Acartia tonsa (Сopepoda) in the Black and Caspian Seas: Review of its success and some lessons

The variety of aquatic nonindigenous animals in marine habitats worldwide includes more than 16 planktonic Copepoda species. Acartia tonsa is a very successful one, distributed in many seas. Its invasion into European seas was analyzed before (Brylinski,1981), but from that time A.tonsa extended its range in European aquatic habitats. The author describes the history of the A.tonsa invasion into the Ponto-Caspian basin as well as some misleading earlier publications. Morphologic differences between A.clausi and A.tonsa, the neglect of which led to the wrong identification, were examined. The data on A.tonsa and total copepod dynamics in the Sevastopol Bay during the period of 1976~1996 and the same data on the Caspian Sea since 1981 were analyzed. The average size of A.tonsa in new habitats decreased, and its relative density in the Black and Caspian Seas gradually increased.     

Discrimination between Acartia (Copepoda: Calanoida) species using their diffraction pattern in a position, rotation invariant digital correlation

Digital images of Acartia discaudata, A. clausi, A. margalefiand A. tonsa were processed to obtain their diffraction pattern.To discriminate between species and sex all diffraction patternswere correlated with a spatial filter, invariant to positionand rotation, for each Acartia male and female. This filterwas made up using a combination of different images of eachspecies and sex. Considering the great similarity between thecopepod species used in this work and between the male and femaleof each species the results obtained are very good. It is concludedthat the method used to discriminate between species of thiscongeneric group can be very useful for the development of anautomated system for the identification of copepods.     

Relationship between specific dynamic action and protein deposition in calanoid copepods

The link between specific dynamic action (SDA) and protein deposition was investigated in copepodites stage V of two calanoid copepod species, the neritic Acartia tonsa and the oceanic Calanus finmarchicus. This was done by measuring respiration before, during, and after a specific feeding period and measuring the incorporation of carbon into proteins. These were also measured on individuals incubated with cycloheximide, an antibiotic that inhibits protein synthesis. The cycloheximide treatment significantly diminished the magnitude of SDA in both A. tonsa and C. finmarchicus, and inhibited carbon incorporation into protein in both species. This provides evidence that the rate at which protein deposition takes place greatly affects the magnitude of SDA. The specific respiration rates of both starving and feeding copepods were generally higher in A. tonsa than in C. finmarchicus. This influenced SDA, the magnitude of SDA normalised to an 8 h feeding period being threefold higher in A. tonsa (78.7+/-25.7 nlO(2) μgC(-1)) than in C. finmarchicus (27.5+/-11.6 nlO(2) μgC(-1)). This difference may arise due to differences in energy allocation in the organisms of the copepodite V stage of the two species. In this stage C. finmarchicus deposits large quantities of storage lipids, predominately wax esters, whereas A. tonsa deposits proteins during somatic growth.     

Production of Bacterial Substrate by Marine Copepods: Effect of Phytoplankton Biomass and Cell Size

Laboratory experiments were performed to evaluate the importanceof grazing activity of the marine copepod Acartia tonsa forproduction of substrate for bacteria. Acartia tonsa were feda range of concentrations of the nanoflagellate Rhodomonas baltica,the diatom Ditylum brightwelli and the dinoflagellate Ceratiumlineatum. Regardless of the concentration of R. baltica, nodetectable response in bacterial biomass was observed due tograzing. However, when A. tonsa grazed the larger phytoplanktoncells of D. brightwelli and C. lineatum, responses in bacterioplanktonwere observed. It was estimated that approximately 54–69%of the grazed carbon was lost to the surroundings when A. tonsawas feeding on these large phytoplankton species. The laboratoryresults were applied to a dataset from a coastal temperate ecosystem.This analysis showed that the copepod contribution to the DOCpool was as important as the leakage from the primary producers.It is concluded, that the DOM contribution from copepods willbe largest when grazing plankton communities are composed oflarge species.     

Seasonal variations in copepod body length: a comparison between different species in the Lagoon of Venice

The seasonal variation in length of the most abundant copepod species in the lagoon of Venice were compared and the relative influence of temperature, chlorophyll concentration and salinity examined. Temperature seems to be the primary factor influencing copepod body length in the lagoon of Venice, but the different species vary markedly in their response. Calanoid copepods (Acartia clausi, A. tonsa, Paracalanus parvus and Centropages ponticus) showed a more definite trend of size variation with temperature than the cyclopoids (Oithona nana and O. similis) and the harpacticoid Euterpina acutifrons. The size of the poecilostomatoids Oncaea media and O. subtilis was not affected by temperature, and was almost constant over time. Differences in the metabolic rates, longevity and specialization of calanoid, cyclopoid and harpacticoid copepods could explain their different responses to temperature.     

Diel variations in Acartia tonsa feeding, respiration and egg production in a Mediterranean coastal lagoon

Short-term changes in abundance, feeding, respiration and spawningby the copepod Acartia tonsa were studied during four 24 h periodsat two stations in a Mediterranean lagoon in May and June of1989 and 1990. Nightly increases of abundance in the upper layer,attributed to nocturnal upward migration, were observed in threeout of the four time series. Nevertheless, occasional dailyincreases were observed too, so that no clear diel patternsin abundance could be defined. Contrarily, diel patterns seemedto appear: (i) for feeding (higher at the beginning of the night),based on gut fluorescence and clearance and ingestion rate measurements;(ii) for respiration (lower at night and based on 8 h incubationperiods); and (iii) for spawning (higher at the end of the night,based on experimental data). The origin of these patterns, aswell as their relationships to environmental data and theirpossible association, are discussed with regard to the availableliterature.     

Physiological and behavioral responses of the mud snails Hydrobia glyca and Hydrobia ulvae to extreme water temperatures and salinities: implications for their spatial distribution within a system of temperate lagoons

Physiological responses (oxygen consumption) and behavioral responses (feeding and activity) of the mud snails Hydrobia ulvae and Hydrobia glyca at different salinities (20 per thousand-80 per thousand) and temperatures (20 degrees and 30 degrees C) were studied. After 24 h under experimental conditions, both Hydrobia species already showed maximal activities (>90%) for a wide salinity range (30 per thousand-70 per thousand), with significant differences in activity between species only outside the usual salinity range of the studied lagoon. In contrast, egestion rates of H. glyca were significantly higher at the lowest salinities tested (30 per thousand and 40 per thousand) irrespective of water temperature, whereas egestion rates of H. ulvae were always significantly higher (57% on average) at 20 degrees C than at 30 degrees C and at the usual salinities found in the field (40 per thousand and 50 per thousand). Both species showed an oxyregulatory response to dissolved oxygen concentrations ranging from saturation to 1.5 mg O(2) L(-1), although specific oxygen consumption rates were significantly higher at 30 degrees C than at 20 degrees C (Q(10)=1.47+/-0.08 for H. ulvae and Q(10)=12.1+/-0.06 for H. glyca) and at the lowest salinities (30 per thousand-50 per thousand for H. ulvae and 30 per thousand-40 per thousand for H. glyca). On average, specific rates were higher for the smaller-sized H. glyca (1.64+/-0.03 microg O(2) mg(-1) ash-free dry weight [AFDW]) than for H. ulvae (1.35+/-0.03 microg O(2) mg(-1) AFDW). Despite the overlapping of their tolerances to high temperatures and salinities, the observed interspecies differences could play a certain role in the distribution of H. ulvae and H. glyca in the studied habitat. In particular, the decreasing feeding activity but increasing respiration of H. ulvae at 30 degrees C for salinities that usually occur in the studied lagoon could represent disadvantages to H. glyca during the warm period.     

Life in the extreme environment at a hydrothermal vent: haemoglobin in a deep-sea copepod.

This is the first study, to my knowledge, quantifying the respiratory pigment haemoglobin discovered in a deep-sea copepod. Haemoglobin in copepods has previously been documented in only one other species from the deep water of an Italian lake. Specimens of the siphonostomatoid Scotoecetes introrsus Humes were collected during submersible dives at 2500 m depth near a hydrothermal vent at the East Pacific Rise (9 degrees N). The haemoglobin content in the copepods' haemolymph was 4.3 +/- 0.6 micrograms per individual female (n = 6) and 1.8 +/- 0.1 micrograms per individual male (n = 6). Weight-specific concentrations of haemoglobin were identical for females and males (0.25 +/- 0.04 and 0.26 +/- 0.02 microgram per microgram dry weight, respectively). These haemoglobin concentrations are higher than those found in other small crustaceans. Activity of the electron transport system indicated that the respiration rates in S. introrsus (13.7 +/- 7.7 microliters O2 per milligram dry weight per hour) were similar to those in the shallow-water copepod Acartia tonsa (9.1 +/- 1.3 microliters O2 per milligram dry weight per hour). It was concluded that the possession of highly concentrated haemoglobin allows S. introrsus to colonize a geologically young, thermally active site such as the vicinity of a hydrothermal vent, despite the prevailing oxygen depletion.     

DMSP-consuming bacteria associated with the calanoid copepod Acartia tonsa (Dana)

DMSP-consuming bacteria (DCB) were recovered from the body and fecal pellets of the copepod Acartia tonsa (Dana). The most probable number of DCB associated with starved A. tonsa was 9.2x10(2) cells copepod(-1). The abundance of DCB recovered from the copepod body increased to 1.6-2.8x10(4) after the copepod fed on DMSP-containing alga. DCB abundance associated with fecal pellets averaged 1.2x10(4) cells pellet(-1). In enrichment cultures, the DCB grew with a doubling time of 1.1-2.9 days, and consumed DMSP at a rate of 4.5-7.5 fmol cell(-1) day(-1). The apparent DMSP-to-DMS conversion efficiency was 25-41% for DCB from copepod body, and 99% for DCB from fecal pellets. Our study demonstrated that copepods and their fecal pellets may harbour dense populations of DCB, and that the copepod-bacteria coupling represents a novel mechanism for DMSP consumption in the water column.     

Cryptic ecological diversification of a planktonic estuarine copepod, Acartia tonsa

The recent discovery of cryptic species in marine holoplankton, organisms that 'drift' in oceanic currents throughout their life cycle, contrasts with their potential for long-distance passive dispersal and presumably high gene flow. These observations suggest that holoplankton species are adapting to surprisingly small-scale oceanographic features and imply either limited dispersal or strong selection gradients. Acartia tonsa is a widespread and numerically dominant estuarine copepod containing deep mitochondrial lineages within and among populations along the northwestern Atlantic coast. In this study, we intensively investigated A. tonsa populations in Chesapeake Bay with the goals of testing species status for the deep lineages and testing for their association with environmental features over space and time. Phylogenetic analyses of DNA sequences from mitochondrial cytochrome c oxidase I (mtCOI) and the nuclear ribosomal internal transcribed spacer (nITS) resolved two concordant monophyletic clades. Deep divergence between the two clades (13.7% uncorrected sequence divergence for mtCOI and 32.2% for nITS) and genealogical concordance within sympatric populations strongly suggest that the two clades represent reproductively isolated cryptic species. Based on restriction fragment length polymorphisms of mtCOI, representatives from the two clades were found consistently associated with contrasting salinity regimes (oligohaline vs. meso-polyhaline) with an overlap between 2 and 12 PSU in samples from 1995 to 2005. Finding these patterns in one of the best-known estuarine copepods reinforces the conclusion that marine biodiversity is underestimated, not only in terms of species numbers, but also with respect to niche partitioning and the potential importance of ecological divergence in marine holoplankton.     

Do Acartia tonsa (Dana) eggs regulate their volume and osmolality as salinity changes?

Subitaneous eggs from an euryhaline calanoid copepod Acartia tonsa were challenged by changes in salinity within the range from full strength salinity, down to zero and up to >70?psu. Egg volume changed immediately, increasing from 2.8?×?10(5)?μm(3) at full strength salinity (35?psu) to 3.8?×?10(5)?μm(3) at 0?psu and back to its initial volume when gradually being returned to full strength salinity. Egg osmolality followed the molality of the surrounding water when challenged within a salinity range from 2 to 50?psu. Egg respiration was not affected when eggs kept at 35?psu was exposed to low salinity (2?psu). These results suggest that eggs are unable to regulate their volume or osmolality when challenged with changes in salinity. Gradual changes in salinity from 35 to 2?psu and back did not harm the eggs (embryos), since the hatching success remained unaffected by such changes in salinity. In contrast, extreme hyper-saline conditions (76?psu) made the eggs implode and killed the embryo. We propose that the embryo is protected from salinity stress by its plasma membrane and that water exchange driven by osmosis is restricted to the perivitelline space of the egg, which acts as a perfect osmometer in the salinity range of 5-35?psu. We hypothesize further that the embryo is able to keep its volume and osmolality constant due to the impermeability of the inner plasma membrane of the egg or by a combination of osmoregulation and reduced permeability of the inner plasma membrane.     

Distribution of zooplankton during opposite tide fluxes in the lagoon complex of Chelem, Yucatan, Mexico]

Zooplankton was surveyed in a tropical lagoon system of the northern coast of the Yucatan Peninsula in high tide, December (1998) and low tide, March 1999 (northerlies season). Zooplankton biomass was measured, zooplankters were counted, and copepods were identified and quantified. Despite the fact that both months were influenced by winds from the North, they showed a different salinity gradient which developed a particular structure of the zooplankton community. Biomass tended to be accumulated in certain areas apparently because of the high residence time of water in Chelem, the forcing effect of the northerlies, and of the tidal current. Biomass values suggest a relatively high secondary production when compared with other systems of the Yucatan Peninsula. The distribution of the copepods Acartia lilljeborgii and A. tonsa is related to saline conditions and tidal flow. The overall faunistic and hydrologic data suggest that even during a single climatic season, the zooplankton community shows strong changes due to mesoscale hydrological processes.     

Nutritive Value and Selection of Food Particles by Copepods During a Spring Bloom of Phaeocystis sp. in the English Channel, as Determined by Pigment and Fatty Acid Analyses

In this study phytoplankton pigments and fatty acids were usedas biomarkers to study trophic relationships between phytoplanktonand zooplankton. These markers permit the characterization ofboth suspended matter and copepods, allowing examination ofthe transfers from food to zooplankton. A drogue study was carriedout to follow a water mass in the coastal waters off the easternEnglish Channel over a 3-day period, with samples collectedevery 3 h. The study focused on the dominant calanoid copepodspecies: Temora longicornis, Acartia clausi and Pseudocalanuselongatus. Our study was performed during the spring phytoplanktonbloom when solitary cells of Phaeocystis sp. formed 90% of thetotal phytoplankton. Fatty acid analyses provided an indicationof the low nutritive value of these algal cells; in contrastto other algal species which had higher nutritional value (e.g.colony-forming diatoms, Cryptophytes and dinoflagellates). Ourresults suggest that all species selectively grazed on Phaeocystissp. and non-selectively on diatoms. Dinoflagellates were avoidedby all species. Temora longicornis selectively grazed on Cryptophytes,which may be related to the nutritional value of this algae.The fatty acid composition of the three copepod species indicatedan ‘herbivorous’ diet for P.elongatus and an omnivorousone for A. clausi and T. longicornis, which is less opportunist.     

Telotroch formation, survival, and attachment in the epibiotic peritrich Zoothamnium intermedium (Ciliophora, Oligohymenophorea)

Abstract. Aspects of the life cycle of the peritrich ciliate Zoothamnium intermedium , an epibiont on calanoid copepods in the Chesapeake Bay, were investigated using host and epibiont cultures. Experiments were designed to characterize the formation, survival, and attachment of free-swimming stages (telotrochs) and to assess whether telotrochs preferentially attach to primary ( Acartia tonsa and Eurytemora affinis ) or alternate hosts from the zooplankton community (the rotifer Brachionus plicatilis , barnacle nauplii, polychaete larvae, and a harpacticoid copepod). The results showed that telotroch formation started 2 h after the death of the host, with >90% of the zooids leaving the host carapace within 7 h. Formation of telotrochs was triggered only by the death of the host, failing to occur when the host was injured or unable to swim. Telotrochs failed to attach to non-living substrates and survived for only 14 h in the absence of host organisms, suggesting that members of Z. intermedium are obligate epibionts. Attachment success decreased with telotroch age, indicating that colonization success in nature may strongly depend on the ability to find a suitable host in a short period of time. Individuals exhibited no preferences in colonizing juvenile or adult stages of A. tonsa or E. affinis . While telotrochs were able to colonize barnacle nauplii and the harpacticoid copepod in the absence of individuals of A. tonsa or E. affinis , they did not attach to the rotifers or polychaete larvae. Telotrochs preferentially colonized individuals of A. tonsa when in the presence of other non-calanoid host species.     

Effects of reduced salinity on survival, growth, reproductive success, and energetics of the euryhaline polychaete Capitella sp. I

Physiological adjustment to water of reduced salinity requires energy expenditure. In this study we sought to determine the fitness costs associated with such adjustment in the euryhaline polychaete Capitella sp. I, and the extent to which such costs could be explained by increased rates of energy expenditure. In a series of experiments conducted at 20 degrees C, salinity was reduced from 30 per thousand to either 25, 20, 15, 12, or 10 per thousand within 72 h after the larvae had been induced to metamorphose. Juveniles were reared on fine, organic-rich sediment. Over the next 15-30 days, we determined survival, growth, fecundity, and rates of respiration and feeding (via fecal pellet production). Larval salinity tolerance was also determined. Juvenile survival at salinities as low as 12-15 per thousand was comparable to that at 30 per thousand. The lower limit of salinity tolerance was 10-12 per thousand at 20 degrees C for both larvae and juveniles. Juveniles grew significantly more slowly at 12-15 per thousand in six of the seven experiments. Fecundity, however, was generally highest at intermediate salinities of 20-25 per thousand, and comparable at 30 and 15 per thousand. No individuals released embryos at 12 per thousand over the approximately 30-day observation periods in any of the three experiments in which the worms were reared at this low salinity. Reduced growth rates were not explained by differences in rates of respiration at different salinities: at reduced salinity, respiration rates were either statistically equivalent to (P>0.10) or significantly below (P<0.05) those recorded for animals maintained at 30 per thousand. Lower growth rates at lower salinities were best explained by reduced feeding rates. Further studies are required to determine whether digestive efficiency, growth hormone concentrations, or reproductive hormone concentrations are also altered by low salinity in this species.     

Differences in the abundance and distribution of copepods in two estuaries of the Basque coast (Bay of Biscay) in relation to pollution

The abundance and spatial distribution of copepod species werecompared in the euhaline region of the polluted estuary of Bilbao[mean biological oxygen demand (BOD): 49748.05 kg day^–1in 1996] and the unperturbed estuary of Urdaibai. Sampling wasperformed at fixed salinity sites, where data of temperature,dissolved oxygen saturation, particulate organic matter, Secchidisk depth and chlorophyll were also obtained. Differences betweenthe estuaries and within the estuaries for environmental variablesand copepod abundances were tested statistically. The dominantspecies Acartia clausi and Paracalanus parvus differed significantlyin abundance between estuaries, and most of neritic speciesdiminished more drastically with decreasing salinity in Bilbaoby the effect of pollution. The different responses observedamong species in relation to pollution and water desalinationare discussed. The lack of the brackish-water species in Bilbaoindicated that water quality worsening upward the estuary ofBilbao not only limited the penetration of neritic species butalso prevented the development of autochthonous estuarine species.At the outer euhaline region of Bilbao, however, pollution wasfound to be low enough to enhance the development of tolerantneritic species that are favoured under moderate pollution conditions.Results indicate that comparisons of copepod abundances anddistributions with salinity in estuaries may be a useful toolto evaluate the health of the different estuarine pelagic habitats.     

Nitrogen metabolism and excretion in the aquatic chinese soft-shelled turtle, Pelodiscus sinensis, exposed to a progressive increase in ambient salinity

This study aimed to determine effects of 6-day progressive increase in salinity from 1 per thousand to 15 per thousand on nitrogen metabolism and excretion in the soft-shelled turtle, Pelodiscus sinensis. For turtles exposed to 15 per thousand water on day 6, the plasma osmolality and concentrations of Na+, Cl- and urea increased significantly, which presumably decreased the osmotic loss of water. Simultaneously, there were significant increases in contents of urea, certain free amino acids (FAAs) and water-soluble proteins that were involved in cell volume regulation in various tissues. There was an apparent increase in proteolysis, releasing FAAs as osmolytes. In addition, there might be an increase in catabolism of certain amino acids, producing more ammonia. The excess ammonia was retained as indicated by a significant decrease in the rate of ammonia excretion on day 4 in 15 per thousand water, and a major portion of it was converted to urea. The rate of urea synthesis increased 1.4-fold during the 6-day period, although the capacity of the hepatic ornithine urea cycle remained unchanged. Urea was retained for osmoregulation because there was a significant decrease in urea excretion on day 4. Increased protein degradation and urea synthesis implies greater metabolic demands, and indeed turtles exposed to 15 per thousand water had significantly higher O2 consumption rate than the freshwater (FW) control. When turtles were returned from 15 per thousand water to FW on day 7, there were significant increases in ammonia (probably released through increased amino acid catabolism) and urea excretion, confirming that FAAs and urea were retained for osmoregulatory purposes in brackish water.     

Space and time distribution of zooplankton in a Mediterranean lagoon (Etang de Berre)

In the Berre lagoon, a large brackish and swallow area near Marseille, the environmental factors (temperature, salinity, oxygen, suspended particulate matter and chlorophyll) generally display strong space and time variations. The rotifer Brachionus plicatilis and the copepod Acartia tonsa constitute the bulk of the zooplankton population during all the year. Their space and time distributions were studied in 23 stations distributed all over the lagoon, during four seasonal cruises (February, June, October, November), at surface and bottom layers. There is no marked difference in the horizontal and vertical distribution of the two species, (except in November when rotifers were prevailing in surface and copepods at depth) and in their time occurence. When the four series of data are pooled, correlation analysis show that A.tonsa is positively correlated with temperature, salinity and seston and negatively to oxygen and chlorophyll. B. plicatilis is positively correlated with temperature and seston, but also with chlorophyll, while salinity has a negative effect. The specific eggs number of both species is chlorophyll dependent. Considering seasonal cruises separately, some differences appear in the sense or the significance of these different correlations. The respective distribution of the two species is only partly dependent on the variation of the environmental factors: most of the variance remains unexplained, as indicated by the result of a stepwise multiple regression analysis using the most significant factors (temperature, salinity and oxygen explain 33 to 42% of the variance in Acartia, while temperature and salinity explain 27 to 28% of the variance in Brachionus). Thus, internal behavioral factors could also play a role in the distribution of organisms, particularly in some cases of aggregations of organisms observed during this study. As the two species occupied the same space habitat most of the year, they are potentially in competition for food. A way to optimize the food utilization could be the time separation of their feeding activity, nocturnal in Acartia and diurnal in Brachionus. Another way could be selective feeding upon food particles depending on their size (Brachionus being able to use finer particles than Acartia) or their quality (Brachionus being more herbivorous than Acartia) as demonstrated in some grazing experiments carried out in parallel.     

Copepods induce paralytic shellfish toxin production in marine dinoflagellates

Among the thousands of unicellular phytoplankton species described in the sea, some frequently occurring and bloom-forming marine dinoflagellates are known to produce the potent neurotoxins causing paralytic shellfish poisoning. The natural function of these toxins is not clear, although they have been hypothesized to act as a chemical defence towards grazers. Here, we show that waterborne cues from the copepod Acartia tonsa induce paralytic shellfish toxin (PST) production in the harmful algal bloom-forming dinoflagellate Alexandrium minutum. Induced A. minutum contained up to 2.5 times more toxins than controls and was more resistant to further copepod grazing. Ingestion of non-toxic alternative prey was not affected by the presence of induced A. minutum. The ability of A. minutum to sense and respond to the presence of grazers by increased PST production and increased resistance to grazing may facilitate the formation of harmful algal blooms in the sea.