Invaders Ctenophores Mnemiopsis leidyi (A. Agassiz) and Beroe ovata Mayer 1912, and Their Influence on the Pelagic Ecosystem of Northeastern Black Sea

We analyzed the state of pelagic ecosystem of northeastern Black Sea affected by invasion of a new settler Beroe ovata in 1999–2001. Development of B. ovata considerably decreased the population of another invader, Mnemiopsis leidyi, that deformed the Black Sea ecosystem for over a decade. Reduction of M. leidyi population limited its influence on the ecosystem and, consequently, we observed recovering of the main components of the Black Sea pelagic ecosystem—zooplankton and fish as well as their eggs and larvae. The relationships between annual and seasonal variability of the population development and size of the both invaders M. leidyi and B. ovata are discussed.     

Somatic organic content of the ctenophores <Emphasis Type="Italic">Mnemiopsis leidyi</Emphasis> (Ctenophora: Lobata) and <Emphasis Type="Italic">Beroe ovata</Emphasis> (Ctenophora: Beroida) in early ontogenetic stages

The organic matter content in the eggs and early larvae of the ctenophores Mnemiopsis leidyi and Beroe ovata from the Black Sea was determined using the adapted microtechnique of dichromate oxidation. The content of organic matter in the eggs of M. leidyi (0.25 μg/indiv.) was 5 times less than in B. ovata (1.28 ± 0.29 μg/indiv.). The somatic content of organic matter was 0.25 ± 0.09 μg/indiv. (25.1 ± 8.3 μg/mg, wet wt) for 2-day-old larvae of M. leidyi (0.2–0.3 mm in body length) and 1.37 ± 0.19 μg/indiv. (67.1 ± 5.7 μg/mg wet wt) for larvae of B. ovata (0.4 mm in body length). The specific organic content of larvae of both species steadily decreased with an increase in ctenophore body size and weight, approaching 3–4 μg/mg of wet weight for 2 mm specimens of M. leidyi and 3–5 μg/mg of wet weight for 6 mm B. ovata. The specific organic content of early larvae was 20–30 times higher than that of adult ctenophores. The results of this investigation could be useful in the evaluation of the energy budget for somatic growth and generative production in these species. Calculations indicate that with specific wet weight growth rates of 0.43/day for M. leidyi larvae and 0.29/day for B. ovata larvae, their true organic increases are respectively 30 and 38% less, i.e., no more than 0.31/day for the former and 0.18/day for the latter species.     

Morphology and dynamic behavior of anal pores during defecation in the ctenophore Pleurobrachia pileus

Defecation in the lobate ctenophore Mnemiopsis leidyi was recently shown to occur periodically with an ultradian rhythm through a single transient anal pore which suddenly appeared, expelled waste, and disappeared afterward. To discover whether this novel method of defecation occurs in other kinds of ctenophores, I examined individuals of Pleurobrachia pileus and Beroe cucumis. Both ctenophores were found to have two identical and permanent anal pores as described in the scientific literature and textbooks. In P. pileus, both anal pores commonly participated in a defecation, but they did so asynchronously with independent and irregular opening and closing kinetics. Individuals of P. pileus defecated with an ultradian rhythm. Closed anal pores in P. pileus and B. cucumis consisted of a continuous ectodermal epithelium overlying a continuous endodermal epithelium with a cup-shaped group of thickened endodermal cells bearing a tuft of cilia which beats into the anal cavity. The rims of opening or closing pores were smooth and uniform without encircling muscles or fibers. This morphology and the continuity of the epithelial layers between defecations suggest that anal pores may not operate by a contractile sphincter, but by a reversible ring of tissue fusion between apposed ectodermal and endodermal epithelia to create an adjustable hole to expel waste.     

Avoidance of hydrodynamically mixed environments by <Emphasis Type="Italic">Mnemiopsis leidyi</Emphasis> (Ctenophora: Lobata) in open-sea populations from Patagonia,Argentina

Biomass distributions of the ctenophore, Mnemiopsis leidyi, were collected during a week-long survey program in a tidal front along the Patagonian shelf in December 1989. Average ctenophore biomass concentrations varied significantly along a north–south gradient and in stratified compared to unstratified waters. The relative vertical distribution of M. leidyi biomass appeared to be constrained by surface levels of vertical shear. Vertical distributions of ctenophore biomass were highly variable at low levels of vertical shear (<4 s⁻¹) at the surface, but at higher levels of surface vertical shear ctenophores occurred deeper in the water column where shear levels were lower. These results indicate that physical conditions are important factors influencing the distribution of M. leidyi along the Patagonian shelf during summer months.     

Feeding by larval and post-larval ctenophores on microzooplankton

Feeding by the coastal ctenophorc, Mnemiopsis leidyi, on microplanktonwas investigated. Larval ctenophores (tentaculate stage) grewbest and had the highest survival rates when offered a mixtureof ciliates and copepod nauplii. Larvae did not survive whenoffered phytoplankton alone. Clearing of planktonjc ciliatesby post-larval ctenophores was a function of the ciliate speciesand the size of the predator. Removal of small ciliates (<20µm in size) and phytoplankton was negligible. Small post-larvalctenophores (volume <4 cm³) had higher biovolume-specificclearing rates (0.5–1.5 1 cm^–3 day^–1) thandid larger ctenophores fed the same ciliate species. Duringin situ incubations, adult M. leidyi removed ciliates, rotifersand copepod nauplii from natural microplankton assemblages.The data indicate that non-crustacean microzooplanlctoo arean important component of the diet of larval and post-larvallocate cteoophores, particularly when copepod standing stocksare low.     

Predator-induced vertical behavior of a ctenophore

Although many studies have focused on Mnemiopsis leidyi predation, little is known about the role of this ctenophore as prey when abundant in native and invaded pelagic systems. We examined the response of the ctenophore M. leidyi to the predatory ctenophore Beroe ovata in an experiment in which the two species could potentially sense each other while being physically separated. On average, M. leidyi responded to the predator’s presence by increasing variability in swimming speeds and by lowering their vertical distribution. Such behavior may help explain field records of vertical migration, as well as stratified and near-bottom distributions of M. leidyi.     

Specific features of the feeding of larval fish of the families Blenniidae and Gobiidae in relation to changes in the coastal plankton community of the Black Sea

Data on the feeding of larvae of mass Black Sea fish species of the families Blenniidae and Gobiidae with a length of 2.2–7.0 mm from coastal waters of the Crimea (Sevastopol) are presented. Despite the tendency for an improvement in the feeding of larval fish, Mnemiopsis leidyi, in the case of a prolonged staying in the plankton in mass amounts in the absence of Beroe ovata, exerts a negative effect on the food resources and the survival of larvae. This is evidenced by the indices of food consumption and the proportion of larvae with empty intestines.     

Defecation by the ctenophore Mnemiopsis leidyi occurs with an ultradian rhythm through a single transient anal pore

Defecation in the ctenophore Mnemiopsis leidyi is a stereotyped sequence of effector responses that occur with a regular ultradian rhythm. Here I used video microscopy to describe new features and correct previous reports of the gastrovascular system during and between defecations. Contrary to the scientific literature, individuals defecated through only one of the two anal canals which possesses the only anal pore. The anal pore was not visible as a permanent structure as depicted in textbooks, but appeared at defecation and disappeared afterward. Time intervals between repeated defecations in individual animals depended on body size, ranging from ~10 min in small larvae to ~1 hr in large adults. Differential interference contrast microscopy revealed that both the opening and closing of the anal pore resembled a reversible ring of tissue fusion between apposed endodermal and ectodermal layers at the aboral end. Individuals of M. leidyi thus appear to have an intermittent anus and therefore an intermittent through‐gut that reoccur at regular intervals. The temporality of a visible anal pore in M. leidyi is novel, and may shed light on the evolution of a permanent anus and through‐gut in animals. In addition, mirror image dimorphism of the diagonal anal complex occurs in larval ctenophores but not in adults, indicating developmental flexibility in diagonal symmetry of the anal complex.     

The first occurrence of the ctenophore <Emphasis Type="Italic">Mnemiopsis leidyi</Emphasis> in the North Sea

After the discovery of large densities of Mnemiopsis leidyi in the Baltic Sea near Kiel by Javidpour et al. (First record of Mnemiopsis leidyi A. Agassiz 1865 in the Baltic Sea, 2006) in October 2006, we investigated the gelatinous zooplankton in the North Sea near Helgoland and recorded Mnemiopsis leidyi for the first time in the North Sea, albeit in much lower densities than those recorded in the Baltic Sea.     

Research into bioluminescence of the Black Sea ctenophores Pleurobrachia pileus O.F. Müller, 1776

The work presents the findings of the laboratory and in situ studies of ctenophore Pleurobrachia pileus O.F. Müller, 1776 which have shown that this species has bioluminescent properties. These organisms were considered non-luminous before. P. pileus bioluminescence was studied on board RV Professor Vodyanitsky during its 116th voyage. Sampling live organisms was preceded by probing with the Salpa MA+ probe to register the daily maximum glow in redoxcline, which in this zone was recorded, as a rule, in the depth range of 60–70 m, where dense clusters of P. pileus were formed at that time. The samples of ctenophores were taken by a Bogorov–Rass plankton net. After the net was closed, it was lifted to the surface at a speed of 0.4–0.5 m s⁻¹. It was shown that only at a temperature not exceeding 14°C, the P. pileus remained alive for 2–3 days. The data provided indicate that the temperature above 14°C is close to the maximum permissible for P. pileus; therefore, chemical and mechanical stimulation experiments were carried out at this temperature (14°C) to agitate ctenophores luminescence. Though, the nature of their signal was significantly different. The total percentage of luminous organisms from the entire catch was 32.43%, which unequivocally proves that P. pileus glows and makes a significant contribution to the intensity of the glow at great depths in redoxcline.     

Spatio-temporal overlap of the alien invasive ctenophore <Emphasis Type="Italic">Mnemiopsis leidyi</Emphasis> and ichthyoplankton in the Bornholm Basin (Baltic Sea)

In 2007 the alien invasive ctenophore Mnemiopsis leidyi A. Agassiz 1865 was recorded for the first time in the Bornholm Basin, an area which serves as important spawning ground for Baltic fish stocks. Since M. leidyi is capable of preying upon early life stages of fish and further might act as food competitor for fish larvae, it is of major concern to investigate the potential threat that this non-indigenous species poses to the pelagic ecosystem of the Baltic Sea. The present study investigates the temporal and spatial overlap of M. leidyi with eggs and larvae of Baltic cod (Gadus morhua L.) and sprat (Sprattus sprattus L.) in order to assess the potential impact of this new invader on two of the most important Baltic fish stocks. Results show variable inter-seasonal distribution and overlap dynamics and thus different seasonal threat-scenarios for the early life stages of cod and sprat. The spatial overlap between M. leidyi and ichthyoplankton was low for most of the period observed, and we conclude that M. leidyi presently does not have a strong impact. However, we detected situations with high overlaps, e.g. for sprat larvae and cod eggs in spring. As the population dynamics of M. leidyi in the central Baltic are not yet fully understood, a future population explosion of the alien ctenophore with possible effects on fish recruitment cannot be ruled out. Furthermore, a possible shift in peak spawning of cod to the early season, when ctenophore abundances were relatively high, might increase the impact of M. leidyi on cod.     

Feeding efficiency of the larval ctenophore Mnemiopsis leidyi A. Agassiz (Ctenophora, Lobata)

Larval stages of the ctenophore Mnemiopsis leidyi rely on metazoanprey, such as Acartia tonsa nauplii and copepodites, to supporthigh growth rates. However, M. leidyi larvae <0.5 mm (totallength) had low retention efficiencies (REs) (proportion ofencountered prey actually ingested), 5.78 ± 2.6% (mean± SE), of nauplii and were often damaged by their encounters.REs of nauplii rapidly increased, 38.94 ± 3.73%, as larvaegrew to a size of     

Impact of hypoxia conditions on the Mnemiopsis leidyi A. Agassiz, 1865 bioluminescence

The findings of the study on the impact of hypoxia on the glow of the Black Sea ctenophore Mnemiopsis leidyi A. Agassiz, 1865 of three size groups (20–30, 30–45, and 45–60 mm) were obtained under experimental conditions. Peculiarities of ctenophore bioluminescence were studied during mechanical and chemical stimulation under the conditions of normoxia (at an oxygen concentration of 5.6–6.7 mg O₂ L⁻¹), moderate hypoxia (2.5–2.8 mg O₂ L⁻¹), and acute hypoxia (1.2–1.5 mg O₂ L⁻¹). An increase in the amplitude and energy of luminescence of the ctenophores mechanically and chemically stimulated was observed at an oxygen concentration of 1.2–1.5 mg O₂ L⁻¹ (acute hypoxia) in two size groups in the lobate form (30–45 and 45–60 mm). The inhibition of amplitude, energy, and duration of the signal was registered in M. leidyi ctenophores at the transitional stage from larva to the lobate form under conditions of acute hypoxia. It was noted that in normoxia, the values of the amplitude and energy of the bioluminescent signal of M. leidyi increase along with a size growth of an individual. This phenomenon was observed both during mechanical and chemical stimulations. Under conditions of acute hypoxia, this trend was mainly preserved. The universality of the relation between the bioluminescence of the organisms and their bioenergetics is obvious. The bioluminescent system of ctenophores has the role of an antioxidant system and is engaged in the neutralization of reactive oxygen species (ROS), that is the process during which photons are emitted. The response of the bioluminescent system to a decrease in oxygen concentration can be associated with an increase in the production of ROS that provides high values of the ctenophore luminescence under hypoxic conditions.     

Digenea parasites of jellyfish and ctenophores of the southern Atlantic

Parasites of planktonic cnidarians and ctenophores in the southern Atlantic Ocean are little known. The aim of this study was to describe three new metacercariae from jellyfish and ctenophores, and assess the importance of the gelatinous zooplankton as intermediate hosts in the life history of digeneans. During examination of zooplankton in Argentine Sea for digeneans that mature in fishes, two species of jellyfish (Phialidium sp. and Liriope tetraphylla Chamiso & Eysenhardt, 1821), and one ctenophore (Mnemiopsis mccradyi Mayer, 1900) were analyzed for parasites. The samples were obtained in Mar del Plata. Three metacercariae belonging to Faustulidae, Lepocreadiidae and Hemiuridae are described. The prevalence (percent of hosts infected) varied from 1.4–30% and the range of intensity (number of individuals of a parasite species in a single infected host) was from 1 to 30 for the different metacercariae. Given the important position of free-swimming cnidarians and ctenophores in the marine food web, and the great number of fishes that have been found with these organisms in their digestive tracts, their importance in the life histories of digeneans should not be underrated.     

Laboratory studies of predation by the ctenophore Mnemiopsis leidyi on the early stages in the life history of the bay anchovy, Anchoa mitchilli

The lobate ctenophore, Mnemiopsis leidyi, consumed eggs andlarvae of the bay anchovy, Anchoa mitchilli, in laboratory experiments.This ctenophore exhibited a type I functional response to increasesin egg densities without reaching saturation at high prey densities.Clearance rate increased with increasing experimental containervolume. There was a 3-fold increase in the volume of water clearedby 2.0–2.5-cm ctenophores and a >5-fold increase for4.5–5.0-cm ctenophores in 15–1 versus 100–200–1containers. Clearance rate was dependent on tenophore lengthbut was probably underestimated for the larger animals due tocontainer effects. The presence of various densities of alternateprey, Acartia hudsonica or Anemia sp. nauplii, in addition toAnchoa mitchilli eggs did not affect the clearance rates onthe eggs alone. Comparison of clearance rates of 2.0–2.5-cmctenophores on various ages of starved and fed bay anchovy larvaeindicated that predation may be higher on yolk-sac larvae thanon eggs but decreases as the larvae grow. After 3 days posthatch starved anchovy larvae become more vulnerable to predationthan fed larvae. The ctenophore, M.leidyi has the potentialto inflict substantial predation pressure on early stages inthe life history of bay anchovy. ¹ Present address: University of Maryland, Center for Environmentaland Estuarine Studies, Chesapeake Biological Laboratory, POBox 38, Solomons, MD 20688-0038, USA     

Blooms of the invasive ctenophore, <Emphasis Type="Italic">Mnemiopsis</Emphasis> <Emphasis Type="Italic">leidyi</Emphasis>, span the Mediterranean Sea in 2009

Blooms of the invasive ctenophore, Mnemiopsis leidyi, occurred in 2009 along the Mediterranean Sea coasts of Spain and Israel. This voracious zooplanktivore spread throughout the Black Sea basin after its introduction in the early 1980s, throughout northern European coastal waters, and now occurs throughout the Mediterranean Sea. M. leidyi occurred throughout the summer along the entire Catalan Spanish and Israeli coasts in 2009. Those locations had high temperatures (18–26°C) and salinities (37–38) during the blooms. The patterns of abundance of large jellyfish along the Catalan coast were unusual in 2009, with low numbers during July, August, and September when ctenophores were abundant. Small populations of those potential predators and food competitors of M. leidyi could have contributed to the ctenophore bloom. The identity of the ctenophores from Spain and Israel was confirmed as M. leidyi by molecular analysis based on DNA sequencing of the nuclear internal transcribed spacer (ITS) regions. This is the first molecular confirmation of M. leidyi in the Mediterranean Sea. Most ctenophores had an ITS genotype previously found in M. leidyi from other invaded regions (the Black, Azov, and Mediterranean seas), as well as native regions in the United States, suggesting common ancestry. Based on the circulation patterns of Mediterranean surface waters and shipping activities, we conclude that the spread of M. leidyi in the Mediterranean probably resulted from re-introductions by ballast water transport and subsequent distribution by currents. We also conclude that the near-simultaneous blooms in opposite ends of both the Mediterranean basins indicate that M. leidyi is resident around the Mediterranean. We discuss environmental conditions, food, and predators of M. leidyi in both regions that would influence the future effects of this voracious consumer on the pelagic food web of the Mediterranean Sea.     

The role of hyperiid parasites as a trophic link between jellyfish and fishes

The trophic interactions between the scyphozoan medusa Chrysaora plocamia and the palm ruff Seriolella violacea were investigated off northern Chile and showed that large numbers of hyperiid amphipods parasitizing the medusa may channel energy back to the fishes, which feed on the parasites. The biomass of hyperiids eaten by the fish was a function of the biomass of hyperiids parasitizing the medusa. This temporally available food supply may enhance fish recruitment. The large number of hyperiids parasitizing diverse jellyfish species represents a missing trophic link in current efforts to understand the effects of jellyfish blooms on marine food webs.     

Ctenophore-zooplankton-phytoplankton interactions in Narragansett Bay, Rhode Island, USA, during 1972-1977

Plankton dynamics at a station in lower Narragansett Bay, RIare compared for six summer and fall seasons, 1972–1977.In four of these years, initiation of the summer pulse of thectenophore Mnemiopsis leidyi was accompanied by a rapid declinein zooplankton abundance and a summer phytoplankton bloom. Terminationof the phytoplankton bloom coincided with depleted ctenophoreabundance and increased zooplankton biomass in two of the years.Yearly variations in the summer abundance of the diatom Skeletonemacostatum were positively related to the magnitude of the ctenophorepulse. The magnitude of ctenophore population was related tothe zooplankton biomass present at the start of the pulse. Theserelationships, the timing and magnitude of the plankton eventssuggest that M. leidyi regulated summer zooplankton and phytoplanktondynamics. Ctenophores may control phytoplankton blooms indirectlythrough their predation on herbivorous zooplankton and directlyby the nutrient excretion accompanying such grazing. This evidencethat a planktonic carnivore two trophic steps removed from thephytoplankton regulates the latter's dynamics in NarragansettBay is analogous to reported regulation of benthic algal (kelp)dynamics by the sea otter, lobster and various crabs throughtheir predation on herbivorous sea urchins. The factors responsiblefor the seasonal decrease in ctenophores remain unresolved;ctenophore predators on Mnemiopsis are absent in NarragansettBay. Infection by the vermiform larval anemone, Edwardsia lineata,grazing by the butterfish, Peprilus triacanthus, and changesin food availability, temperature and salinity likewise do notexplain this disappearance.     

Primary inhibition: a mechanism for sudden stoppage of metachrony in ctenophores

The ctenophores Beroë cucumis and Pleurobrachia pileus exhibit rapid stoppage of comb plate beating, without accompanying muscular contraction, in response to an orally applied mechanical stimulus. This phenomenon, termed ‘primary inhibition’ by Göthlin, was re-examined by high-speed video microscopy and intracellular recording. The most remarkable features of this event were that (1) inhibition was associated with only one or two comb plates in the row, (2) inhibition occurred nearly anywhere in the ciliary beat cycle, (3) the inhibited plate acted as a mechanical blockade to the propagation of additional metachronal waves, and (4) a single depolarizing post-synaptic potential occurred nearly simultaneously with comb plate inhibition. B. cucumis and P. pileus have evolved a neurally controlled behavior to rapidly stop comb plate metachrony.

     

Associations between gelatinous zooplankton and hyperiid amphipods (Crustacea: Peracarida) in the Gulf of California

Hyperiid amphipods are pelagic crustaceans that live associated with gelatinous zooplankton including medusae, ctenophores, siphonophores, and salps. Standard plankton sampling disrupts natural associations, so the most reliable way to determine an association is through direct observation of the organisms in their environment. The planktonic fauna of the Gulf of California dwelling between 10 and 3000 m was surveyed using SCUBA diving and a remotely operated submersible (ROV) during March 2003. Here we report our observations on a total of 14 symbiotic associations found between the hyperiid amphipods and various taxa of gelatinous zooplankton. We found parental care behavior in a group of amphipods (Oxycephalidae) in which this phenomenon has not been previously reported. For two hyperiid species, Euthamneus rostratus and Vibilia australis, we present the first information on their symbiotic relations. Additional hosts were discovered for other well-known and widely distributed hyperiid species (i.e. Brachyscelus crusculum, Hyperoche medusarum). Photographic evidence of some of these interactions is included in this contribution. This is the first survey of these relationships in the Gulf of California, and many aspects of the ecology and biology of these symbioses remain to be studied.