An optimised multi-host trematode life cycle: fishery discards enhance trophic parasite transmission to scavenging birds
Overlapping distributions of hosts and parasites are critical for successful completion of multi-host parasite life cycles and even small environmental changes can impact on the parasite's presence in a host or habitat. The generalist Cardiocephaloides longicollis was used as a model for multi-host trematode life cycles in marine habitats. This parasite was studied to quantify parasite dispersion and transmission dynamics, effects of biological changes and anthropogenic impacts on life cycle completion. We compiled the largest host dataset to date, by analysing 3351 molluscs (24 species), 2108 fish (25 species) and 154 birds (17 species) and analysed the resultant data based on a number of …
Understanding myxozoan infection dynamics in the sea: Seasonality and transmission of Ceratomyxa puntazzi
Abstract Ceratomyxa puntazzi affects the sharpsnout seabream, Diplodus puntazzo , a recently explored aquaculture species in the Mediterranean. Little is known about the transmission and seasonality of marine myxozoans, although this knowledge is of considerable importance for the design of management strategies for aquaculture. In the present study on C. puntazzi we investigated the potential pathways of transmission as well as the parasite abundance in fish and its density in environmental water samples, throughout a full year. We performed monthly sentinel fish exposures in a C. puntazzi enzootic environment and quantified waterborne stages in seawater. Two novel C. puntazzi -specific PC…
Myxobolus albin. sp. (Myxozoa) from the Gills of the Common GobyPomatoschistus micropsKrøyer (Teleostei: Gobiidae)
A recent investigation into the myxozoan fauna of common gobies, Pomatoschistus microps, from the Forth Estuary in Scotland, revealed numerous myxosporean cysts within the gill cartilage. They were composed of polysporous plasmodia containing myxobolid spores that were morphologically different from the other known species of Myxobolus and from the myxosporeans previously recorded from this host (i.e. the ceratomyxid Ellipsomyxa gobii, infecting the gall bladder, and the kudoid Kudoa camarguensis, infecting the muscle tissues). Spores were ovoid, 9.4 x 9.1 microm with a thickness of 6.6 microm, with two pyriform polar capsules, the polar filaments of which had four to five turns. Molecular …
Species complexes and phylogenetic lineages of Hoferellus (Myxozoa, Cnidaria) including revision of the genus: A problematic case for taxonomy
Background Myxozoans are metazoan parasites whose traditional spore morphology-based taxonomy conflicts DNA based phylogenies. Freshwater species of the genus Hoferellus are parasites of the excretory system, with several members infecting food and ornamental fish species, as well as amphibians. This study aims to increase our understanding of their molecular diversity and development, aspects about which little is known, and to generate a molecular diagnostic tool to discriminate between different pathogenic and non-pathogenic Hoferellus spp. Methods SSU and ITS rDNA phylogeny, along with morphological descriptions using light and electron microscopy were used to identify and characterize …
Zschokkella hildae Auerbach, 1910: phylogenetic position, morphology, and location in cultured Atlantic cod.
Abstract The myxozoan Zschokkella hildae Auerbach, 1910, was detected with a prevalence of 100% in cultured Atlantic cod, Gadus morhua L. aged 1+ from a culture facility on the west coast of Scotland. Sporogonic stages of Z. hildae, plasmodia producing 2–5 mature spores, were located predominantly in the collecting ducts and ureters of the kidney, and spores were present in the urine collected from the bladder. Less frequently, plasmodia were detected in the interstitial tissue of the kidney. The parasite prevalence in cultured fish was considerably higher than reported in wild fish but no obvious signs of pathology were detected. SSU rDNA sequencing and phylogenetic analysis showed that Z.…
The joint evolution of the Myxozoa and their alternate hosts: A cnidarian recipe for success and vast biodiversity
The relationships between parasites and their hosts are intimate, dynamic and complex; the evolution of one is inevitably linked to the other. Despite multiple origins of parasitism in the Cnidaria, only parasites belonging to the Myxozoa are characterized by a complex life cycle, alternating between fish and invertebrate hosts, as well as by high species diversity. This inspired us to examine the history of adaptive radiations in myxozoans and their hosts by determining the degree of congruence between their phylogenies and by timing the emergence of myxozoan lineages in relation to their hosts. Recent genomic analyses suggested a common origin of Polypodium hydriforme, a cnidarian parasit…
Cardicola aurata sp. n. (Digenea: Sanguinicolidae) from Mediterranean Sparus aurata L. (Teleostei: Sparidae) and its unexpected phylogenetic relationship with Paradeontacylix McIntosh, 1934
A new sanguinicolid trematode, Cardicola aurata sp. n., is described from gilthead seabream Sparus aurata L., from off the Spanish Mediterranean coast. The morphology of C. aurata sp. n. generally agrees with the diagnosis of the genus, however, in contrast to all other reported Cardicola spp. the male pore is located sub-medially at the posterior end of the body instead of sinistrally before the posterior end of the body. Based on a comparison of the morphology as well as partial 28S and ITS2 rDNA sequence data from the present species with that from closely related species, it was decided to emend the diagnosis of Cardicola rather than create a new genus, as the aberrant position of the m…
Host–parasite relationship of Ceratomyxa puntazzi n. sp. (Myxozoa: Myxosporea) and sharpsnout seabream Diplodus puntazzo (Walbaum, 1792) from the Mediterranean with first data on ceratomyxid host specificity in sparids
Sparidae are economically important fishes to both, fisheries and aquaculture in the Mediterranean. Species diversification is an important strategy for the development of Mediterranean aquaculture. One of the species recently introduced is the sharpsnout seabream Diplodus puntazzo (Walbaum, 1792). During a parasitological study of fish from the Gulf of Valencia and the Mar Menor (Spain), myxozoan spores belonging to the genus Ceratomyxa were found in the gall bladder of D. puntazzo. A morphological description of the spores, which includes histology and transmission electron microscopy (TEM) as well as molecular (SSU ribosomal DNA) data resulted in the erection of a new species, Ceratomyxa…
Molecular and morphological identification of larval opecoelids (Digenea: Opecoelidae) parasitising prosobranch snails in a Western Mediterranean lagoon.
In a study of the digeneans parasitising molluscs in the Els Alfacs lagoon (Ebro Delta, Western Mediterranean) we found heavy infections with sporocysts emitting two types of cotylocercous cercariae in the prosobranch trochid gastropod Gibbula adansonii and with metacercariae in the prosobranch nassariid gastropod Cyclope neritea. A comparative analysis using ITS ribosomal DNA sequences from these larval stages and published sequences of 17 larval and adult opecoelid stages allowed us to elucidate the life-cycle of Macvicaria obovata and to confirm the identification of Cainocreadium labracis based on cercarial morphology. We provide molecular evidence for the identification and the first d…
Description of embryonic development and ultrastructure in miracidia ofCardiocephaloides longicollis(Digenea, Strigeidae) in relation to active host finding strategy in a marine environment
The functional ultrastructure and embryonic development of miracidia in naturally released eggs of the trematode Cardiocephaloides longicollis were studied using light and transmission electron microscopy. This species has operculated eggs and embryogenesis occurs in the marine environment before an actively infecting ciliated miracidium hatches. Six different developmental stages were identified. The lack of pores in the eggshell indicates its impermeability and the miracidium's dependency on glycogen nutritive reserves, contained in numerous vitellocytes in early embryos. As the development advances, these merge into larger vitelline vacuoles that encircle the miracidium and may aid its h…
Skoulekia meningialis n. gen., n. sp. (Digenea: Aporocotylidae Odhner, 1912) a parasite surrounding the brain of the Mediterranean common two-banded seabream Diplodus vulgaris (Geoffroy Saint-Hilaire, 1817) (Teleostei: Sparidae): description, molecular phylogeny, habitat and pathology.
This study describes a new aporocotylid genus and species, Skoulekia meningialis n. gen., n. sp. which was detected in the ectomeningeal veins surrounding the optic lobes of the brain of the common two-banded seabream Diplodus vulgaris (Geoffroy Saint-Hilaire, 1817) from the Gulf of Valencia (Mediterranean Sea). A detailed morphological description of S. meningialis is provided, including drawings, measurements and scanning electron microscopy images as well as a phylogenetic study of S. meningialis and closely related taxa using DNA sequence data obtained from whole ITS2 and partial 18S and 28S rDNA regions. Morphology as well as molecular phylogeny strongly support the erection of a new g…
Speciation of the Paradeontacylix spp. (Sanguinicolidae) of Seriola dumerili. Two new species of the genus Paradeontacylix from the Mediterranean.
Abstract Two new species of teleost blood fluke belonging to the sanguinicolid genus Paradeontacylix are described from the greater amberjack, Seriola dumerili , i.e. Paradeontacylix ibericus n. sp. from the Iberian Peninsula and Paradeontacylix balearicus n. sp. from the Balearic Islands. P. ibericus n. sp. and P. balearicus n. sp. show morphological similarities with Paradeontacylix kampachi and Paradeontacylix grandispinus respectively, which occur in mixed infection in S. dumerili from Japan. Multivariate analysis of morphometrical data provided statistical evidence for the separation of four species. However, component by component analysis did not show statistically significant differ…
Estimating trematode prevalence in snail hosts using a single-step duplex PCR: how badly does cercarial shedding underestimate infection rates?
Background: Trematode communities often consist of different species exploiting the same host population, with two or more trematodes sometimes co-occuring in the same host. A commonly used diagnostic method to detect larval trematode infections in snails has been based on cercarial shedding, though it is often criticized as inaccurate. In the present study we compare infection prevalences determined by cercarial emission with those determined, for the first time, by molecular methods, allowing us to quantify the underestimation of single and double infections based on cercarial emission. We thus developed a duplex PCR for two host-parasite systems, to specifically differentiate between sin…
Morphological and molecular redescription of the myxozoanUnicapsula pflugfelderiSchubert, Sprague & Reinboth 1975 from two teleost hosts in the Mediterranean. A review of the genusUnicapsulaDavis 1924
Elongate plasmodia with myxosporean spores belonging to the genus Unicapsula, Davis, 1924 were found in the skeletal muscle of the striped seabream, Lithognathus mormyrus (L.), a candidate for the mediterranean aquaculture. The only species of Unicapsula described from the Mediterranean is Unicapsula pflugfelderi Schubert et al. 1975, which occurs in the picarel, Spicara smaris (L.). For morphological and molecular comparison of U. pflugfelderi from S. smaris with Unicapsula sp. from L. mormyrus measurements of plasmodia and spores, ultrastructural details and 18S and 28S rDNA sequences were analysed. Whereas plasmodia were 2-3 times larger in S. smaris than in L. mormyrus (length 2.47-0.81…
Kudoa trifolia sp. n. ? molecular phylogeny suggests a new spore morphology and unusual tissue location for a well-known genus
A new species of myxozoan, Kudoa trifolia sp. n., was found in various organs of the golden grey mullet, Liza aurata (Risso), and the thinlip mullet, L. ramada (Risso), from the western Mediterranean. Spores developed in subspherical plasmodia of 0.28-1 mm diameter within connective tissue, predominantly in the spleen, the outer wall of the gall bladder and the gut, the mesenteries and occasionally also in the gills. The spores of K. trifolia differ from the commonly known shape of Kudoa by considerable enlargement of one of the four valve cells, thus forming a 'spore body', which contains the major part of the binucleate sporoplasm. Scanning electron microscopy of the spores revealed the p…
Infection dynamics of two renal myxozoans in hatchery reared fry and juvenile Atlantic cod Gadus morhua L.
SUMMARYIn order to study the infection dynamics of 2 renal myxozoans, Zschokkella hildae Auerbach, 1910 and Gadimyxa atlanticaKøie, Karlsbakk and Nylund, 2007 in cultured Atlantic cod, Gadus morhua L. aged 3–19 months, a specific single-round PCR assay and a double-label in situ hybridization protocol were developed. The results demonstrated that the 2 myxozoans show spatial separation of their development with regard to spore formation inside the renal tubules versus the collecting ducts and ureters, as well as temporal separation with Z. hildae proliferating and developing spores only once the G. atlantica infection decreases, despite the presence of both myxozoans in the smallest fry stu…
3D Morphology, ultrastructure and development of Ceratomyxa puntazzi stages: first insights into the mechanisms of motility and budding in the Myxozoa.
Free, amoeboid movement of organisms within media as well as substrate-dependent cellular crawling processes of cells and organisms require an actin cytoskeleton. This system is also involved in the cytokinetic processes of all eukaryotic cells. Myxozoan parasites are known for the disease they cause in economical important fishes. Usually, their pathology is related to rapid proliferation in the host. However, the sequences of their development are still poorly understood, especially with regard to pre-sporogonic proliferation mechanisms. The present work employs light microscopy (LM), electron microscopy (SEM, TEM) and confocal laser scanning microscopy (CLSM) in combination with specific…
Oncomiracidial development, survival and swimming behaviour of the monogenean Sparicotyle chrysophrii (Van Beneden and Hesse, 1863)
Abstract Oncomiracidial development of Sparicotyle chrysophrii , a monogenean parasite of Sparus aurata , was analysed using 450 eggs. Parasite morphological changes in time, data on hatching success, as well as oncomiracidial survival and swimming behaviour were recorded. Eggs were maintained at 20 °C and exposed to LD 12:12. They were observed under the stereomicroscope every 8 h until they hatched. Thereafter, 155 oncomiracidia were isolated in separate wells and observed every 2 h until their death. Most of the hatchings occurred in a short period of time (approximately 24 h). Hatching success was 87% and the hatching period ranged from 5 to 10 days after deposition, with most of the ha…
Data from: The joint evolution of the Myxozoa and their alternate hosts: a cnidarian recipe for success and vast biodiversity
The relationships between parasites and their hosts are intimate, dynamic and complex; the evolution of one is inevitably linked to the other. Despite multiple origins of parasitism in the Cnidaria, only parasites belonging to the Myxozoa are characterized by a complex life cycle, alternating between fish and invertebrate hosts, as well as by exceptionally high species diversity. This inspired us to examine the history of reciprocal interactions and adaptive radiations in myxozoans and their hosts by determining the degree of congruence between their phylogenies and by timing the emergence of myxozoan lineages in relation to their hosts. Recent genomic analyses suggested a common origin of …