Protistan epibionts of the ctenophore Mnemiopsis mccradyi Mayer

Mnemiopsis mccradyi, a common coastal ctenophore, was observed to bear two distinct, exclusive assemblages of protistan epibionts. The mobiline peritrich, Trichodina ctenophorii (Estes et al., 1997), and small Flabellula-like gymnamoebae inhabited only the surface of the comb plates. By contrast, small Vexillifera-like gymnamoebae and large Protoodinium-like dinoflagellates were found on the ectoderm. The relationship of the epimicrobial protists with their host varied from possible mutualism (vexilliferids) to commensalism (trichodinids) to parasitism (flabellulids and protoodinids). Trichodinids may benefit from comb plate attachment by enhanced food capture. Although they did not obviously impair comb plate beating, they did distort the surface and appear to produce fissures in the comb plate surface, which could provide inroads for more severe comb plate damage by amoebae. By contrast, when flabellulid amoebae occurred in very high surface densities (up to 5000 mm^–2), they clearly damaged comb plates by eroding the surface. Where flabellulid pseudopodia invaded the comb plate, we observed local degradation of comb plate cilia, as evidenced by central pair disorientation and plasma membrane perturbation and overt phagocytosis of comb plate cilia. Ectodermal vexilliferids, which occurred at much lower densities, did not appear to have any degradative impact on the ctenophore. By contrast, clusters of ectodermal protoodinids were found in localized depressions most likely caused by invasive phagocytosis. The impact of the protistan assemblages on ctenophore populations is unclear, but under conditions of severe infestation they might depress ctenophore population density.     

The ontogeny and maintenance of adult symmetry properties in the ctenophore, Mnemiopsis mccradyi

Ctenophores are biradially symmetrical animals. The body is composed of four identical quadrants which are organized along an oral-aboral axis. Most species have eight comb rows, two tentacles, and an apical organ (located on the aboral surface). During embryogenesis there is a fixed pattern of cleavage, a precocious specification of blastomere developmental potential, and an inability to regulate for portions of the embryo that have been removed. When blastomeres are separated at the two-cell stage each blastomere develops into a "half-animal" with four comb rows, one tentacle, and half an apical organ. In contrast, adult ctenophores regenerate readily. When an adult ctenophore is cut in half to produce "half-animals," in most cases each half regenerates the missing half. In some cases, however, bisected animals remain as "half-animals" which repair the wound site but do not replace all of the missing structures. When animals are cut in half along the tentacular or esophageal axis at different stages of embryogenesis a transition period is detected when the capacity for adult regeneration begins. This transition occurs at the time when the formation of the apical organ is complete and comb row function becomes coordinated. Embryos bisected prior to this time remain as "half-animals" even after growing to large reproductive sizes, while animals bisected after the transition period usually regenerate the missing structures within 2-3 days. When adult "half-animals" (produced by bisection either before or after the transition period) are cut into "quarter-pieces," the pieces regenerate to form either "half-animals" or whole animals. Thus, "half-animals" produced prior to the transition period--although they failed to undergo embryonic regulation--have not irreversibly lost the capacity to form whole animals if challenged to regenerate during adult stages. When aboral blastomeres destined to form the apical organ, tentacles, and comb rows are removed from early cleavage stages (prior to the transition period), the embryo does not form these structures at the appropriate time. However, the resulting deficient adults spontaneously form these structures from remaining blastomere lineages soon after hatching. These experiments suggest that as long as some quadrant-specific cells of the oral pole are present at the time of the transition period, the structures of that quadrant will be spontaneously replaced during the adult period.(ABSTRACT TRUNCATED AT 400 WORDS)     

A novel cilia-based feature within the food grooves of the ctenophore Mnemiopsis mccradyi Mayer

We describe a novel compound ciliary structure (g-cilium) from the food groove of the lobate ctenophore Mnemiopsis mccradyi. G-cilia are small, flat compound ciliary organelles that are oriented with their tips pointing toward the mouth. Typically three to four rows of g-cilia line the inner surface of the tentacular groove, which together with the transport groove, make up the food groove. G-cilium cells are 11.4 m long and 4.2 m wide at the g-cilium base. The g-cilium itself is 3.4 m long and tapers to a flat, sharp tip. G-cilia are not motile but are surrounded by many hundreds of smaller, actively motile cilia that beat with orally-directed effective strokes. G-cilia contain 50 conventional `9+2' cilia embedded in a fibrous core that arises from the cell body. In addition, g-cilia contain mitochondria, thousands of small membrane-bounded vesicles and rod bacteria. G-cilia basal bodies are anchored by large, strongly-banded rootlets that extend approximately the entire length of the cell. G-cilia may have organizational, sensory and/or secretory function within the feeding apparatus. Their placement strongly suggests that they play critical roles in feeding. They may enhance the efficiency of prey capture and so contribute to M. mccradyi's well-known voracious appetite. By enhancing prey capture they probably play a critical role in the capacity of this organism to follow prey dynamics, so contributing to dense blooms in mid-late summer in coastal regions.     

The development of bioluminescence in the ctenophore Mnemiopsis leidyi

The photocytes of the ctenophore Mnemiopsis have a discontinuous distribution along the radial canal between the sites where the comb plate cilia cells are located on the side of the canal which contains the testes. They are separated from the lumen of the canal by a population of gastric cells. Cytologically these cells are characterized by a condensed nucleus and cytoplasm which stains lightly with basophilic dyes.The ability of the ctenophore embryo to produce light appears at the developmental stage when the comb plate cilia first begin to grow out. At this stage four light-producing areas are present; each area corresponds to one quadrant of the adult animal. At the sites of light production, a population of cells can be identified that have some of the cytological properties of the photocytes of the adult animal. Within 8–10 hr after light production begins there is a 10-fold increase in the amount of light produced by an embryo and a cytological maturation of its photocytes; during this time period there is no increase in photocyte number. At about the time the embryo begins to feed, each light-producing region splits into two regions, each of which corresponds to a radial canal.During the process of embryogenesis the photocyte cell lineage is first segregated from non-photocytes at the differential division which gives the 8-cell stage embryo. The M macromere lineage goes on to form photocytes, but the E macromere lineage does not. The M macromeres form a micromere at the aboral pole of the embryo at each of the next two cleavages; during these cleavages the potential for photocyte differentiation continues to segregate with the M macromeres. During the division which gives the 64-cell stage the M macromeres divide equally; the potential for photocyte differentiation segregates with the M macromeres nearest the oral-aboral axis. M macromeres which are isolated from the embryo at the 8-, 16-, or 32-cell stage of development will continue to cleave as though they were part of a normal embryo and differentiate to form photocytes.The events that are responsible for the differential division during the formation of the 8-cell stage embryo have been studied by centrifuging eggs to produce fragments of different cytoplasmic composition. Egg fragments which contain only cortical cytoplasm differentiate comb plate cilia cells, but do not produce photocytes. Cortical fragments with a small amount of yolk differentiate comb plate cilia cells and photocytes. Both the M and E macromeres from cortical fragments with no yolk produce comb plate cilia. Only M macromeres containing yolk form photocytes; if an M macromere forms photocytes it does not form comb plate cilia.     

Ionic currents of smooth muscle cells isolated from the ctenophore Mnemiopsis

The ionic currents of smooth muscle cells isolated from the ctenophore Mnemiopsis were examined by using conventional two-electrode voltage clamp and whole-cell patch clamping methods. Several separable currents were identified. These include: (1) a transient and (2) a steady-state voltage-activated inward current; both are tetrodotoxin (TTX) and saxitoxin (STX) insensitive, partly reduced by decreasing external Ca2+ or Na+ or by addition of 5 mM Co2+, D-600 or verapamil and are totally blocked with 5 mM Cd2+; (3) an early, transient, cation-dependent, outward K+ current (IKCa/Na); (4) a transient, voltage-activated, outward K+ current provisionally identified as IA; (5) a delayed, steady-state, voltage-activated outward K+ current (IK) and (6) a late, transient, outward K+ current which is blocked by Cd2+ and evident only during long voltage pulses. Despite their phylogenic origin, most of these currents are similar to currents identified in many vertebrate smooth and cardiac muscle preparations, and other excitable cells in higher animals.     

Extreme mitochondrial evolution in the ctenophore Mnemiopsis leidyi: Insight from mtDNA and the nuclear genome

Recent advances in sequencing technology have led to a rapid accumulation of mitochondrial DNA (mtDNA) sequences, which now represent the wide spectrum of animal diversity. However, one animal phylum--Ctenophora--has, to date, remained completely unsampled. Ctenophores, a small group of marine animals, are of interest due to their unusual biology, controversial phylogenetic position, and devastating impact as invasive species. Using data from the Mnemiopsis leidyi genome sequencing project, we Polymerase Chain Reaction (PCR) amplified and analyzed its complete mitochondrial (mt-) genome. At just over 10 kb, the mt-genome of M. leidyi is the smallest animal mtDNA ever reported and is among the most derived. It has lost at least 25 genes, including atp6 and all tRNA genes. We show that atp6 has been relocated to the nuclear genome and has acquired introns and a mitochondrial targeting presequence, while tRNA genes have been genuinely lost, along with nuclear-encoded mt-aminoacyl tRNA synthetases. The mt-genome of M. leidyi also displays extremely high rates of sequence evolution, which likely led to the degeneration of both protein and rRNA genes. In particular, encoded rRNA molecules possess little similarity with their homologs in other organisms and have highly reduced secondary structures. At the same time, nuclear encoded mt-ribosomal proteins have undergone expansions, likely to compensate for the reductions in mt-rRNA. The unusual features identified in M. leidyi mtDNA make this organism an interesting system for the study of various aspects of mitochondrial biology, particularly protein and tRNA import and mt-ribosome structures, and add to its value as an emerging model species. Furthermore, the fast-evolving M. leidyi mtDNA should be a convenient molecular marker for species- and population-level studies.     

Chemical composition and oxygen consumption rates of the ctenophore Bolinopsis infundibulum from the Gulf of Maine

Quantitative determinations of chemical composition and oxygenconsumption rates were made for a deep-living population ofthe lobate ctenophore Bolinopsis infundibulum. Animals werecollected in the Gulf of Maine with the submersible ‘Johnson-Sea-Link’during September 1989 at depths ranging from 120 to 240 m. Carbonand nitrogen contents were similar to values reported for epipelagicctenophores. Lipid and protein levels were lower than valuestypical of epipelagic ctenophores, but higher than those ofmesopelagic species. Carbohydrate was nearly an order of magnitudehigher than previously recorded for B.infundibulum. Oxygen consumptionrates ranged from 0.004 to 0.235 µl O₂ mg^–1 dryweight h^– at temperatures ranging from 5 to 7°C. Carbon-specificmetabolic rates ranged from 0.21 to 12.73 µl O₂ mg^–1C h^–1. Energy expenditures estimated from respirationdata (     

Multiple inductive signals are involved in the development of the ctenophore Mnemiopsis leidyi.

Ctenophores possess eight longitudinally arrayed rows of comb plate cilia. Previous intracellular cell lineage analysis has shown that these comb rows are derived from two embryonic lineages, both daughters of the four e(1) micromeres (e(11) and e(12)) and a single daughter of the four m(1) micromeres (the m(12) micromeres). Although isolated e(1) micromeres will spontaneously generate comb plates, cell deletion experiments have shown that no comb plates appear during embryogenesis following the removal of e(1) descendents. Thus, the m(1) lineage requires the inductive interaction of the e(1) lineage to contribute to comb plate formation. Here we show that, although m(12) cells are normally the only m(1) derivatives to contribute to comb plate formation, m(11) cells are capable of generating comb plates in the absence m(12) cells. The reason that m(11) cells do not normally make comb rows may be attributable either to their more remote location relative to critical signaling centers (e.g., e(1) descendants) or to inhibitory signals that may be provided by other nearby cells such as sister cells m(12). In addition, we show that the signals provided by the e(1) lineage are not sufficient for m(1)-derived comb plate formation. Signals provided by endomesodermal progeny of either the E or the M lineages (the 3E or 2M macromeres) are also required.     

Regeneration of ciliary comb plates in the ctenophore Mnemiopsis leidyi. i. morphology

Regeneration of missing body parts in model organisms provides information on the mechanisms underlying the regeneration process. The aim here is to use ctenophores to investigate regeneration of their giant ciliary swimming plates. When part of a row of comb plates on Mnemiopsis is excised, the wound closes and heals, greatly increasing the distance between comb plates near the former cut edges. Video differential interference contrast (DIC) microscopy of the regeneration of new comb plates between widely separated plates shows localized widenings of the interplate ciliated groove (ICG) first, followed by growth of two opposing groups of comb plate cilia on either side. The split parts of a new plate elongate as their bases extend laterally away from the ICG widening and continue ciliogenesis at both ends. The split parts of a new plate grow longer and move closer together into the ICG widening until they merge into a single plate that interrupts the ICG in a normal manner. Video DIC snapshots of dissected gap preparations 1.5–3‐day postoperation show that ICG widenings and/or new plates do not all appear at the same time or with uniform spacing within a gap: the lengths and distances between young plates in a gap are quite variable. Video stereo microscopy of intact animals 3–4 days after the operation show that all the new plates that will form in a gap are present, fairly evenly spaced and similar in length, but smaller and closer together than normal. Normal development of comb plates in embryos and growing animals is compared to the pattern of comb plate regeneration in adults. Comb plate regeneration differs in the cydippid Pleurobrachia that lacks ICGs and has a firmer mesoglea than Mnemiopsis. This study provides a morphological foundation for histological, cellular, and molecular analysis of ciliary regeneration in ctenophores. J. Morphol. 2011. © 2011 Wiley Periodicals, Inc.     

The ctenophore Mnemiopsis in native and exotic habitats: U.S. estuaries versus the Black Sea basin

The native habitats of the ctenophore, Mnemiopsis, are temperate to subtropical estuaries along the Atlantic coast of North and South America, where it is found in an extremely wide range of environmental conditions (winter low and summer high temperatures of 2 and 32 °C, respectively, and salinities of <2–38). In the early 1980s, it was accidentally introduced to the Black Sea, where it flourished and expanded into the Azov, Marmara, Mediterranean and Caspian Seas. We compile data showing that Mnemiopsis has high potentials of growth, reproduction and feeding that enable this species to be a predominant zooplanktivore in a wide variety of habitats; review the population distributions and dynamics of Mnemiopsis in U.S. waters and in the Black Sea region; and examine the effects of temperature and salinity, zooplankton availability and predator abundance on Mnemiopsis population size in both regions, and the effects of Mnemiopsis on zooplankton, ichthyoplankton and fish populations, focusing on Chesapeake Bay and the Black Sea. In both regions, Mnemiopsis populations are restricted by low winter temperatures (<2 °C). In native habitats, predators of Mnemiopsis often limit their populations, and zooplanktivorous fish are abundant and may compete with the ctenophores for food. By contrast, in the Black Sea region, no obvious predators of Mnemiopsis were present during the decade following introduction when the ctenophore populations flourished. Additionally, zooplanktivorous fish populations had been severely reduced by over fishing prior to the ctenophore outbreak. Thus, small populations of potential predators and competitors for food enabled Mnemiopsis populations to swell in the new habitats. In Chesapeake Bay, Mnemiopsis consumes substantial proportions of zooplankton daily, but may only noticeably reduce zooplankton populations when predators of Mnemiopsis are uncommon. Mnemiopsis also is an important predator of fish eggs in both locations. In the Black Sea, reductions in zooplankton, ichthyoplankton and zooplanktivorous fish populations have been attributed to Mnemiopsis. We conclude that the enormous impact of Mnemiopsis on the Black Sea ecosystem occurred because of the shortage of predators and competitors in the late 1980s and early 1990s. The appearance of the ctenophore, Beroe ovata, may promote the recovery of the Black Sea ecosystem from the effects of the Mnemiopsis invasion.     

Calcium-sensitive action potential of long duration in the fertilized egg of the ctenophore Mnemiopsis leidyi

The membrane properties of fertilized eggs of the ctenophore Mnemiopsis leidyi were studied using standard microelectrode techniques. The resting potential was approximately -80 mV, and was dependent on the extracellular K concentration. Depolarizing current injections elicited an action potential with an initial peak amplitude of +20 to +40 mV (duration about 5 sec) and a long lasting (duration 3 to 10 min) plateau phase. The depolarizing phase and the plateau phase appeared to have different ionic mechanisms. The entire action potential could be prevented by removal of extracellular Ca, but only the amplitude of the depolarizing phase, not the plateau phase, was dependent on the extracellular Ca concentration. The plateau phase was not observed in the absence of Ca, but in the presence of Ca its duration was dependent on the external Ca concentration. The data suggest that the plateau phase is activated as a consequence of Ca influx during the initial depolarizing phase. Removal of external Na resulted in only minor changes in the waveform of repolarization. The action potential was resistant to low concentrations of Mn and Cd in the presence of Ca. The role of this action potential in ctenophore development is not known, but in its waveform and duration it resembles the sperm-gated potentials that have been seen in eggs of other phyla. These experiments show ctenophore embryos to be excitable at very early stages, and suggest their utility in the study of the differentiation of cellular electrical properties.     

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.     

Life-stage dependent, in situ dietary patterns of the lobate ctenophore Mnemiopsis leidyi Agassiz 1865

Analysis of in situ gut contents of the ctenophore Mnemiopsisleidyi collected during summer months of 1998 at Woods Hole,MA, USA indicates that dietary changes accompanied developmentof this zooplankter. The transition from cydippid to lobatemorphologies involved a shift from a microplanktonic diet dominatedby protists to a metazoan-based diet. Dietary diversity increasedrapidly during the transition from cydippid to lobate stagebut remained essentially similar through most (>3.0 cm totallength) of the lobate stage. These stage-dependent dietary differencesmay have important implications for understanding populationdynamics of M. leidyi.     

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     

The changing ecology of primate parasites: Insights from wild‐captive comparisons

Host movements, including migrations or range expansions, are known to influence parasite communities. Transitions to captivity—a rarely studied yet widespread human‐driven host movement—can also change parasite communities, in some cases leading to pathogen spillover among wildlife species, or between wildlife and human hosts. We compared parasite species richness between wild and captive populations of 22 primate species, including macro‐ (helminths and arthropods) and micro‐parasites (viruses, protozoa, bacteria, and fungi). We predicted that captive primates would have only a subset of their native parasite community, and would possess fewer parasites with complex life cycles requiring intermediate hosts or vectors. We further predicted that captive primates would have parasites transmitted by close contact and environmentally—including those shared with humans and other animals, such as commensals and pests. We found that the composition of primate parasite communities shifted in captive populations, especially because of turnover (parasites detected in captivity but not reported in the wild), but with some evidence of nestedness (holdovers from the wild). Because of the high degree of turnover, we found no significant difference in overall parasite richness between captive and wild primates. Vector‐borne parasites were less likely to be found in captivity, whereas parasites transmitted through either close or non‐close contact, including through fecal‐oral transmission, were more likely to be newly detected in captivity. These findings identify parasites that require monitoring in captivity and raise concerns about the introduction of novel parasites to potentially susceptible wildlife populations during reintroduction programs.     

Timing and size of blooms of the ctenophore Mnemiopsis leidyi in relation to temperature in Narragansett Bay, RI

The ctenophore Mnemiopsis leidyi is at the northern extreme of its geographic range in Narragansett Bay, an estuary on the northeast coast of the United States. Blooms have typically been observed in late summer and fall according to records from 1950 to 1979. We document an expansion of the seasonal range of this important planktonic predator to include springtime blooms during the 1980s and 1990s. This shift to an earlier seasonal maximum is associated with increasing water temperature in Narragansett Bay. Temperatures in spring have risen, on average, 2 °C from 1950 to 1999 with warm years being associated with the positive phase of the North Atlantic Oscillation. During 1999, M. leidyi appeared earlier in spring and was more abundant than during any previous year for which records are available. Changes in the seasonal pattern and abundance of this predator are likely to have important effects on planktonic ecosystem dynamics of Narragansett Bay. These include reduction of zooplankton abundance in spring followed by increases in size and frequency of summer phytoplankton blooms. Earlier blooms of M. leidyi may also reduce survival of eggs and larvae of fish because, as in 1999, they coincide with the period of peak spawning.     

Triggering and regulatory mechanisms of ciliary motion in the ctenophore Bolinopsis. III. Electric excitability and inherent contractility of ciliated cells]

Rhythmical electrostimulation is able to produce in a tissue strip of Bolinopsis series of beats of combs-plates. However, the beat frequency, within one series, is only poorly controlled by electrical stimuli. Isolated comb-plate cells with a cilium cut off maintain rhythmical contractions stimulated both mechanically and electrically. A lot of microtubules has been found in the apical region of these cells. It is supposed that it is these microtubules, probably together with the associated root filaments, that are responsible for cell motility. Mutual mechanical stimulation of ciliary cells in these motions is, presumably, a signal providing intratissue propagation of metachronal wave.