocarbons, PAHs, and heavy metals) from an industrial area in the Southern Tyrrhenian Sea (Bagnoli-Coroglio).Functional annotation of the A. clausi transcriptome generated as reference here, showed a good quality of the assembly and great homology with other copepod and crustacean sequences in public databases. This is one of the few available transcriptomic resources for this widespread copepod species of great ecological relevance in temperate coastal areas. Differential expression analysis between females exposed to the elutriate and those in control seawater identified 1000 differentially expressed genes, of which 743 up- and 257 down-regulated. Within the up-regulated genes, the most represented functions were related to proteolysis (lysosomal protease, peptidase, cathepsin), response to stress and detoxification (heat-shock protein, superoxide dismutase, glutathione-S-transferase, cytochrome P450), and cytoskeleton structure (α- and β-tubulin). Down-regulated genes were mostly involved with ribosome structure (ribosomal proteins) and DNA binding (histone proteins, transcription factors). Overall, these results suggest that processes such as transcription, translation, protein degradation, metabolism of biomolecules, reproduction, and xenobiotic detoxification were altered in the copepod in response to polluted elutriates. In conclusion, our results contribute to gaining information on the transcriptomic responses of copepods to polluted sediments. They will also prompt the selection of genes of interest to be used as biomarkers of exposure to PAHs and heavy metals in molecular toxicology studies on copepods, and in general, in comparative functional genomic studies on marine zooplankton.

DISTRIBUTION OF SOME PONTO-CASPIAN AND ALIEN COPEPODS (CRUSTACEA, COPEPODA) IN PLANKTON OF THE DON RIVER BASIN

In 2018-2019, the zooplankton was studied in the Don River from the source to the mouth including the Tsimlyansk Reservoir, Volga-Don shipping canal, and the upper part of Taganrog Bay of the Sea of Azov. Habitats of two Ponto-Caspian species of copepods ( Heterocope caspia and Eurytemora caspica ) and of three alien species, Mediterranean copepod Calanipeda aquaedulcis , a representative of the neritic zone Acartia ( Acanthacartia ) tonsa and East Asian euryhaline Thermocyclops taihokuensis were found. For the first time, the findings of T. taihokuensis were recorded in the Don River upstream and downstream of the Tsimlyansk Reservoir and in water bodies of the Volga-Don shipping canal. It is shown that the Ponto-Caspian Eurytemora caspica inhabits the Don River basin and Taganrog Bay of the Sea of Azov. The European copepod E. affinis which was previously recorded in the region was not found in the studied areas of the basin. The occurrence (>80% of samples) of the Ponto-Caspian species and Calanipeda aquaedulcis was the highest. A recent invader Thermocyclops taihokuensis reached the maximum abundance (>100 000 ind./m). By an example of the Tsimlyansk Reservoir, it is found that the way of the spread of the Ponto-Caspian and alien species in the Don River basin may be large-scale activities on the introduction of planktonic and benthic invertebrates conducted in the 1950-1970s in order to improve the food supply of valuable fish species. The history of dispersal of the studied copepod species and their population characteristics are discussed.

Spreading of Alien Zooplankton Species of Ponto-Caspian Origin in the Reservoirs of the Volga and Kama Rivers

Zooplankton was studied in August 2015–2017 in eight reservoirs of the Volga River, in an unregulated part of the river between the cities of Volgograd and Astrakhan, and in three reservoirs of the Kama River. The Ponto-Caspian species were recorded in the Volga River downstream of the city of Kazan (south of 55°32′ N) and in the Kama River from the mouth to the upper reaches of the Kama Reservoir (59°20′ N). Six alien species (Heterocope caspia, Calanipeda aquaedulcis, Eurytemora caspica, Cornigerius maeoticus maeoticus, Cercopagis pengoi, and Podonevadne trigona ovum) were recorded in the Volga reservoirs and three species (Heterocope caspia, Eurytemora caspica, and Cercopagis pengoi) were recorded in the Kama reservoirs. It was found first time that copepods Heterocope caspia and Eurytemora caspica spread and naturalized in the areas of all three Kama reservoirs (within the distance of 1000 km from the Volga River); the cladoceran Cercopagis pengoi formed a disrupted range with a group of habitats in the mouth part of the Kama River (55°12′–55°26′ N) and north near the city of Perm (57°53′–58°26′ N). The boundary of the ranges of Calanipeda aquaedulcis, Cornigerius maeoticus, and Cercopagis pengoi shifted 300–400 km to the north in the Volga River and 300 km in the Kama River; they occupied almost all area of the Kuibyshev Reservoir except for the upper reaches of its Volga part. The range expansion of the cladoceran Podonevadne trigona ovum was not observed; this species was found only in the Volgograd Reservoir (46°18′ N). It was revealed that by 2017 the Mediterranean copepod Calanipeda aquaedulcis had become common (occurrence in more than 90% of samples), locally numerous in the Volga River from the city of Astrakhan (52° N) to the mouth of the Kama River (55°12′ N) and in the Kama River from the mouth to the upper reaches of the Kama part of the Kuibyshev Reservoir (55°24′ N). It is revealed that a new species Eurytemora caspica (described in 2013), but not E. affinis (as it was believed earlier), lives in the Volga and Kama rivers. The prospects of the further spread of Ponto-Caspian species up the Volga and Kama rivers and their role in the zooplankton in water bodies are discussed.

The Mediterranean Copepod Calanipeda aquaedulcis Kritschagin, 1873 (Crustacea, Calanoida) in the Volga River Reservoirs

The Mediterranean copepod Calanipeda aquaedulcis Kritschagin, 1873 was first recorded in the Kuibyshev Reservoir in August 2015. It has been detected at all surveyed stations from the Volga-Kama reach to the dam of the Zhiguli hydroelectric power plant; the most northern finding of the copepod has been recorded in the mouth of the Kama River (55°24′ N). C. aquaedulcis (0.3–7.3 thous. ind./m3) is in the group of dominant species and forms, on average, 13% of the total abundance and biomass of zooplankton. Comparatively large (1.0–1.4 mm) copepods reproduce intensively; females carry up to 18 eggs (on average 10 ± 0.6). The main part of the population (>90%) are represented by nauplii. The species has been found in smaller quantities (0.04–1.1 thous. ind./m3) throughout the Saratov Reservoir, which is located downstream the cascade. The ecology of the species and its potential importance in the zooplankton of the Volga reservoirs is discussed.

Identifying copepod functional groups from species functional traits.

We gathered information on the functional traits of the most representative copepod species in the Mediterranean Sea. Our database includes 191 species described by 7 traits encompassing diverse ecological functions: minimal and maximal body length, trophic group, feeding type, spawning strategy, diel vertical migration and vertical habitat. Cluster analysis in the functional trait space revealed that Mediterranean copepods can be separated into groups with distinct ecological roles.

Effects of low pH and raised temperature on egg production, hatching and metabolic rates of a Mediterranean copepod species (Acartia clausi) under oligotrophic conditions

This study includes the first information on the combined effect of low pH and raised temperature on egg production rate (EP), hatching success (HS), excretion and respiration of the Mediterranean copepod Acartia clausi. Adult individuals of A. clausi and fresh surface seawater were collected at a coastal station in Saronikos Gulf during April 2012. Four different conditions were applied: two different pH levels (present: 8.09 and future: 7.83) at two temperature values (present: 16°C and present+4 °C= 20°C). EP and HS success decreased significantly over the duration of exposure at future pH at both temperature conditions. However, the analysis of the combined effect of pH, T, chlorophyll α and the duration of the experiments on EP and HS revealed that ocean acidification had no discernible effect, whereas warming; food and the duration of exposure were more significant for the reproductive output of A. clausi. Temperature appeared to have a positive effect on respiration and excretion. Acidification had no clear effect on respiration, but a negative effect on the A. clausi excretion was observed. Acidification and warming resulted in the increase of the excretion rate and the increase was higher than that observed by warming only. Our findings showed that a direct effect of ocean acidification on copepod’s vital rates was not obvious, except maybe in the case of excretion. Therefore, the combination of acidification with the ambient oligotrophic conditions and the warming could result in species being less able to allocate resources for coping with multiple stressors.

Changes in expression of stress genes in copepods feeding upon a non-brevetoxin-producing strain of the dinoflagellate Karenia brevis

Effects of the toxic Gulf of Mexico dinoflagellate Karenia brevis on its copepod grazers are equivocal, in that this dinoflagellate is ingested by various copepods, but may be toxic to, and/or nutritionally inadequate for grazers. Recent studies have shown that when the Mediterranean copepod Calanus helgolandicus fed on K. brevis, egg production rates and egg viability declined steadily over time, reaching almost zero levels after 5 days of feeding (Turner et al., 2012). The K. brevis strain used in that study was chemically analyzed and shown not to contain any brevetoxins, but may have contained other harmful metabolites. Here we present gene expression analyses by reverse transcription-quantitative PCR (RT-qPCR) in C. helgolandicus after different exposure times (3, 5 and 8 days) to the same non-brevetoxin-containing K. brevis strain examined previously. The analyzed genes have a primary role in generic stress responses, defense systems (e.g. aldehyde, free fatty acid and free radical detoxification) and apoptosis regulation in other organisms. After 3 days of feeding on K. brevis, gene expression levels in copepods did not show significant changes. However, after 5 days of exposure, expression of stress-response genes was significantly reduced. After prolonged exposure for 8 days, expression of genes for 5 of 6 aldehyde dehydrogenases was strongly reduced, but expression of other genes was not coherently reduced, or increased. Microscopic observations revealed that after only a single day of feeding on K. brevis, freshly-spawned eggs were morphologically similar to those produced by copepods feeding on control diets, but after 3 days of feeding on K. brevis, eggs exhibited altered membrane cell morphology and apoptotic features such as granulation and degeneration of the cytoplasm matrix, compared to the unaltered eggs produced by copepods feeding on control diets. The changes in gene expression levels in copepods feeding on K. brevis were similar to those noted previously for copepods feeding upon diatoms that contained oxylipins, which interfered with copepod reproductive success. Changes in gene expression in copepods feeding upon toxic algal diets may offer important early warning signals of copepod stress responses to these diets.

Biogeographic effects of the Gulf of Mexico red tide dinoflagellate Karenia brevis on Mediterranean copepods

There may be biogeographic aspects of interactions between toxic phytoplankton and their zooplankton grazers. Grazers that naturally co-occur with a given species of toxic phytoplankton may have evolved mechanisms to counteract adverse effects of phytoplankton toxins. Conversely, grazers that have no co-evolutionary experience with a toxic phytoplankter may be more susceptible to its effects. This may also be true for toxic metabolites other than neurotoxins that adversely affect copepod reproduction and development such as the well-described diatom oxylipins. In order to test this hypothesis, we investigated interactions in terms of feeding, reproductive success and survival of a copepod feeding on a potentially toxic dinoflagellate species with which the copepod does not naturally co-occur: the red tide dinoflagellate Karenia brevis from the Gulf of Mexico and the copepod Calanus helgolandicus from the Mediterranean. We additionally compared interactions of these two allopatric plankters with various co-occurring sympatric ones, including the copepod Temora stylifera and a non-neurotoxic strain of the dinoflagellate Alexandrium tamarense, both from the Mediterranean, and as a control, the non-toxic dinoflagellate Prorocentrum minimum. Both Mediterranean copepods fed, reproduced and survived on diets of K. brevis from the Gulf of Mexico, but neither copepod did as well on this diet as on diets of A. tamarense from the Mediterranean or the control diet of P. minimum. Of the two copepods, T. stylifera fared worse on a diet of K. brevis than did C. helgolandicus. Egg hatching success for both copepods feeding on K. brevis was sharply diminished over the seven days of the experiments. This was surprising, since we subsequently discovered that our culture of K. brevis contained no brevetoxins. However, our culture appeared to contain another as yet unidentified compound. Similarly, we have previously demonstrated that our culture of A. tamarense, which contained no saxitoxins or aldehydes, did contain another unidentified compound that reduced egg hatching success by inhibiting sperm from fertilizing eggs. Thus, although diets of the dinoflagellate from the Gulf of Mexico (K. brevis) caused adverse effects on both of the Mediterranean copepods, T. stylifera was also adversely affected by the Mediterranean dinoflagellate (A. tamarense). The copepod T. stylifera which co-occurs in the Gulf of Mexico with the dinoflagellate K. brevis was far more adversely affected by feeding on a sole diet of this dinoflagellate than was the Mediterranean copepod (C. helgolandicus) which never naturally co-occurs with this dinoflagellate. Thus, any putative biogeographic effects of copepods feeding on allopatric versus sympatric dinoflagellates did not clearly emerge from our data. However, since both species of dinoflagellates appear to contain additional undescribed chemicals other than the neurotoxins for which they are best known, and these compounds are potentially related to the adverse effects we recorded, it appears that understanding of the biogeography must await further defining the biochemistry of some harmful algae:grazer interactions.

Marine biological invasions in waters of the port of Novorossiysk in the Black Sea

The results of the monitoring of ballast waters of commercial vessels and research on the ecosystem biodiversity of the Novorossiysk Port are reported. Data on structure of immigrant fauna, its abundance, survival and origin of species were obtained. It has been established that the risk of introduction of Mediterranean species into the Novorossiysk Bay is the most probable. The basic “risk groups” are copepods and polychaetes. It has been hypothesized, that ship ballast water can become a primary factor of the “mediterranization” of the copepod fauna (Copepoda) in the northeast of the Black Sea. During the period of research in the Novorossiysk Bay, 36 species of Mediterranean copepods were recorded. A massive number of the cyclopoid copepod Oithona brevicornis Giesbr., 1891, a new species for the Black Sea, was recorded in samples collected in the autumn of 2005 and 2006. The status of the invader was attributed to the polychaete of the Streblospio genus. The necessity of ship ballast water control in Russia and the development of methodology, methods, and regulations for the prevention of the intrusion of pathogenic and potentially dangerous organisms by marine traffic were corroborated.

Cannibalistic behaviour of rock-pool copepods: An experimental approach for space, food and kinship

Studies on cannibalism in harpacticoid copepods are restricted to predation on naupliar larvae in rock-pool harpacticoids of the genus Tigriopus. An earlier experimental study on the Mediterranean copepod Tigriopus fulvus indicated that females recognized their own larvae and preferentially preyed on nauplii other than their own. In a series of laboratory experiments, we tested if there were differences in naupliar predation as a function of crowding, food level and sex in Tigriopus brevicornis and T. fulvus. Results show that cannibalism was restricted to the first larval stages (N1 and N2). Both food availability and adult density significantly affected the predation rate. Contrary to earlier suggestions, adult males also preyed on the nauplii. We found no evidence that adults spare their own offspring, for neither T. fulvus nor T. brevicornis.This is in accordance with what one would expect for species having the life history characteristics of Tigriopus, i.e.: multiple broods and large number of offspring. Earlier results indicating parental care in Tigriopus must be taken with caution.

Phenological changes in the Northwestern Mediterranean copepods Centropages typicus and Temora stylifera linked to climate forcing

Planktonic copepods play a major role in the fluxes of matter and energy in the marine ecosystem, provide a biological pump of carbon into the deep ocean, and play a role in determining fish recruitment. Owing to such ecological considerations, it is essential to understand the role that climate might play in the interannual variability of these organisms and the mechanisms by which it could modify the ecosystem functioning. In this study, a causal chain of meteorological, hydrological and ecological processes linked to the North Atlantic Oscillation (NAO) was identified in the Ligurian Sea, Northwestern Mediterranean. The forcing by the NAO drives most of the hydro-climatic variability during winter and early spring. Subsequently, interannual and decadal changes of the dominant copepods Centropages typicus and Temora stylifera were significantly correlated to the state of the hydro-climatic signal and tightly coupled to the NAO. Direct and indirect effects whose influence promoted phenological changes in the two copepod populations drove the species' responses to climatic forcing. Opposite responses of the analysed species were also highlighted by these results. While years characterized by the positive phase of the NAO leads to enhancement of the strength and the forward move of the C. typicus peak, they act negatively on the annual cycle of T. stylifera, the abundance of which drops twofold and the annual peak appears delayed in time. In contrast, low NAO years lead to high abundance of T. stylifera and a forward timing of its peak, and acts in turn negatively on the C. typicus annual cycle in both abundance (low) and timing (delayed). Owing to the synchronism between hydro-climatic conditions and the NAO, and the major role of these species in the pelagic ecosystem of the studied area, these results provide key elements for interpreting and forecasting decadal changes of planktonic populations in the Ligurian Sea.

Infection with the dinoflagellate parasite Blastodinium spp. in two Mediterranean copepods

Infection with the intestinal parasite Blastodinium mangini resulted in reduced survival of starved adults of the Mediterranean copepod Oncaea sp. No such effect was measurable for Corycaeus sp. infected by Blastodinium navicula. Both sexes of Oncaea sp. adults were infected by B. mangini and infected copepods were able to mate successfully. However, Oncaea sp. females infected by B. mangini did not produce eggs and, thus, appeared to be sterile. By inducing sterility, the harmful effect of B. mangini infection on Oncaea sp. populations is bound to be more profound than the effect on the individual level. The mechanism of infection by Blastodinium spp. remains unknown, but uptake of parasite zoospores by Oncaea sp. copepodites concurs with the hypothesis that infection occurs through the ingestion of zoospores by juvenile hosts.

Vertical zonation patterns for Mediterranean copepods from the surface to 3000 m at a fixed station in the Tyrrhenian Sea

Vertical zonation patterns for Mediterranean copepods from the surface to 3000 m at a fixed station in the Tyrrhenian Sea