Life cycle and molecular phylogeny of the dinoflagellates Chytriodinium and Dissodinium,ectoparasites of copepod eggs

The dinoflagellates Chytriodinium affine, C. roseum and Dissodinium pseudolunula are ectoparasites of crustacean eggs. Here, we present new observations regarding their life cycle based on coastal plankton samples and incubations and analyze their molecular phylogeny using the small subunit ribosomal RNA gene (SSU rDNA) as a marker. In contrast to the typical stages already documented for its life cycle, we observed that D. pseudolunula dinospores may exceptionally differentiate inside a globular cyst. Despite its parasitic life style, the cysts and dinospores of D. pseudolunula contain chlorophyll a. We obtained the first SSU rDNA sequences for the genera Chytriodinium (the type C. roseum and C. affine) and Dissodinium (D. pseudolunula). Classical taxonomical schemes have ascribed these genera to the order Blastodiniales. However, our SSU rDNA-based phylogenetic analysis shows that these ectoparasites form a clade in the Gymnodinium sensu stricto group, unarmored dinokaryotic dinoflagellates of the order Gymnodiniales. They branch in a subgroup composed of warnowiids, polykrikoids, the type of Gymnodinium, G. fuscum and G. aureolum. Although Chytriodinium and Dissodinium appear to be relatives based on SSU rDNA phylogeny, feeding and host specificity, their life cycles are substantially different. Based on these data we consider that the type of life cycle is a poor criterion for classification at the family level. We suggest that the morphology of the infective cell is probably the most reliable phenotypic characteristic to determine the systematic position of parasitic dinoflagellates.     

Population differences in the timing of diapause: adaptation in a spatially heterogeneous environment

Summary Populations of the planktonic copepod, Diaptomus sanguineus, live in permanent and temporary freshwater ponds in Rhode Island. All ponds in which they occur become uninhabitable at some time during the year, but the nature and timing of the harsh period varies both spatially and temporally. Females produce discrete clutches either of subitaneous eggs which hatch immediately or of diapausing eggs which hatch the following season. The two egg types show distinct chorion morphologies under transmission electron microscopy. In permanent ponds the copepods start making diapausing eggs in March, one month before rising water temperatures induce planktivorous sunfish to become active. In temporary ponds diapausing eggs are produced, in a complex pattern from May to July, before the water disappears in late summer or early fall.We investigated the spatial scale at which D. sanguineus is adapted to this complex environment. In a reciprocal transfer experiment between temporary and permanent bodies of water, female copepods placed in new ponds made subies of water, female copepods placed in new ponds made subitaneous and diapausing eggs in the same sequence as control females retained in their home ponds. The copepod populations enter diapause at times appropriate for the local habitat conditions they experience, but inappropriate for other, nearby ponds. Transplanted females were unable to sense a change in pond type or to adjust egg production accordingly. We conclude that D. sanguineus populations are adapted to the specific conditions of isolated ponds rather than to a broader geographical region containing several pond types.     

Molecular Phylogeny of the Parasitic Dinoflagellate Chytriodinium within the Gymnodinium Clade (Gymnodiniales,Dinophyceae)

The dinoflagellate genus Chytriodinium, an ectoparasite of copepod eggs, is reported for the first time in the North and South Atlantic Oceans. We provide the first large subunit rDNA (LSU rDNA) and Internal Transcribed Spacer 1 (ITS1) sequences, which were identical in both hemispheres for the Atlantic Chytriodinium sp. The first complete small subunit ribosomal DNA (SSU rDNA) of the Atlantic Chytriodinium sp. suggests that the specimens belong to an undescribed species. This is the first evidence of the split of the Gymnodinium clade: one for the parasitic forms of Chytriodiniaceae (Chytriodinium, Dissodinium), and other clade for the free‐living species.     

Asterocheres crinoidicola n. sp., a copepod (Siphonostomatoida: Asterocheridae) parasitic on crinoids in Belize

A new species of siphonostomatoid copepod, Asterocheres crinoidicola, is parasitic on two closely related comasterid crinoids (Nemaster grandis and Davidaster rubiginosus) in Belize, Central America. An unusually long terminal prolongation of the third segment of the endopod of leg 1 distinguishes this species from all congeners. This is the first report of a copepod parasitic on a crinoid in the Caribbean.     

Phylogeny,Evidence for a Cryptic Plastid,and Distribution of Chytriodinium Parasites (Dinophyceae) Infecting Copepods

Spores of the dinoflagellate Chytriodinium are known to infest copepod eggs causing their lethality. Despite the potential to control the population of such an ecologically important host, knowledge about Chytriodinium parasites is limited: we know little about phylogeny, parasitism, abundance, or geographical distribution. We carried out genome sequence surveys on four manually isolated sporocytes from the same sporangium, which seemed to be attached to a copepod nauplius, to analyze the phylogenetic position of Chytriodinium based on SSU and concatenated SSU/LSU rRNA gene sequences, and also characterize two genes related to the plastidial heme pathway, hemL and hemY. The results suggest the presence of a cryptic plastid in Chytriodinium and a photosynthetic ancestral state of the parasitic Chytriodinium/Dissodinium clade. Finally, by mapping Tara Oceans V9 SSU amplicon data to the recovered SSU rRNA gene sequences from the sporocytes, we show that globally, Chytriodinium parasites are most abundant within the pico/nano‐ and mesoplankton of the surface ocean and almost absent within microplankton, a distribution indicating that they generally exist either as free‐living spores or host‐associated sporangia.     

Epizootiology of Amblyospora connecticus (Microsporida) in Field Populations of the Saltmarsh Mosquito, Aedes cantator, and the Cyclopoid Copepod, Acanthocyclops vernalis

The natural ecology of a heterosporous microsporidium, Amblyospora connecticus was investigated at three different salt marsh habitats during 1986–1989. The parasite has a well-defined seasonal transmission cycle that occurs regularly each year and intimately involves the primary mosquito host, Aedes cantator, and the intermediate copepod host, Acanthocyclops vernalis. In the spring, the microsporidium is horizontally transmitted from the copepod, where it appears to overwinter, to the mosquito via the ingestion of haploid spores produced in the copepod. Mosquitoes develop a benign infection, and females transmit the microsporidium transovarially to their progeny via infected eggs. Oviposition occurs during the summer and infected eggs hatch synchronously in the fall causing widespread epizootics. Infected larvae die, and the cycle is completed when meiospores are released into the pool and subsequently are eaten by A. vernalis, which reappears in the fall and early winter. Amblyospora connecticus thereby persists by surviving in one of two living hosts throughout most of its life cycle rather than in the extra-corporeal environment. This represents an important survival strategy for A. connecticus as results show the salt marsh habitat to be a relatively unstable environment that is subject to periodic flooding and drying. The adaptive significance of utilizing an intermediate host in the life cycle is discussed as it directly facilitates transmission and enhances survival of the microsporidium.     

Copepod eggs survive a decade in the sediments of the Baltic Sea

Many planktonic calanoid copepod species have been proved to spend a part of their life cycle as benthic resting eggs. In addition to avoiding seasonally occurring unfavourable conditions resting stages may also be used as a long-term survival strategy. The aim of this study was to find out for how long eggs of calanoid copepods retain their viability in the sediments of the Baltic Sea. The occurrence of viable copepod eggs in sea bottom sediment was studied in Pojovik Bay, SW coast of Finland. Eggs were found throughout a 25 cm deep core but deeper than 20 cm they were very scarce. Eggs were incubated at 12 °C in order to check the viability, and their age was estimated by determining the sediment accumulation rate with ¹³⁷Cs-method. Viable eggs were estimated to be 10–13 yrs old, some possibly even 18–19 yrs. Most eggs in the top 8 cm were viable, their age being up to 7–8 yrs. Nauplii that hatched from the eggs belonged to Acartia bifilosa and Eurytemora affinis, A. bifilosa dominating the hatchers of the top sedment layers and E. affinis the deeper layers. Preliminary evidence is presented that E. affinis produces true diapause eggs in the Baltic Sea.     

Dissodinium pseudocalani sp. nov., ein parasitischer Dinoflagellat auf Copepodeneiern

Zusammenfassung 1.Dissodinium pseudocalani ist eine neue, auf den Eiern des CopepodenPseudocalanus elongatus ektoparasitisch lebende Peridinee. Die Art tritt im Plankton der Deutschen Bucht von Mitte April bis Anfang Juni auf.2. Anfänglich ist der blasenförmige Parasit mit einem stabilen Saug-Haftorgan in seiner Wirtszelle verankert. Nachdem der Inhalt des Eies aufgenommen ist, löst er sich als kugelförmige Primärzyste von einem Durchmesser zwischen 151–250 µ ab. Sie enthält einen gefärbten Nahrungsballen, der während der Vermehrungsteilungen zusammenschrumpft.3. Durch simultane Teilung entstehen in der Primärzyste 8, 16 oder 32 ovale Sekundärzysten, in denen sukzedan jeweils 16 oder 32 begeißelte Dinosporen gebildet werden. Die Dinosporen sind farblos und gehören demGymnodinium-Typ an. Die Infektion derPseudocalanus-Eier konnte nicht direkt beobachtet, sondern nur aus den verschiedenen im Plankton gefundenen Entwicklungsstadien erschlossen werden.

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Dissodinium pseudocalani sp. nov., a parasitic dinoflagellate on copepod eggs

In spring 1967 and 1968, a new marine dinoflagellate species,Dissodinium pseudocalani, was discovered off Helgoland in the German Bight. The species lives as ectoparasite on eggs of the copepodPseudocalanus elongatus. The vesicular parasitic stage adheres to the host by a suction organ. After the substrate of the egg is consumed, the parasite develops into a spherical primary cyst which produces 8, 16 or 32 oval secondary cysts by simultaneous cell divisions. Each secondary cyst forms 16 or 32 dinospores. The dinospores are colourless, flagellated and of theGymnodinium-type. During reproduction a large reddish or greenish coloured food source is resorbed by the protoplast and diminishes in size. In regard to its mode of reproduction,Dissodinium pseudocalani is related toD. lunula and the parasitic species ofChytriodinium.

     

Saving for the future: Pre‐winter uptake of algal lipids supports copepod egg production in spring

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Copepod feeding behaviour and egg production during a dinoflagellate bloom in the North Sea

Feeding strategies of copepods were studied during a dinoflagellate-dominated bloom in the North Sea in August 2001. The aim of this study was to evaluate the importance of mesozooplankton grazing as a biological loss factor of harmful algal blooms under natural conditions. Therefore, ingestion, egestion and egg production experiments were performed with the most abundant copepod species Calanus helgolandicus, Temora longicornis and Acartia sp. feeding on the natural phytoplankton community. Dinophysis norvegica and Ceratium furca were the most abundant dinoflagellate species at the time of the experiments. Grazing experiments as well as examination of fecal pellet content revealed C. helgolandicus fed efficiently on D. norvegica. Ingestion rates up to 47 cells female⁻¹ h⁻¹ were measured and a large proportion of the C. helgolandicus fecal pellets contained intact D. norvegica cells. Dinophysis cells were rarely seen in fecal pellets produced by T. longicornis, and never observed in pellets produced by Acartia sp. The ingestion rate of C. furca, which was the dominating Ceratium species, mimicked that of D. norvegica. C. helgolandicus grazed significantly on C. furca (16 cells female⁻¹ h⁻¹), while the ingestion rate of T. longicornis was low and Acartia sp. was not able to graze on C. furca. Egg production experiments revealed that 92% of the C. helgolandicus females produced eggs. The specific egg production rate and the proportion of females producing eggs among T. longicornis were low. This field experiment clearly shows that some copepod species feed efficiently on D. norvegica and C. furca under natural conditions, which may affect the bloom development of these dinoflagellates.     

Naricolax insolitus n. sp., a bomolochid copepod (Poecilostomatoida) parasitic in the nasal cavities of silver pomfret Pampus argenteus off Taiwan

A new species of bomolochid copepod (Poecilostomatoida), Naricolax insolitus n. sp., parasitic in the nasal cavities of the silver pomfret Pampus argenteus (Euphrasen) from the Strait of Taiwan is described. The new species is distinguished from its only known congener, N. atypicus Ho, Do & Kasahara, 1983, by possessing the following four apomorphic features: (1) a complex outgrowth on the egg-sac attachment area; (2) a bent egg-sac; (3) a sharp hook (modified seta V) on the caudal ramus; and (4) an armature of II,I,4 (instead of II,I,5) on the terminal segment of leg 4 exopod. This is the first record of parasitic copepod from the nasal cavities of the silver pomfret.     

Zoogeography of parasitic Copepoda of the New Zealand region

The islands of New Zealand are believed to be fragments from the Gondwanaland supercontinent that are now over 2 000 km from either Australia or Antarctica. Despite this, the marine fish parasitic copepod fauna is neither isolated nor distinctive, but reflects the southward extension of the tropical Indo-Pacific fauna and also the circumpolar element. Only one of the 49 known genera, representing 18 families, is endemic and speciation within all the families is low.Although the origin of the marine fish parasitic copepod fauna can be explained in terms of host dispersal patterns, the derivation of the euryhahne endemic Abergasilus and the freshwater Paeonodes and Thersitina is still an enigma.The copepod associates of the invertebrates are still virtually unknown and no conclusions can be drawn.     

Life cycle ofSchizochytriodinium calani nov. gen. nov. spec., a dinoflagellate parasitizing copepod eggs

During the Polarstern-cruise ARK IV/2 June 1987, in the Fram Strait, dinophytes parasitizing copepod eggs were observed. In the laboratory on board, vegetative reproduction was documented and re-infection ofCalanus glacialis andC. hyperboreus eggs was experimentally established. During food uptake, a primary cyst produces successively several secondary cysts, all separating immediately after formation from the primary cyst. In every one of these free floating secondary cysts up to 256 dinospores are formed by palintomy. Re-infection only occurred after a “maturation time” of at least 2 days after formation of the dinospores. The life cycle is compared to that of other similar parasitic dinophyte genera:Apodinium Chatton,Chytriodinium Chatton,Dissodinium Klebs in Pascher andMyxodinium Cachon, Cachon & Bouquaheux. As the taxon under discussion does not fit in with any species or genus known so far, it is described asSchizochytriodinium calani nov. gen. nov. spec. Dedicated to Dr. Dr. h. c. P. Kornmann on the occasion of his 80th birthday. Mitglied der Taxonomischen Arbeitsgruppe an der BAH.     

External morphology of the male and female of Sphyrion lumpi (Krøyer,1845) (Copepoda; Siphonostomatoida; Sphyriidae)

Sphyrion lumpi is a sexually dimorphic, parasitic copepod which causes significant losses in fisheries in the North Atlantic. Studies involving both light and scanning electron microscopy revealed important details of the external morphology of both sexes that are discussed in relation to other members of the family Sphyriidae. Conclusions are drawn regarding the life cycle of S. lumpi. The present finding of this parasite on Urophycis tenuis constitutes a new host record.     

Lernanthropus corteziensis n. sp. (Copepoda: Lernanthropidae), parasitic on the gills of a teleost fish in Mexican waters

A new species of parasitic copepod, Lernanthropus corteziensis (Siphonostomatoida: Lernanthropidae), is described and illustrated. The copepod has been found in the Sea of Cortez (Bahia de la Paz) on the gills of Diapterus peruvianus, a teleost fish known in the local vernacular as mojarra.     

Choniomyzon inflatus n. sp. (Crustacea: Copepoda: Nicothoidae) associated with Ibacus novemdentatus (Crustacea: Decapoda: Scyllaridae) from Japanese waters

A new species of parasitic copepod, Choniomyzon inflatus n. sp., is described based on specimens collected from the external egg masses of the smooth fan lobster Ibacus novemdentatus Gibbes captured in the North Pacific Ocean off Ainan, Ehime Prefecture, western Japan. The new species differs from its congeners in having a globular to ovoid prosome, in bearing asymmetrically arranged denticles at a rounded apex of both the terminal segment of the antenna and the maxilliped, and in lacking serrate lobes on the basis of legs 1 and 2. The species is similar in size and shape to the host’s eggs, which may be interpreted as egg mimicry. The new species is the first member of Choniomyzon Pillai, 1962 from subtropical regions.     

Great spotted cuckoo eggshell microstructure characteristics can make eggs stronger

Obligate avian brood parasites lay stronger eggs than their hosts or non‐parasitic relatives because they are rounder and have a thicker eggshell. Additionally, some other characteristics of the brood parasitic eggshells related to their microstructure such as size and orientation of calcite crystal units could also contribute to generating even stronger shells. An eggshell microstructure formed by small randomly oriented calcite crystal units can increase the robustness of the eggshells of birds. Here, the eggshell microstructure of avian brood parasites as well as their hosts have been characterized in detail, using X‐ray diffraction analyses to estimate the size and degree of orientation of calcite crystal units making the eggshell. Specifically, the brood parasitic great spotted cuckoo Clamator glandarius and two hosts (jackdaws Corvus monedula and magpie Pica pica) and one non‐host species (the pigeon, Columba livia domestica) were considered. Calcite crystal of the eggshell of the brood parasitic species was smaller and more randomly oriented than those of the eggshells of non‐parasitic species, which suggest that eggshell microstructure would contribute to explain why parasitic eggs are more resistant to breakage than those of their hosts.     

The parasitic copepod Lernaeocera branchialis negatively affects cardiorespiratory function in Gadus morhua

The parasitic copepod Lernaeocera branchialis had a negative effect on cardiorespiratory function in Atlantic cod Gadus morhua such that it caused pronounced cardiac dysfunction with irregular rhythm and reduced stroke amplitude compared with uninfected fish. In addition, parasite infection depressed the postprandial cardiac output and oxygen consumption.     

Parasitic dinoflagellates and ellobiopsids (Ellobiopsidae) of the coastal waters of the sea of Japan

Five species of parasitic dinoflagellates of the genera Protoodinium, Paulsenella, Duboscquella, Syndinium, and Dissodinium and two species of ellobiopsids of the genus Ellobiopsis are described. Figures and distribution data are provided. All species, except for Dissodinium pseudolunula Swift ex Elbrachter et Drebes, are first records for the Russia Far-Eastern seas.