Synopsis of the Species of Coccidians Reported in Marine Fish

Saraiva, Aurélia; Eiras, Jorge C.; Cruz, Cristina; Xavier, Raquel

doi:10.3390/ani13132119

Open AccessReview

Synopsis of the Species of Coccidians Reported in Marine Fish

¹

Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, Edifício FC4, 4169-007 Porto, Portugal

²

CIIMAR, Interdisciplinary Center of Marine and Environmental Research, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos s/n, 4450-208 Matosinhos, Portugal

³

CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO, Laboratório Associado, Campus Agrário de Vairão, Universidade do Porto, 4485-661 Vila do Conde, Portugal

⁴

BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Campus Agrário de Vairão, 4485-661 Vila do Conde, Portugal

^*

Authors to whom correspondence should be addressed.

Animals 2023, 13(13), 2119; https://doi.org/10.3390/ani13132119

Submission received: 20 April 2023 / Revised: 15 June 2023 / Accepted: 17 June 2023 / Published: 26 June 2023

(This article belongs to the Special Issue Advances in Fish Pathology)

Download

Browse Figures

Versions Notes

Abstract

:

Simple Summary

Apicomplexa (Levine, 1970) are obligate parasites, of both vertebrate and invertebrate hosts, and may be responsible for important diseases. The majority of piscine apicomplexans are coccidians, which infect the cells of the alimentary tract and other extra-intestinal tissues. The goal of this work is to provide up-to-date information about the diversity of these parasites in marine fish. For this purpose, available information concerning Coccidia morphology and molecular profile, the hosts and the organs they infect, as well as their geographic distribution, was assembled. It is remarkable that from the 100 morphologically described species, only 6 have available genetic data.

Abstract

Eimeriid coccidians represent one of the largest groups of parasitic unicellular organisms and comprise many species of veterinary and medical importance. The aim of this work is to provide information, as complete as possible, concerning the oocyst phase of the species of coccidians (Apicomplexa: Eimeriorina) with four sporocysts, which were reported in marine fish. For each species, the accepted scientific name and respective authorities, its synonyms, reported hosts, site of infection (organ), and geographic distribution have been assembled. Available information on morphology (oocyst, sporocyst, and sporozoite) and GenBank accession numbers were also compiled. A total of 100 species of coccidians were described and reported from 60 families of marine fishes. Most species have been described from marine teleosts, with only 14 of the species described from marine elasmobranchs. Most of the species reported in marine fish belong to the genera Eimeria and Goussia, and only a handful belong to the genera Epieimeria, Calyptospora, and Crystallospora. Although marine coccidians have began to be described for more than one century, the collection of genetic data on marine fish coccidians only started in the 2010s and remains largely disconnected from the morphological analysis of specimens, which is available for only six formally described species.

Keywords:

apicomplexa; eimeriorina; Eimeria; Goussia; Epieimeria; Calyptospora; Crystallospora; fish

1. Introduction

Eimeriid coccidians represent one of the largest groups of parasitic unicellular organisms and comprise many species of veterinary and medical importance [1]. Although the first fish coccidian studies were conducted in the last decade of the nineteenth century, still, little is known about the life cycles, morphology, phylogenetic, and infection patterns of these parasites, especially those that occur in marine fish.

Coccidians infecting marine fish belong to the genera Eimeria Schneider, 1875; Goussia Labbé, 1896; Epieimeria Dyková and Lom, 1981; Calyptospora Overstreet, Hawkins and Fournie, 1984; and Crystallospora Labbé, 1896. It should be stressed that the genus Goussia was erected to accommodate piscine coccidians with oocysts possessing four sporocysts, with two valves joined by a longitudinal suture. This genus has a controversial history, but the studies conducted in the last decades indicate that Goussia is a valid genus, which seems to represent the ancestral state of the Sarcocystidae, Eimeriidae, and Calyptosporidae [2,3,4]. Importantly, Benajiba et al. [5] suppressed the genus Epieimeria Dyková and Lom, 1981, on the basis of the intracellular gamogony, merogony, and sporogony of the type species E. anguillae. Observations conducted by Sitjà-Bobadilla et al. [6] further support the suppression of this genus. If these features are confirmed in all described species of the genus Epieimeria, they should be moved to the genus Eimeria.

Adding to a troubled taxonomy, the information on coccidians that infect marine fish is currently widely dispersed across both older and more recent scientific publications and, apart from the annotated list provided in the work of Dyková and Lom [7] from the early 1980s, no other attempt has been made to review all the information on fish coccidians. The aim of this work is to compile, as complete as possible and for the first time, the available information concerning the oocyst phase of the species of coccidians (Apicomplexa: Eimeriorina) with four sporocysts which has been reported from marine fish.

The specific objectives of this review were to provide: (i) an up-to-date list of species of marine piscine coccidians; (ii) a complete overview of their known hosts, geographic range, and infected organs; (iii) morphological characterization of each species and, whenever possible, drawings of their oocysts; (iv) a summary of their phylogenetic affinities; and (v) a discussion of the state of the art, identifying knowledge gaps and future research areas.

2. Materials and Methods

A bibliographic search was performed using all available databases and fields included on Web of Science (https://www.webofscience.com/wos/woscc/basic-search) with the following search string: (Coccid* or Goussia or Eimeria or Epieimeria or Crystallospora or Calyptospora) and fish.

For the purpose of constructing a list of species infecting marine fish, species that were given a generic but not specific assignations were not considered. Additionally, species for which a Stieda body was not referred, but that were still reported in genus Eimeria, were maintained in this genus until new data are available.

For each coccidian species, we assembled the accepted scientific name and respective authorities, eventual synonyms (syn), hosts, site of infection (organ), and geographic distribution. Regarding the geographic distribution, the precision of the available information in the reviewed manuscripts varied significantly (in some cases, a country was mentioned; in others, an ocean; and in others, a very specific location on the coast of a country). In cases for which sea(s) or ocean(s) were not referenced in the original publication, this information was added.

Available information on morphology and dimensions (oocyst, sporocyst, and sporozoite) is detailed according to what was reported in the reviewed publications. GenBank accession numbers, whenever available, were also compiled. Additionally, any other information that was deemed important was also supplied. Hosts’ family and names (both vernacular and scientific names) were reported according to FishBase [8].

Measurements, unless otherwise stated, are provided in µm. Oocysts were redrawn whenever good drawings were available in the literature (Figure 1, Figure 2, Figure 3 and Figure 4). In all presented drawings, scale bars are adapted to equal to 10 µm. Some drawings are not to scale.

Additionally, genetic data available on NCBI’s GenBank (https://www.ncbi.nlm.nih.gov/genbank/) for the 18S rRNA region of piscine coccidians, including those of lineages recovered from marine fish which were not identified to the species level, were compiled for phylogenetic analysis. Based on previously published phylogenies and the recognized existence of different genetic groups [4], as well as results from BLAST (Basic Local Alignment Tool) analysis, five different phylogenetic trees were reconstructed using Bayesian inference, implemented in MrBayes v3.2.6 [9]. Sequence alignment was performed using MAFFT software [10], and sequence models of evolution were selected using jModelTest 2.1.6 [10]. Based on the BLAST analysis of the sequences from ingroups, either Isospora belli (DQ060661) or Intranuclear coccidium (AY728896) were selected as outgroups. Three available sequences were not considered due to their short length, all belonging to Goussia clupearum (MF468314, MF468308 and MT463285).

3. Results

Our search resulted in 100 species of coccidians, detected in 60 families of marine fishes (Table 1), and distributed among 5 genera: Calyptospora and Crystallospora, both with 1 described species each; Epieimeria, with 4 described species; Eimeria, with 64 species; and Goussia, with 30 species. For some species, it was not possible to obtain all information concerning the characteristics taken into account for this review.

3.1. Species List

Calyptospora funduli (Duszynski, Solangi and Overstreet, 1979) Overstreet, Hawkings and Fournie, 1984

Syn: Eimeria funduli Duszynski, Solangi and Overstreet, 1979.

Host: Gulf killifish, Fundulus grandis, Fundulidae; Saltmarsh topminnow, Fundulus jenkinsi, Fundulidae; Bayou killifish, Fundulus pulvereus, Fundulidae; Longnose killifish, Fundulus similis, Fundulidae; Mummichog, Fundulus heteroclitus, Fundulidae; Inland silverside, Menidia beryllina, Atherinopsidae; gulf toadfish, Opsanus beta, Batrachoididae.

Locality: Off US and Gulf of Mexico, Atlantic Ocean.

Organ: Liver, pancreas, occasionally fat tissue, mesentery, ovary, intestine, gall bladder and dermis.

Oocysts: Spherical, 25 (20–31), without residuum (Figure 1(1)).

Sporocysts: Ovoid 10 (9–11) × 6 (5–7), bearing 10 to 25 sporopodia that support a veil, one to four small refractile granular residua.

Sporozoites: With one large refractile body near posterior end.

GenBank accession number: 18S rRNA: GU479670, FJ904646, FJ904645, FJ904644, FJ904643.

Infection cannot be transmitted directly by oocysts. Crustaceans (Palaemonetes and Macrobrachium species) act as intermediate hosts.

In heavy infections, large aggregations of oocysts replaced up to 85% of the liver. Heavy infections have a detrimental effect on hosts.

References: [11,12,13,14]

Crystallospora crystalloides (Thélohan, 1893) Labbé, 1899

Syn: Coccidium crystalloides, Thélohan, 1893; Crystallospora thelohani, Labbé, 1896; Eimeria crystalloides, (Thélohan, 1983) Doflein, 1909.

Host: Shore rockling, Gaidropsarus mediterraneus (referred as Motella fusca), Gaidropsaridae; Three-bearded rockling, Gaidropsarus vulgaris (referred as Motella maculate and M. tricirrata), Gaidropsaridae.

Locality: Atlantic Sea; Mediterranean Sea.

Organ: Intestine.

Oocyst: Round, 20–24 (Figure 1(2)).

Sporocysts: 15 × 9.5.

References: [7,13,15]

Eimeria adioryxi Diouf and Toguebaye, 1994

Host: Red squirrelfish, Sargocentron hastatum (referred as Adioryxi hastatus), Holocentridae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Intestine.

Oocysts: Spherical, 9.7 ± 0.6, without residuum (Figure 1(3)).

Sporocysts: Ovoid, 6.8 ± 0.8 long and 5.1 ± 0.3 wide, with Stieda body, four refringent granular residua; Sporozoites: Forming a cross.

References: [16]

Eimeria anguillae Léger and Holland, 1992

Syn: Epieimeria anguillae, (Léger and Holland, 1922) Dyková and Lom, 1981.

Host: European eel, Anguilla anguilla, Anguillidae; New Zealand longfin eel, Anguilla dieffenbachiii, Anguillidae; short-finned eel, Anguilla australis, Anguillidae; American eel, Anguilla rostrata, Anguillidae.

Locality: Languedoc and Camargue lagoons, Mediterranean Sea; Adriatic Sea.

Organ: Intestine.

Oocysts: Spherical, 8.0–12.8 (Figure 1(4)).

Sporocysts: Ellipsoidal, 5.6–8.8 × 2.4–5.6, hexagonal in transverse section, with Stieda body and globular residuum.

Sporozoites: Curved.

GenBank accession number: 18S rRNA: GU479633, GU593704.

These parasites can cause mucosa and submucosa degeneration, emaciation and death.

References: [5,7,13,17,18,19,20]

Eimeria ashburneri Molnár and Rodhe, 1988

Host: Red Pandora, Pagellus bellottii, Sparidae; bluespotted seabream, Pagrus caeruleostictus (referred as Sparus caeruleostictus), Sparidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Intestine.

Oocysts: Spherical 8.5 ± 0.6, without residuum (Figure 1(5)).

Sporocysts: Ovoid, 5.9 ± 0.6 long by 3.9 ± 0.4 wide, with Stieda body, small granular residuum.

Sporozoites: Falciform, two per sporocysts arranged in cross.

Molnár and Rohde [21] detected this species in freshwater fish, Golden perch, Macquaria ambigua, Percichthydae.

References: [16]

Eimeria atherinae Daoudi, Radujkovic, Marquès and Bouix, 1987

Host: Big-scale sand smelt, Atherina boyeri, Atherinidae.

Locality: Kotor Bay, Adriatic Sea; Thau pond, Mediterranean Sea.

Organ: Intestine.

Oocysts: Spherical 12 (11.5–13.5), without residuum (Figure 1(6)).

Sporocysts: Ellipsoidal 8.0 (7.0–9.0) × 5.0 (4.5–5.5) with Stieda body (in drawings not visible), granular residuum.

Sporozoites: 7.0 × 1.5.

References: [19,20]

Eimeria banyulensis Lom and Dyková, 1982

Host: Axillary wrasse, Symphodus mediterraneus (referred as Crenilabrus mediterraneus), Labridae; Grey wrasse, Symphodus cinereus, Labridae.

Locality: Banyuls-sur-Mer, Mediterranean Sea; Adriatic Sea.

Organ: Intestine.

Oocysts: Spherical, 6.5–8.5), without residuum (Figure 1(7)).

Sporocysts: Ellipsoidal, 4.5–5.5 × 3.0–4.0, without Stieda body, with a mass of granular residuum.

Sporozoites: Ellipsoidal 1.5–2.0.

References: [7,20,22,23]

Eimeria bouixi Daoudi and Marquès, 1986

Host: European seabass, Dicentrarchus labrax, Moronidae.

Locality: Mediterranean Sea.

Organ: Pyloric caeca.

Oocysts: Spherical, 7.0 (6.0–7.6) (Figure 1(8)).

Sporocysts: Ellipsoidal, 4.4 (4.0–4.9) × 3.0 (2.6–3.2) without Stieda body.

Sporozoites: 3.0–1.0.

According to the authors all developing stages are intra-nuclear.

References: [24]

Eimeria brevoortiana Hardcastle, 1944

Host: Atlantic menhaden, Brevoortia tyrannus, Clupeidae.

Locality: US coast of North Carolina, Atlantic Ocean.

Organ: Pyloric caeca, testes.

Oocysts: Spherical 17.0–30.0 or ellipsoidal 15.0–22.0 × 26.0–30.0), with residuum (Figure 1(9)).

Sporocysts: Elongate, 16.0 × 6.0, with residuum; no information of Stieda body.

Sporozoites: Unflexed.

Reference: [7,13,25]

Eimeria catalana Lom and Dyková, 1981

Host: Axillary wrasse, Symphodus mediterraneus (referred as Crenilabrus mediterraneus), Labridae; grey wrasse, Symphodus cinereus, Labridae; blackbar hogfish, Bodianus speciosus, Labridae; Guinean parrotfish, Scarus hoefleri, Scaridae.

Locality: Banyuls-sur-Mer, Mediterranean Sea; Adriatic Sea; off Senegal, Atlantic Ocean.

Organ: Intestine.

Oocysts: About eleven residua in the form of a few refractile granules (Figure 1(10)).

Sporocysts: Ovoid, 7.5–8.5 × 5.5–6.5, with a narrower end bearing a flat ring-like thickening around Stieda body; granular residuum.

Sporozoites: C shaped and with flexed ends.

Reference: [7,13,20,23,26]

Eimeria cheilodactyli Molnár and Rodhe, 1988

Host: Red morwong, Morwong fuscus (referred as Cheilodactylus fuscus), Latridae.

Locality: Tasmania Sea.

Organ: Pyloric caeca, intestine.

Oocysts: Round, 11.2 (10.5–11.5), without residuum (Figure 1(11)).

Sporocysts: Elongate ellipsoidal, 9.6 (8.6–10.4) × 4.2 (4.0–4.4), Stieda body small, scattered coarse of granular residuum.

Sporozoites: Vermiform with one end reflexed.

References: [27]

Eimeria chollaensis Upton, Garder and Duszynski, 1988

Host: Haller’s round ray (=round stingray), Urobatis halleri (=Urolophus halleri), Urotrygonidae.

Locality: Gulf of California, Pacific Ocean.

Organ: Spiral valve.

Oocysts: Ovoid, 13.3 (11.2–16.0) × 9.7 (8.0–10.8), lenght/width ratio 1.4 (1.2–1.5) (Figure 1(12)).

Sporocysts: Ovoid, 8.9 (8.0–10.0) × 4.9 (4.2–5.6), lenght/width ratio 1.8 (1.6–2.1), with Stieda but no substieda body, compact spherical residuum, 2.5 (2.0–3.4).

Sporozoites: Elongate, arranged head to tail within the sporocyst, with numerous transverse striations anteriorly and with a single, ovoid refractile body.

Sporulation exogenous. All oocysts recovered unsporulated from faeces.

Reference: [28,29]

Eimeria ciliatae Molnár and Rodhe, 1988

Host: Sand sillago, Sillago ciliata (referred as sand whiting), Sillaginidae.

Locality: Tasmania Sea.

Organ: Pyloric caeca, intestine.

Oocysts: Round, 14.0 (13.4–14.2), without residuum (Figure 1(13)).

Sporocysts: Oval, 11.2 (10.9–11.7) × 7.3 (6.7–7.6), with small thickenings and cap on tapered end, round and finely granular residuum.

Sporozoites: Vermiform.

References: [21]

Eimeria citriformis Dogiel, 1948

Host: Tilesina gibbosa, Agonidae.

Locality: Sea of Japan.

Organ: Pyloric caeca.

Oocysts: Spherical, 15 (Figure 1(14)).

Sporocysts: Lemon-like, 8.0–9.0 × 5.0.

Reference: [7,30]

Eimeria clini Fantham, 1932

Host: Clinus superciliosus, Clinidae.

Locality: Off South Africa (Atlantic Ocean or Indian Ocean?).

Organ: Intestine.

We were unable to obtain the article describing this species or any subsequent one.

Reference: [7]

Eimeria dakarensis Faye, 1988

Host: Bluespotted seabass, Cephalopholis taeniops, Serranidae; Blacktip grouper, Epinephelus fasciatus (referred as Epinephelus alexandrinus), Serranidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Pyloric caeca, intestine.

Oocysts: Spherical, 11.4 ± 0.7, without residuum (Figure 1(15)).

Sporocysts: Pear-shaped 6.8 ± 0.6 long by 4.6 ± 0.9 wide, with Stieda body, four refringent granular residua.

References: [16]

Eimeria dicentrarchi Daoudi and Marquès, 1986

Host: European seabass, Dicentrarchus labrax, Moronidae.

Locality: Languedoc, Mediterranean Sea; Adriatic Sea.

Organ: Pyloric caeca, intestine.

Oocysts: Spherical, 11.2 (10.6–12.2) (Figure 1(16)).

Sporocysts: Ellipsoidal, 6.8–8.6 × 4.2–5.6, with a flattened, split-like Stieda body, four to five dispersed granular residua.

Sporozoites: Banana shaped, 4.8–6.9 × 1.4–2.0.

References: [24,31]

Eimeria dingleyi Davies, 1978

Host: Shanny, Lipophryus pholis (referred as Blennius pholis), Bleenniidae.

Locality: Saint George Channel, Welsh coast, Atlantic Ocean.

Organ: Intestine.

Oocysts: Spherical, 16.1–19.2 to subspherical, 18.8–20.0 × 13.9–14.2, without residuum (Figure 1(17)).

Sporocysts: Spherical to ellipsoid 9.4–9.9 × 5.8–6.1, without Stieda body, without residuum.

Sporozoites: 8.6–9.0 × 2.6–3.1, single large refractile body at broad end.

Reference: [7,32]

Eimeria dogieli (Dogiel, 1948) Pellérdy, 1963

Syn: E. sphaerica Dogiel, 1948.

Host: Ocellated blenny, Opinthocentrus ocellatus, Opisthocentridae.

Locality: Sea of Japan.

Organ: Kidney.

Oocysts: Irregular form, tightly pressed against sporocysts, without residuum.

Sporocysts: Spherical, 4.5–5.0, without residuum.

Reference: [7,30]

Eimeria dykovae Molnár and Rohde, 1988

Host: Red morwong, Morwong fuscus (referred as Cheilodactylus fuscus), Latridae.

Locality: Tasmania Sea.

Organ: Pyloric caeca, intestine.

Oocysts: Round, 7.8 (7.2–8.4), without residuum (Figure 1(18)).

Sporocysts: Oval, 5.6 (5.1–5.9) × 3.3 (3.2–3.5), with Stieda body, round finely granular residuum.

Sporozoites: Vermiform.

References: [27]

Eimeria ethmalosae Diouf and Toguebaye, 1994

Host: Bonga shad, Ethmalosa fimbriata, Clupeidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Testes.

Oocysts: Spherical, variable size, 22–53 (Figure 1(19)).

Sporocysts: 9.2–12.5 × 6.7–8.3, four to five refringent granular residua, with Stieda body.

This species has three sizes of oocysts which were designated as micro-oocysts, meso-oocysts and macro-oocysts.

References: [16]

Eimeria etrumei Dogiel, 1940

Host: Etrumeus micropus, Dussumieriidae.

Locality: Sea of Japan.

Organ: Testes.

Oocysts: Spherical, 33.0–36.0, without residuum (Figure 1(20)).

Sporocysts: Long and fusiform about 20.0 × 5.0, without residuum.

Reference: [7,30]

Eimeria euzeti Daoudi, Radujkovic, Marquès and Bouix, 1987

Host: Common eagle ray, Myliobatis aquila, Myliobatidae.

Locality: Kotor Bay, Adriatic Sea.

Organ: Liver.

Oocysts: Spherical 13 (12.5–14.0) without residuum (Figure 1(21)).

Sporocysts: 7.0–8.0 × 5.0–6.0 with numerous refringent granules, without Stieda body.

Sporozoites: 8.0 × 1.5 with a refringent body.

References: [19]

Eimeria evaginata Dogiel 1948

Host: Sebastes taczanowskii, Sebastidae; Steller’s sculpin Myoxocephalus stelleri, Cottidae.

Locality: Sea of Japan.

Organ: Pyloric caeca.

Oocysts: Spherical 10.0–12.0, without residuum (Figure 1(22)).

Sporocysts: Oval 6.0–6.5 × 4.5, very small residuum.

Sporozoites: Arcuate

Reference: [7,30]

Eimeria gabonensis Diouf and Toguebaye, 1994

Host: Gabon gurnard, Chelidonichthys gabonensis, Triglidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Intestine.

Oocysts: Spherical, 9.6 ± 0.6, without residuum (Figure 1(23)).

Sporocysts: 6.8 ± 0.6 long by 4.6 ± 0.5 wide, Stieda body splitlike, four refringent granular residua.

Sporozoites: Falciform.

References: [16]

Eimeria gigantea (Labbé, 1896) Reichenow, 1921

Syn: Pfeifferia gigantea Labbé, 1896, Coccidium giganteum, Labbé, 1896, Pfeifferella gigantea (Labbé, 1896) Labbé, 1899.

Host: Porbeagle, Lamna nasus (referred as Lamna cornubica), Lamnidae.

Locality: Off France (Atlantic Ocean or Mediterranean Sea?).

Organ: Spiral valve.

Oocysts: About 70.0 × 40.0.

References: [7,33,34]

Eimeria gobii Fantham, 1932

Host: Barehead goby, Caffrogobius nudiceps (referred as Gobius nudiceps), Gobiidae.

Locality: Off South Africa (Atlantic Ocean or Indian Ocean?).

Organ: Intestine.

We were unable to obtain the article describing the species or any subsequent one.

Reference: [7]

Eimeria halleri Upton, Bristol, Gardner and Duszynski, 1986

Host: Haller’s round ray, Urobatis halleri (referred as Urolophus halleri), Urotrygonidae.

Locality: Off Mexico, Pacific Ocean.

Organ: Spiral valve.

Oocysts: Spherical or subspherical, 16.8 (15.0–18.0), without residuum (Figure 1(24)).

Sporocysts: Ovoid, 11.1(10.0–13.0) × 6.8 (6.0–7.5), length/thickness ratio 1.7 (1.4–2.0), with Stieda and substieda bodies. Granular particles or a spherical mass residuum.

Sporozoites: Comma-shaped, 9.9 (9.0–11.0) × 3.2 (2.8–4.0) with ovoid posterior and spherical anterior refractile bodies.

References: [35]

Eimeria harpodoni Setna and Bana, 1935

Host: Bombay-duck, Harpadon nehereus, Synodontidae.

Locality: Off Bombay, Indian Ocean.

Organ: Intestine.

Oocysts: Spherical, 14 (12–16) large honeycomb-like residuum (Figure 2(25)).

Sporocysts: Elliptical, 9.6 × 4.6, with a neck and an inverted V-shaped appendage, small granular residuum.

Sporozoites: Curved.

Reference: [7,13,15]

Eimeria hexagona Lom and Dyková, 1981

Host: Shore rockling, Gaidropsarus mediterraneus (referred as Onos tricirratus), Gaidropsaridae.

Locality: Banyuls-sur-Mer, Mediterranean Sea.

Organ: Pyloric caeca, intestine.

Oocysts: Average 12, without residuum (Figure 2(26)).

Sporocysts: Ovoid to ellipsoidal 7 (6.8–7.2) × 6 (5.8–6.4), with a collar-like encircling the Stieda body, coarsely granular residuum.

Sporozoites: Sausage-like.

Reference: [7,13,26]

Eimeria insignis Lom and Dyková, 1982

Host: Small red scorpionfish, Scorpaena notate, Scorpaenidae.

Locality: Banyuls-sur-Mer, Mediterranean Sea.

Organ: Pyloric caeca.

Oocysts: Spherical, 12 (10–13), without residuum.

Sporocysts: Ellipsoidal 7.0 (6.8–7.4) × 5.2 (4.8–5.4), without Stieda body; no discernible suture indicative of two shell valves, without residuum (Figure 2(27)).

Sporozoites: 4.2 × 1.4.

Reference: [7,22]

Eimeria ivanae Lom and Dyková, 1981

Host: Comber, Serranus cabrilla, Serranidae; painted comber, Serranus scriba, Serranidae.

Locality: Banyuls-sur-Mer, Mediterranean Sea; Adriatic Sea; off Senegal, Atlantic Ocean.

Organ: Pyloric caeca, intestine.

Oocysts: 10.5 (10.0–11.5), no oocyst residuum (Figure 2(28)).

Sporocysts: 5.8 (5.0–6.5) ×4.4 (4.0–4.6) with Stieda body encircled by a thickening, with granular residuum.

Sporozoites: 8.0 × 6.8.

Reference: [7,16,20,23,26]

Eimeria kayarensis Diouf and Toguebaye, 1994

Host: Brown ray, Raja miraletus, Rajidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Spiral valve.

Oocysts: Ellipsoidal 16.7 ± 1.1 × 13.9 ± 0.9, without residuum (Figure 2(29)).

Sporocysts: Ellipsoidal, with Stieda body, scattered refringent granular residuum.

Sporozoites: Falciform.

Reference: [16]

Eimeria kotorensis Daoudi, Radujkovic, Marquès and Bouix, 1987

Host: Blotched picarel, Spicara maena, Sparidae.

Locality: Kotor Bay, Adriatic Sea.

Organ: Intestine.

Oocysts: Round, 13.0–14.5 (Figure 2(30)).

Sporocysts: Ellipsoids 10.0 (9.5–11.0) × 6.0 (5.0–6.5), with Stieda body and with several central refringent granular residuum.

Sporozoites: Disposed lengthwise, vermiform, 8.5 × 2.0 with refringent granule in a middle position.

Reference: [19]

Eimeria lairdi Lom and Dyková, 1981

Host: Shorthorn sculpin, Myoxocephalus scorpius, Cottidae.

Locality: Grand Banks off the coast of New-foundland, Atlantic Ocean.

Organ: Pyloric caeca.

Oocysts: Spherical, 12.0 (10.0–15.0) often coated with a layer of amorphous substance, no residuum (Figure 2(31)).

Sporocysts: Almost spherical, 6.0 (5.0–8.0), with a wide collar-like thickening encircling Stieda body. Central, roughly granular residuum.

Sporozoites: Vermiform 8.0 × 1.5.

Reference: [7,26]

Eimeria maggieae Lom and Dyková, 1981

Host: Common Pandora, Pagellus erythrinus, Sparidae.

Locality: Banyuls-sur-Mer, Mediterranean Sea; Adriatic Sea.

Organ: Intestine.

Oocysts: Average 12, wall hardly seen.

Sporocysts: Ellipsoidal to ovoid 5.3 (4.8–5.7) × 8.0 (7.5–8.3), knob-like thickening encircling the Stieda body. Residuum not always visible.

Sporozoites: Twisted.

References: [7,20,23,26]

Eimeria merlangi Zaika, 1966

Host: Whiting, Merlangius merlangus (referred as Odontogadus merlangus euxinus), Gadidae.

Locality: Black Sea.

Organ: Intestine, gall bladder.

We were unable to obtain the article describing this species or any subsequent one.

Reference: [7]

Eimeria myoxocephali Fitzgerald, 1975

Host: Great sculpin, Myoxocephalus poliacanthocephalus, Cottidae.

Locality: US Coast of Washington, Pacific Ocean.

Organ: Intestine.

Oocysts: Spherical 37.2 (34–40), without residuum (Figure 2(32)).

Sporocysts: Small, round residuum.

Sporozoites: Elongate 16.7 × 3.7 sausage-shaped with a single refractile globule.

Reference: [7,36]

Eimeria nesowai Lom and Dyková, 1995

Host: Common silver belly, Gerres subfasciatus (referred to as Gerres ovatus), Gerreidae.

Locality: Off Australia, Pacific Ocean.

Organ: Pyloric caeca, intestine.

Oocysts: Subspherical, 12.9 (12.0–14.0), without residuum (Figure 2(33)).

Sporocysts: Ellipsoidal, 7.0 (6.5–7.5) × 4.2 (3.5–4.7), with Stieda body, without residuum.

Sporozoites: 6.5 × 1.3.

References: [37]

Eimeria nishin Fujita, 1934

Host: Pacific herring, Clupea pallasii pallassi, Clupeidae; Atlantic herring, Clupea harengus (referred as Clupea harengus harengus), Clupeidae.

Locality: Off Japan, off Russia Far East and off North American coast, Pacific Ocean.

Organ: Testes.

We were unable to obtain the article describing this species or any subsequent one.

Reference: [7]

Eimeria nucleocola Lom and Dyková, 1981

Host: shorthorn sculpin, Myoxocephalus scorpius, Cottidae.

Locality: Grand Banks, off the coast of Newfoundland, Atlantic Ocean.

Organ: Pyloric caeca.

Oocysts: 13.0 (12.0–14.0), no residuum (Figure 2(34)).

Sporocysts: Ellipsoidal, 6.8 (6.0–7.3) × 5.3 (4.9–6.0), with knob-like Stieda body hardly visible, without residuum.

Sporozoites: Sausage-like.

References: [7,13,26]

Eimeria ottojiroveci Dyková and Lom, 1983

Syn: Eimeria jiroveci Lom and Dyková, 1981 (=nomen pre-occupied)

Host: Thornback ray, Raja clavata, Rajidae; Brown ray, Raja miraletus, Rajidae.

Locality: Banyuls-sur-Mer, Mediterranean Sea; Adriatic Sea.

Organ: Spiral valve, intestine.

Oocysts: 12.0–13.0, without residuum (Figure 2(35)).

Sporocysts: 8.3 (8.0–8.5) × 6.3 (6.0–6.5), prominent protruding knob-like Stieda body, large granular residuum.

Sporozoites: 11.0 × 1.8, with one pointed and one rounded end.

References: [7,20,23,26]

Eimeria palavensis Marquès and Capapé, 2001

Host: Blackmouth catshark, Galeus melastomus, Carcharhiniformes, Pentanchidae.

Locality: Off Languedoc, Mediterranean Sea.

Organ: Spiral valve, intestine.

Oocysts: Round, 12.7 (12.0–14.4), with residuum (Figure 2(36)).

Sporocysts: Tapering toward one end and with Stieda body 10.9 (9.7–12.1) × 5.6 (4.8–6.4), with two refringent granular residua.

Sporozoites: Vermiforms, 9.1 (8.8–9.4) × 2.1 (2.0–2.3).

References: [38]

Eimeria patagonensis Timi and Sardella, 1998

Host: Argentine anchovy, Engraulis anchoita, Engraulidae.

Locality: Off Argentina, Atlantic Ocean.

Organ: Testes.

Oocysts: Spherical 43.3 (43.0–44.1), residuum with three to four coarse refringent granules immersed in a thin mass 15.5 (15.1–16.5) × 12.7 (11.9–13.0) (Figure 2(37)).

Sporocysts: Elongated and fusiform, 31.9 (30.9–33.0) × 8.0 (7.2–8.2), without Stieda body, with spherical residuum, 5.1 (4.1–6.2), arranged in a pyramid in the oocyst.

Sporozoites: Ovoid, 10.3 (8.2–12.4) × 5.3 (4.1–6.2).

References: [39]

Eimeria perciformis Diouf and Toguebaye, 1994

Host: Bastard grunt, Pomadasys incisus, Haemulidae; Dungat grouper, Epinephelus goreensis, Serranidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Intestine

Oocysts: Spherical, 9.7 ± 0.6, without residuum (Figure 2(38)).

Sporocysts: Ellipsoidal, 5.9 ± 0.8 long by 3.9 ± 0.3 wide, with Stieda body, four refringent granular residua.

Sporozoites: Falciform.

References: [16]

Eimeria petrovici Daoudi, Radujkovic, Marquès and Bouix, 1987

Host: Ocellated wrasse, Symphodus ocellatus, Labridae.

Locality: Kotor Bay, Adriatic Sea.

Organ: Intestine.

Oocysts: 12.0 (11.0–12.5), without residuum (Figure 2(39)).

Sporocysts: Ellipsoids, 8.7 (7.5–9.0) × 4.5 (4.0–5.0), with Stieda body and with several central refringent granules.

Sporozoites: 7.5 × 1.5 disposed lengthwise and with a refringent globule and striations in the roundest extremity.

References: [19,23]

Eimeria phyllopterycis Upton, Stamper, Osborn, Mumford, Zwick, Kinsel and Overstreet, 2000

Syn: Eimeria phyllopteryx Osborn, Stamper, Reimschuessel, Greenwell, Swick, and Kinsel 1999, nomen nudum.

Host: Common seadragon, Phyllopteryx taeniolatus, Syngnathidae.

Locality: United States aquarium (endemic to waters off southern Australia).

Organ: Intestine.

Oocysts: Spherical, 30.9 (28.0–34.4), without residuum (Figure 2(40)).

Sporocysts: Ellipsoidal, 24.3 (23.4–25.6) × 10.4 (9.2–11.2), shape index (length/wide) 2.33 (2.14–2.70), with Stieda and substieda bodies, numerous granules of various size residuum.

Sporozoites: 26.0–31.0 × 3.0–3.5, each with 3 refractile bodies.

References: [40]

Eimeria pleurostici Molnár and Rodhe, 1988

Host: Marilyna pleurosticta (referred as toad fish, Sphaeroides pleurosticus), Tetraodontidae.

Locality: Tasmanian Sea.

Organ: Intestine.

Oocysts: Round, 9.3 (9.1–9.6) (Figure 2(41)).

Sporocysts: Ellipsoidal/oval, 6.7 (6.3–7.0) × 4.4 (4.2–4.6), with plug-like Stieda body, and round or ellipsoidal, finely granular residuum.

Sporozoites: Vermiform.

References: [27]

Eimeria pneumatophori Dogiel, 1948

Host: Chub mackerel, Scomber japonicus (referred as Pneumatophorus japonicus), Scombridae.

Locality: Sea of Japan.

Organ: Liver.

Oocysts: Spherical, 12.5–13.0, without residuum.

Sporocysts: Oval, 5.0–6.0 ×3.5–4.0; no reference to Stieda body.

References: [7,30]

Eimeria raiarum Van den Berghe, 1937

Syn: Eimeria rajarum Diouf and Toguebaye, 1994 lapsus.

Host: Blue skate, Dipturus batis, (referred as Raja batis), Rajidae.

Locality: English Channel and French coast, Atlantic Ocean.

Organ: Intestine.

Oocysts: Spherical 17.5–28.0 with residuum 10.5–2.4.

Sporocysts: Ovoid 7.0 × 6.2 with very small residuum.

References: [7,34]

Eimeria raibauti Daoudi, Radujkovic, Marquès and Bouix, 1989

Host: Poor cod, Trisopterus minutus, Gadidae; Norway pout, Trisopterus esmarkii, Gadidae.

Locality: Adriatic Sea; Mediterranean Sea; North Sea, Atlantic Ocean.

Organ: Pyloric caeca.

Oocysts: Spherical, 33.0 (30.0–35.0), to ovoid, 37.2 (35–40) × 30.5 (29.0–33.0), without residuum.

Sporocysts: Ovoid, 16.7 (15.5–18.5) × 10.3 (9.0–11.0) with Stieda body and substieda, hexagonal section and refringent granular residuum.

Sporozoites: Vermiforms, 15.0 × 3.5.

References: [23,41,42]

Eimeria rohdei Lom and Dyková, 1995

Host: Fan-bellied leatherjacket, Monachantus chinensis, Monachantidae.

Locality: Off Australia, Pacific Ocean.

Organ: Pyloric caeca.

Oocysts: Spherical, 7.5 (7.0–8.5) (Figure 2(42)).

Sporocysts: Ellipsoidal 5.1 (4.5–6.0) × 3.0 (2.5–3.5), fine granular residuum, very small Stieda body.

Sporozoites: Curved, 5.0 × 1.0.

References: [37]

Eimeria roussillona Lom and Dyková, 1981

Host: Labrus viridis (referred as Labrus turdus), Labridae.

Locality: Banyuls-sur-Mer, Mediterranean Sea.

Organ: Intestine.

Oocysts: 11.0 (10.0–12.0) (Figure 2(43)).

Sporocysts: Elongate ellipsoids, 7.8 (7.5–8.5) × 4.1 (3.5–4.5), with Stieda body, refractile granular residuum.

Sporozoites: Sausage-like, 10.6 × 1.2.

References: [7,26]

Eimeria ryptici Diouf and Toguebaye, 1994

Host: Spotted soapfish, Rypticus subbifrenatus, Serranidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Intestine.

Oocysts: Spherical, 8.1 ± 0.5, without residuum (Figure 2(44)).

Sporocysts: Ovoid 4.9 ± 0.3 long by 3.4 ± 0.4 wide, Stieda body split-like, three to four refringent granular residua.

Sporozoites: Falciform.

References: [16]

Eimeria sardinae (Thélohan, 1890) Reichenow, 1921

Syn: Coccidium sardinae Thélohan, 1890, Eimeria oxyphila Dobell, 1919, lapsus, Eimeria oxyspora Dobell, 1919, Eimeria snijdersi Dobell, 1920.

Host: Atlantic herring, Clupea harengus (referred as Clupea harengus harengus), Clupeidae; European pilchard, Sardina pilchardus (also referred as Clupea pilchardus), Clupeidae; round sardinella, Sardinella aurita, Clupeidae; madeiran sardinella, Sardinella maderensis, Clupeidae; South american pilchard, Sardinops sagax, Clupeidae; European sprat, Sprattus sprattus, Clupeidae; European anchovy, Engraulis encrasicolus, Engraulidae.

Locality: North Sea, Barents Sea; Baltic Sea; Adriatic Sea; Mediterranean Sea; Black Sea; White Sea; Sea of Japan.

Organ: Testes, seminiferous tubules.

Oocysts: Spherical, 33–65 (Figure 2(45)).

Sporocysts: Long, fusiform 25.0–35.0 × 7.0–8.0; ratio of length to width 3:1 or more; large refractile bodies residuum.

Sporozoites: Rod-like.

According to Diouf and Toguebaye [43] this species has three sizes of oocysts which were called micro-oocysts, meso-oocysts and macro-oocysts.

According to Morrison and Hawkins [44] sporocysts without Stieda body.

References: [7,13,20,23,30,43,44,45,46,47,48,49,50]

Eimeria scorpaenae Zaika, 1966

Host: Black scorpionfish Scorpaena porcus, Scorpaenidae.

Locality: Black Sea.

Organ: Intestine.

We were unable to obtain the article describing this species or any subsequent one.

References: [7]

Eimeria sillaginis Molnár and Rodhe, 1988

Host: Sand sillago (referred as sand whiting), Sillago ciliata, Sillaginidae.

Locality: Tasmania Sea.

Organ: Pyloric caeca, intestine.

Oocysts: Round, 8.0–9.5, without residuum (Figure 2(46)).

Sporocysts: Ellipsoidal, 5.5–7.6 × 3.0–5.0, with Stieda body appearing as

group of 3 small tubercles, round finally granular residuum.

Sporozoites: Vermiform, 4.1–6.0 × 1.5–2.0.

References: [27,37]

Eimeria smaris (Daoudi, 1987) Daoudi, Radujkovic, Marquès and Bouix, 1989

Syn: Eimeria maenae Daoudi, 1987.

Host: Picarel, Spicara smaris, Sparidae.

Locality: Adriatic Sea.

Organ: Intestine.

Oocysts: Round, 9.2 (8.0–9.5), without residuum (Figure 2(47)).

Sporocysts: Oval, 5.4 (5.0–6.5) × 4.3 (4.0–4.5), with Stieda body, several refringent granular residua.

Sporozoites: Vermiforme 5.0 × 1.5.

References: [20,41]

Eimeria southwelli Halawani, 1930

Syn: Eimeria quentini Boulard, 1977

Host: Whitespotted eagle ray, Aetobatus narinari (referred as Aetobatis narinari), Aetobatidae; cownose ray, Rhinoptera bonasus, Rhinopteridae.

Locality: Indian Ocean; Malaysia, Pacific Oceans; North Atlantic Ocean.

Organ: Serosa of the liver, spleen, spiral valve, uterine lining and celomic cavity.

Oocysts: 15–63 × 10–15, polymorphic, pear to elongate shaped, no residuum (Figure 2(48)).

Sporocysts: 10–12 pear-shaped, aligned in a row, with a ridge-like structure along the length and Stieda body. Central residuum.

Sporozoites: Club-shaped, 5.0–10.0 × 2.0.

This species causes high host mortality.

References: [7,13,33,51,52]

Eimeria sparis Sitja-Bobadilla, Palenzuela and Alvarez-Pellitero, 1996

Syn: Eimeria spari Diouf and Toguebaye, 1996.

Host: Gilthead seabream, Sparus aurata, Sparidae; Bluespotted seabream, Pagrus caeruleostictus, Sparidae.

Locality: Mediterranean Sea; Atlantic Ocean.

Organ: Intestine.

Oocysts: Spherical to subspherical, 9.4–14.6, two refractile bodies residuum (Figure 3(49)).

Sporocysts: Ellipsoidal, 6.0–9.7 × 4.0–6.5, with aster shape Stieda body, single body to a mass of granular residuum.

Sporozoites: Vermiform.

References: [6,53,54,55,56]

Eimeria syacii Diouf and Toguebaye, 1994

Host: Channel flounder, Syacium micrurum, Cyclopsettidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Intestine.

Oocysts: Spherical, 10.7 ± 1.1, without residuum (Figure 3(50)).

Sporocysts: Ellipsoidal, 6.6 ± 0.7 long by 4.1 ± 0.5 wide, with Stieda body, with compact residuum.

References: [16]

Eimeria symphodi Daoudi, Radujkovic, Marquès and Bouix, 1989

Host: Sublet, Symphodus rostratus, Labridae.

Locality: Adriatic Sea; Mediterranean Sea.

Organ: Intestine.

Oocysts: Round 17.3 (16.0–19.0), without residuum (Figure 3(51)).

Sporocysts: Oval 12.1 (11.0–13.00) × 5.8 (5.5–6.3) with Stieda body.

Sporozoites: Vermiforms, 9.0 × 2.0; two large refringent granular residua.

References: [20,23,41]

Eimeria syngnathi Yakimoff and Gousseff, 1936

Host: Black-stripped pipefish, Syngnathus abaster (referred as Syngnathus nigrolineatus), Syngnathidae.

Locality: Black Sea; Caspian Sea.

Organ: Intestine.

Oocysts: Ellipsoidal, 24.5–32.0 ×16.7–24.5, with residuum (Figure 3(52)).

Sporocysts: Ellipsoidal, 10.6–14.4 × 7.7–9.2, no reference to Stieda body.

Sporozoites: Broad clavate.

References: [7,30]

Eimeria triglae Daoudi, Radujkovic, Marquès and Bouix, 1989

Host: Tub gurnard, Chelidonichthys lucerna (referred as Trigla lucerna), Triglidae; piper gurnard, Trigla lyra, Triglidae.

Locality: Off France, Mediterranean Sea.

Organ: Pyloric caeca.

Oocysts: Round, 9.8–19.5 (Figure 3(53)).

Sporocysts: Oval, 7.3 (7.0–8.0) × 5.0 (4.5–5.5), hexagonal section and with Stieda body.

Sporozoites: Elongated and with four to six refringent granular residua.

References: [41]

Eimeria variabilis (Thélohan, 1893) Reichenow, 1921

Syn: Coccidium variabile, Thélohan, 1893; Goussia variabilis (Thélohan, 1893), Labbé, 1896.

Host: Longspined bulhead, Taurulus bubalis (referred as Cottus bubalis), Cottidae; corkwing wrasse, Symphodus melops (referred as Crenilabrus melops), Labridae; rock goby, Gobius paganellus (referred as Gobius bicolor), Gobiidae.

Locality: Celta and Irish Seas, Atlantic Ocean.

Organ: Pyloric caeca, intestine.

Oocysts: Spherical, 11.9–14.6, to subspherical 13.9–14.3 × 9.2–10.9, without residuum (Figure 3(54)).

Sporocysts: 8.5–9.2 × 5.0–5.5, a lid-like Stieda body, without residuum.

Sporozoites: Elongated with both ends flexed.

GenBank accession number: 18S rRNA: GU479674.

References: [7,13,32,57]

Eimeria zygaenae Mandal and Chakravarty, 1965

Host: Winghead shark, Euphyra blochii (referred as Sphyrna blochii), Sphyrnidae.

Locality: Indian Ocean.

Organ: Intestine

Oocysts: 12.1–14.3.

Sporocysts: About 8.8 × 5.5.

References: [7]

Epieimeria isabellae Lom and Dyková, 1982

Host: European conger, Conger conger, Congridae.

Locality: Adriatic Sea; Mediterranean Sea.

Organ: Intestine.

Oocysts: Irregular round, average 12.5 (12–14), without residuum (Figure 3(55)).

Sporocysts: Ovoid, 8.0 (7.6–8.4) × 5.5 (5–6) with collar-like apical thickening around Stieda body, lens-like substieda body, some with a single minute granular residuum.

Sporozoites: Twisted cross-wise or C-shaped, 1.5–2.0.

References: [7,13,20,22,23]

Epieimeria lomae Daoudi, Radujkovic, Marquès and Bouix, 1987

Host: Black scorpionfish, Scorpaena porcus, Scorpaenidae.

Locality: Kotor Bay, Adriatic Sea.

Organ: Pyloric caeca.

Oocysts: Spherical, 11.5 (10.0–12.0), without residuum (Figure 3(56)).

Sporocysts: Elliptic, 6.8 (6.5–7.5) × 4.7 (4.0–5.0), very small Stieda body and three to five retractile granular residua.

Sporozoites: Club shaped.

References: [19,20,23]

Epieimeria ocellata Landsberg, 1993

Host: Red drum, Sciaenops ocellatus, Sciaenidae.

Locality: Off Florida, Atlantic Ocean.

Organ: Intestine.

Oocysts: Roughly spherical, 9.6 (8.8–11.0) × 9.3 (8.0–11.0), without residuum (Figure 3(57)).

Sporocysts: Ellipsoidal, 6.9 (6.0–8.0) × 4.1 (4.0–5.0), with Stieda body.

Sporozoites: 5.6 (5.0–7.0) × 1.8 (1.0–2.0), with flexed ends.

References: [58]

Epieimeria puytoraci Daoudi, Radujkovic, Marquès and Bouix, 1989

Host: East Atlantic peacock wrasse, Symphodus tinca, Labridae.

Locality: Adriatic Sea.

Organ: Intestine.

Oocysts: Round, 13.7 (13.0–14.5), four to seven refringent and spherical residua (Figure 3(58)).

Sporocysts: Ellipsoidal 8.9 (8.5–10.0) × 5.0 (4.5–5.5), with Stieda body and several refringent granular residuum.

Sporozoites: 7.0 × 1.5.

References: [41]

Goussia aculeati Jastrzebski, 1984

Host: Three-spined stickleback, Gasterosteus aculeatus, Gasterosteidae.

Locality: Baltic Sea, Atlantic Ocean.

Organ: Intestine.

Oocysts: Subspherical, 14.5 × 11.0 (Figure 3(59)).

References: [13]

Goussia arrawarra Molnár and Rodhe, 1988

Host: Sand sillago (referred as sand whiting), Sillago ciliata, Sillaginidae.

Locality: Tasmania Sea.

Organ: Intestine.

Oocysts: Ellipsoidal, 14.5 (14.3–15.1) × 10.7 (10.1–10.9), without residuum (Figure 3(60)).

Sporocysts: Elongate ellipsoidal, 9.4 (9.3–9.6) × 4.8 (4.6–5.0), lentiform or scattered, finely granular residuum.

Sporozoites: Banana-shaped.

References: [27]

Goussia auxidis (Dogiel, 1948) Dyková and Lom, 1983

Syn: Eimeria auxidis, Dogiel, 1948.

Host: Pacific saury, Colobatis saira, Scomberesocidae; albacore, Thunnus alalunga, Scombridae; slender tuna, Allothunnus fallai, Scombridae; skipjack tuna, Katsuwonus pelamis, Scombridae; yellowfin tuna, Thunnus albacares, Scombridae; bullet tuna, Auxis rochei (referred as Auxis maru), Scombridae; Blue mackerel, Scomber australasicus, Scombridae.

Locality: Pacific Ocean.

Organ: Kidney, liver, spleen.

Oocysts: 17–37, without residuum (Figure 3(61)).

Sporocysts: 9–14 × 5–8, no Stieda body.

Sporozoites: Elongate and curve.

References: [7,30,59]

Goussia bayae Matsche, Adams and Blazer, 2019

Host: White perch, Morone americana, Moronidae.

Locality: Chesapeake Bay, Atlantic Ocean.

Organ: Hepatic bile ducts and gallbladder.

Oocysts: Subspherical, 26.2 (22.0–30.0) × 21.8 (18.0–25.0), lenght/width ratio 1.2 (1.1–1.3), with micropyle, without residuum (Figure 3(62)).

Sporocysts: Ellipsoidal, 12.6 (10.0–14.0) × 7.8 (6.0–9.0), lenght/width ratio 1.6 (1.4–1.9), 2 valves joined by a longitudinal suture, without residuum.

Sporozoites: Sligthy arcuate.

GenBank accession number: 18S rRna: MH758783-4; 28S rRNA: MH758782; Cytochrome oxidase I: MH792860, Cytochrome b: MH792861, Cytochrome III: MH792862.

References: [60]

Goussia bigemina Labbé, 1896

Syn: Eimeria bigemina (Labbé, 1896) Yakimoff, 1929.

Host: Small sandeel, Ammodytes tobianus, Ammodytidae.

Locality: Atlantic Ocean.

Organ: Intestine.

We were unable to obtain the article describing this species or any subsequent one.

References: [7]

Goussia caseosa Lom and Dyková, 1982

Host: Roughhead grenadier, Macrourus berglax, Macrouridae.

Locality: North-western Atlantic Ocean.

Organ: Swim bladder, gall bladder, intestine, blood vessels of mesentery.

Oocysts: Round rectangular, 42.0 (40.0–47.0), without residuum (Figure 3(63)).

Sporocysts: Ellipsoid 19.2 (18.0–20.3) × 13.6 (12.0–15.5), thick wall with two valves fused by a faintly visible suture, without residuum.

Sporozoites: C shaped 26.0 × 7.0.

References: [7,13,22,61]

Goussia clupearum (Thélohan, 1894) Labbé, 1896

Syn: Coccidium sp., Thélohan, 1892; Coccidium clupearum, Thélohan, 1894; Eimeria clupearum, (Thélohan, 1894) Doflein, 1909; Eimeria wenyoni, Dobell, 1919.

Host: Pontic shad, Alosa immaculata, Clupeidae; Atlantic herring, Clupea harengus, Clupeidae; Pacific herring, Clupea pallassii pallassii, Clupeidae; European pilchard, Sardina pilchardus (also referred as Clupea pilchardus), Clupeidae; round sardinella, Sardinella aurita, Clupeidae; madeiran sardinella, Sardinella maderensis, Clupeidae; Sprattus sprattus, Clupeidae; European anchovy, Engraulis encrasicolus, Engraulidae; Etrumeus micropus, Dussumieriidae; Atlantic mackerel, Scomber scombrus, Scombridae; Atlantic chub mackerel, Scomber colias, Scombridae; Bullet tuna, Auxis rochei, Scombridae; little tunny, Euthynnus alleteratus, Scombridae; European spratblue whiting, Micromesistius poutassou, Gadidae; pouting, Trisopterus luscus, Gadidae; False scad, Caranx rhonchus, Carangidae; lookdown, Selene vomer, Carangidae; Atlantic horse mackerel, Trachurus trachurus, Carangidae; common two banded seabream, Diplodus vulgaris, Sparidae; two-banded seabream, Diplodus prayensis, Sparidae; red porgy, Pagrus pagrus (referred as Sparus pagrus pagrus), Sparidae; blackspot picarel, Spiraca melanurus, Sparidae; West African goatfish, Pseudopeneus prayensis, Mullidae; garfish, Belone belone, Belonidae.

Locality: Adriatic Sea; Mediterranean Sea; Atlantic Ocean; Pacific Ocean.

Organ: Liver, gonads, stomach, intestine.

Oocysts: Spherical, 14.0–30.0, suture of the two valves difficult to discern (Figure 3(64)).

Sporocysts: Ellipsoidal, 8.0–12.0 × 4.0–10.0, coarse refractile granular residuum.

Sporozoites: Curved.

GenBank accession number: 18S rRNA: KT025255-56; MW006822-29; MT463280-85; MF468299-307; MF468309-313.

Considerable potential to affect the commercial value of very affected fish.

According to Xavier et al. [62,63], morphologically similar Goussia sequenced from fish hosts from family Clupeidae (Atlantic herring and European pilchard) and those sequenced from Gadidae (T. luscus and M. poutassou) clustered in two distinct clades, and those sequenced from the Atlantic chub mackerel (Scombridae) formed a different lineage.

References: [7,13,18,20,23,30,44,46,48,64,65,66,67,68,69,70]

Goussia cruciata (Thélohan, 1892) Labbé, 1896

Syn: Coccidium cruciatum Thélohan, 1892; Eimeria cruciata (Thélohan, 1892) Yakimoff, 1929.

Host: Atlantic horse mackerel, Trachurus trachurus (also referred as Caranx trachurus), Carangidae; Blue jack mackerel, Trachurus picturatus, Carangidae; Mediterranean horse mackerel, Trachurus mediterraneus, Carangidae; Chilean jack mackerel, Trachurus murphyi, Carangidae; Cape horse mackerel, Trachurus capensis, Carangidae; Cunene horse mackerel, Trachurus trecae, Carangidae; Rough scad, Trachurus lathami, Carangidae; White trevally, Pseudocaranx dentex, Carangidae.

Locality: Atlantic Ocean; Mediterranean Sea, Adriatic Sea; Pacific Ocean.

Organ: Liver.

Oocysts: Spherical, 17–26, without residuum (Figure 4(65)).

Sporocysts: Ellipsoidal, 7.0–10.0 × 5.5–8.4, two valves connected by a difficult to discern sutural line. Cluster of coarse refractile granular residuum, forming trirradiate star rarely a cross inside the oocyst.

Sporozoites: Vermiforms, 5.0–9.0 × 1.3–1.5.

References: [7,20,23,37,65,68,71,72,73,74,75]

Goussia dakarensis Diouf and Toguebaye, 1993

Host: Parrot grunt, Pomadasys perotaei, Haemulidae; bigeye grunt, Brachydeuterus auritus, Haemulidae; lesser African threadfin, Galeoides decadactylus, Polynemidae.

Locality: Off Senegal, Atlantic Ocean.

ORGAN: Liver.

Oocysts: Spherical 15.0 (13.0–17.0), without residuum (Figure 4(66)).

Sporocysts: Ellipsoid, 8.0 (7.5–9.5) × 6.9 (6.0–7.5), with sutural line and few granular residua.

Sporozoites: Falciform.

References: [66]

Goussia decapteri Diouf and Toguebaye, 1993

Host: False scad, Caranx rhonchus (referred as Decapterus rhonchus), Carangidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Liver.

Oocysts: Spherical, 16.1 (13.0–18.5), without residuum (Figure 4(67)).

Sporocysts: Ellipsoidal 7.9 (7.0–8.5) × 5.9 (5.0–7.0), arranged two in two perpendicular planes, single compact mass residuum.

Sporozoites: Falciform.

References: [66]

Goussia echinata Friend, Lovy and Hershberger, 2016

Host: Atlantic herring, Clupea harengus, Clupeidae.

Locality: NW Atlantic Ocean.

Organ: Pyloric caeca, intestine.

Oocysts: Ellipsoidal, 18.7 (18.0–19.3) × 11.1 (9.4–11.7); lenght/width 1.7 (1.5–2.0), without residuum, exogened sporulated oocysts with 3 variable long spines in each pole, 15.1 (2.9–20.8) (Figure 4(68)).

Sporocysts: 9.2 (7.8–11.1) × 4.1 (2.9–4.8); lenght/width 2.3 (1.9–3.8), with plentiful residuum.

References: [70]

Goussia emissolei Diouf and Toguebaye, 1993

Host: Barbeled houndshark, Leptocharias smithii, Leptochariidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Intestine.

Oocysts: Ellipsoidal 19.3 (16.0–22.0) × 15.2 (11.5–18.0), without residuum (Figure 4(69)).

Sporocysts: 9.8 (9.0–12.0) × 7.5 (6.5–8.5), thin sutural line, few refringent granular residua.

Sporozoites: Falciform.

References: [66]

Goussia ethmalotis Obiekezie, 1986

Host: Bonga shad, Ethmalosa fimbriata, Clupeidae.

Locality: Off Nigeria, Atlantic Ocean.

Organ: Liver.

Oocysts: Spherical 30.0–37.0, whitout residuum (Figure 4(70)).

Sporocysts: 12.0 (10.0–13.0) × 6.5 (6.0–8.0), with dehiscence suture line, without residuum.

Sporozoites: Reflexed at both ends, arranged crosswise like a “x”.

References: [76]

Goussia exoceti Diouf and Toguebaye, 1993

Host: Fourwing flyingfish, Hirundichthys affinis, Exocoetidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Liver.

Oocysts: Irregular in shape, often ellipsoidal, 26.1 (23.0–30.0) × 22.9 (22.0–25.0), without residuum (Figure 4(71)).

Sporocysts: Ellipsoidal, 12.3 (11.0–14.5) × 8.7 (7.5–9.5), few refringent granular residua.

Sporozoites: Falciform.

References: [66]

Goussia floridana Landsberg, 1993

Host: Red drum, Sciaenops ocellatus, Sciaenidae.

Locality: Off Florida, Atlantic Ocean.

Organ: Pyloric caeca, intestine.

Oocysts: Subspherical, 19.9 (19.0–21.0) × 15.9 (14.0–18.0), without residuum (Figure 4(72)).

Sporocysts: Ellipsoidal, 12.6 (11.0–14.0) × 7.5 (7.0–9.0) indistinct suture line, 1 to 14 granular residua.

Sporozoites: 11.0 (10.0–12.0) × 3.9 (3.0–4.0).

References: [58]

Goussia gadi (Fiebiger, 1913) Dyková and Lom, 1981

Syn: Eimeria gadi Fiebiger, 1913; Eimeria (Goussia) gadi Fiebiger, 1913; Eimeria (Goussia) gadi (Fiebiger, 1913) Grassé, 1953; Eimeria jadviagae Grabda, 1983.

Host: Fourbeard rockling, Enchelyopus cimbrius, Gaidropsaridae; haddock, Melanogrammus aeglefinus (referred as Gadus aeglefinus), Gadidae; Atlantic cod, Gadus morhua, Gadidae; saithe, Pollachius virens (referred as Gadus virens), Gadidae; haddock, Melanogrammus aeglefinus, Gadidae; bigeye grenadier, Macrourus holotrachys (refered as Coryphaenoides holotrachis), Macrouridae; Coryphaenoides ferrieri, Macrouridae.

Locality: Atlantic Ocean.

Organ: Swimbladder.

Oocysts: Spherical, 20.0–33.0 (Figure 4(73)).

Sporocysts: 11.0–15.0 × 7.5–10.0.

Sporozoites: C-shaped 16.0 × 4.0.

Can render a non-functional swimbladder being fatal for the fish.

References: [7,13,30,46,77]

Goussia girellae Kent, Fournie, Snodgrass and Elston, 1988

Host: Opaleye, Girella nigricans, Girellidae.

Locality: Californian tide pools, Pacific Ocean.

Organ: Gills, intestine, liver and spleen.

Oocysts: Elongate 24.8 (20.1–28.8) × 14.7 (12.5–16.3), without residuum.

Sporocysts: Ellipsoidal, 8.5 (6.8–12.1) × 4.5 (4.0–5.6), no Stieda body, residuum in form of coarse granules.

Sporozoites: With refractile body near posterior end.

Heavily infected fishes moribund.

References: [13,78]

Goussia kuehae Székely, Borkhanuddin, Shaharom, Embong and Molnár, 2013

Syn: Eimeria sp. described by Gibson-Kueh et al. [79,80].

Host: Barramundi (referred as Asian seabass), Lates calcarifer, Latidae.

Locality: Malaysian, Vietnamese and Australian marine cultures.

Organ: Intestine.

Oocysts: Ellipsoidal 37.9 (37.0–40.0) × 29.3 (28.0–30.0), two or three pale round residua, 7.8 (7.0–8.5), and some round or amorphous compact residua, 1.0–3.5 (Figure 4(74)).

Sporocysts: Ellipsoidal, 16.2 (15.2–17.0) × 6.7 (5.7–8.0) located very loosely in the oocyst, with two valves and indistinct longitudinal suture and scattered dots residuum.

Sporozoites: Banana-shaped, 14.7 (14.0–15.7) × 2.6 (2.3–2.7).

GenBank accession number:18S rRna: JF261137-40.

References: [81]

Goussia luciae Lom and Dyková, 1982

Host: Red mullet, Mullus barbatus, (referred to as sea mullet), Mullidae.

Locality: Off France, Mediterranean Sea; Adriatic Sea.

Organ: Intestine.

Oocysts: Irregular shape, diameter 10.0 (9.5–10.8), without residuum (Figure 4(75)).

Sporocysts: Ellipsoidal 7.5 (6.8–8.0) × 5.5 (5.0–6.0), wall with two valves fused by a distinct suture line

Sporozoites: 12.0 × 1.3 C or S-shaped, one small residuum.

References: [7,20,22,23]

Goussia lucida (Labbé, 1893) Labbé, 1896

Syn: Coccidium lucidum, Labbé, 1893; Eimeria lucida, (Labbé, 1893) Reichenow, 1921; Eimeria scyllii, (Drago, 1902) Levine and Becker, 1933.

Host: Dusky smooth-hound, Mustelus canis, Triakidae; Smooth-hound, Mustelus mustelus (referred as Mustelus vulgaris), Triakidae; Lesser spotted dogfish, Scyliorhinus caniculus, Scyliorhinidae; Nursehound, Scyliorhinus stellaris (also referred as Scyllium catulus and Scyllium stellaris), Scyliorhinidae; Picked dogfish, Squalus acanthias (also referred as Acanthias vulgaris and Acanthias achantias), Squalidae; Longnose spurdog, Squalus blainvillei, Squalidae.

Locality: Atlantic Ocean; Adriatic Sea; Mediterranean Sea.

Organ: Intestine.

Oocysts: Spherical, 11.0 (10.5–11.5), without residuum (Figure 4(76)).

Sporocysts: Subspherical, 5.6 (5.0–6.0) × 5.3 (5.0–5.5), without Stieda body, residuum composed of just a few granules.

Sporozoites: 7.2 × 1.4, flexed curled around each other.

References: [7,13,20,22,23,29]

Goussia lusca Gestal and Azevedo, 2006

Host: Pouting, Trisopterus luscus, Gadidae.

Locality: North East Atlantic Ocean.

Organ: Liver.

Oocysts: 31.7 (28.8–35.4).

Sporocysts: 13.7 (13.1–14.4) × 9.2 (8.5–9.8), wall with outer multilamellated filamentous extensions.

References: [82]

Goussia microcanthi Molnár and Rodhe, 1988

Host: Stripey, Microcanthus strigatus, Microcanthidae.

Locality: Tasmania Sea.

Organ: Intestine.

Oocysts: Oval, 12.2 (11.7–13.5) × 10.9 (10.1–11.7) (Figure 4(77)).

Sporocysts: Elongated ellipsoidal, 11.0 (10.9–11.2) × 4.6 (4.5–4.7), scattered residuum.

Sporozoites: Banana-shaped.

References: [27]

Goussia motellae (Labbé, 1893) Labbé, 1896

Syn. Coccidium motellae, Labbé, 1893; Eimeria motellae, (Labbé, 1893) Yakimoff, 1929.

Host: Three-bearded rockling, Gaidropsarus vulgaris (referred as Motella tricirrata), Gaidropsaridae.

Locality: Off France, Atlantic Ocean.

Organ: Pyloric caeca and intestine.

We were unable to obtain the article describing this species or any subsequent one.

References: [7]

Goussia senegalensis Faye, 1988

Host: African forktail snapper, Apsilus fuscus, Lutjanidae; red Pandora, Pagellus bellottii, Sparidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Liver.

Oocysts: Spherical, 17.4 (15.5–9.0), without residuum (Figure 4(78)).

Sporocysts: Ovoid 9.8 (9.5–10.5) × 8.7 (8.0–9.0), with suture and some longitudinal lines and dense granular residuum.

Sporozoites: Falciform and with a transverse band one-third from posterior end.

References: [66]

Goussia soumbediounensis Diouf and Toguebaye, 1993

Host: Barbeled houndshark, Leptocharias smithii, Leptochariidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Intestine.

Oocysts: Spherical, 11.8 (10.0–14.5), without residuum (Figure 4(79)).

Sporocysts: Spherical 6.8 (5.0–9.5), with suture line, few refringent granular residuum.

Sporozoites: Falciform, with tips folded over.

References: [66]

Goussia sparis Sitja-Bobadilla, Palenzuela and Alvarez-Pellitero, 1996

Host: Gilthead seabream, Sparus aurata, Sparidae.

Locality: Mediterranean Sea; Atlantic Ocean.

Organ: Intestine.

Oocysts: 17.4 (16.0–21.0) × 14.4 (13.0–18.0), without residuum (Figure 4(80)).

Sporocysts: 9.5 (8.6–10.3) × 6.5 (5.7–7.4), with scarcely visible suture line, several granular residuum.

Sporozoites: Vermiforms, 9.3 (9.2–9.7) × 3.2 (3.2–3.5).

References: [6]

Goussia spraguei Morrison and Poyton, 1989

Host: Atlantic cod, Gadus morhua, Gadidae; haddock, Melanogrammus aeglefinus, Gadidae.

Locality: Off Nova Scotia, Atlantic Ocean.

Organ: Kidney.

Oocysts: Spherical, average 16.2–16.8.

Sporocysts: 11.5–12.2 × 7.4–7.8, with small residuum.

Sporozoites: Curved.

References: [83,84]

Goussia squali (Fitzgerald, 1975) Lom and Dyková, 1992

Syn: Eimeria squali, Fitzgerald, 1975.

Host: Picked dogfish, Squalus acanthias, Squalidae.

Locality: US coast of Washington, Pacific Ocean.

Organ: Spiral valve.

Oocysts: Ellipsoidal with pitted wall, 24.0–36.0 × 20.0–29.0, with a large (12.4) residuum (Figure 4(81)).

Sporocysts: Unflexed, about 19.6 × 5.9.

Sporozoites: 13.6 × 2.2 slender spindle-shaped.

References: [7,13,36]

Goussia thelohani Labbé, 1896

Syn. Coccidium sp. Thélohan, 1894; Eimeria thélohani (Labbé, 1896) Yakimoff, 1929.

Host: Labrus sp., Labridae; East Atlantic peacock wrasse, Symphodus tinca, Labridae; yellowfin bream, Acanthopagrus australis Sparidae; goldlined seabream, Rhabdosargus sarda, Sparidae.

Locality: Off France, Atlantic Ocean; Adriatic Sea; off Australia, Pacific Ocean.

Organ: Liver.

Oocysts: Round, 16–23.0, without residuum (Figure 4(82)).

Sporocysts: Ovoid, 8.0–11.5 × 7.5–9.5, sutural line quite visible; with one to six refringent granular residuum.

References: [7,20,23,37]

Goussia trachinoti Diouf and Toguebaye, 1993

Host: Pompani, Trachinotus ovatus, Carangidae.

Locality: Off Senegal, Atlantic Ocean.

Organ: Liver.

Oocysts: Spherical, 10.9 (9.5–12.0), without residuum.

Sporocysts: Ovoid, 5.9 (5.5–6.5) × 4.5 (4.0–5.0), with refringent granular residuum (Figure 4(83)).

Sporozoites: Vermiform.

References: [66]

Figure 1. Diagrammatic illustrations of coccidian’s oocysts redrawn from publications referred after species name. 1—Calytospora funduli from Duszynski et al., 1979; 2—Crystallospora crystalloides from Lom and Dyková, 1992; 3—Eimeria adioryxi from Diouf and Toguebaye, 1994; 4—Eimeria anguillae from Hine, 1975; 5—Eimeria ashburneri from Diouf and Toguebaye, 1994; 6—Eimeria atherinae from Daoudi et al., 1987; 7—Eimeria banyulensis from Lom and Dyková, 1982; 8—Eimeria bouixi from Daoudi and Marquês, 1986; 9—Eimeria brevoortiana from Hardcastle, 1944; 10—Eimeria catalana from Lom and Dyková, 1981; 11—Eimeria cheilodactyli from Molnár and Rodhe, 1988; 12—Eimeria chollaensis from Upton et al., 1988; 13—Eimeria ciliatae from Molnar and Rodhe, 1988; 14—Eimeria citriformis from Bykhovskaya-Pavlovskaya et al., 1964; 15—Eimeria dakarensis from Diouf and Toguebaye, 1994; 16—Eimeria dicentrarchi from Daoudi and Marquês, 1986; 17—Eimeria dingleyi from Davies, 1978; 18—Eimeria dykovae from Molnár and Rodhe, 1988; 19—Eimeria ethmalosae from Diouf and Toguebaye, 1994; 20—Eimeria etrumei from Bykhovskaya-Pavlovskaya et al., 1964; 21—Eimeria euzeti from Daoudi et al., 1987; 22—Eimeria evaginata from Bykhovskaya-Pavlovskaya et al., 1964; 23—Eimeria gabonensis from Diouf and Toguebaye, 1994; 24—Eimeria halleri from Upton et al., 1986. Scale bar = 10 µm. Figure 1(6–10, 14, 16, 20–22) and Figure 2(25) are not to scale.

Figure 2. Diagrammatic illustrations of coccidian’s oocysts redrawn from publications referred after species name. 25—Eimeria harpodoni from Setna and Bana, 1935; 26—Eimeria hexagona from Lom and Dyková, 1992; 27—Eimeria insignis from Lom and Dyková, 1982; 28—Eimeria ivanae from Lom and Dyková, 1981; 29—Eimeria kayarensis from Diouf and Toguebaye, 1994; 30—Eimeria kotorensis from Daoudi et al., 1987; 31—Eimeria lairdi from Lom and Dyková, 1981; 32—Eimeria myoxocephali from Fitzgerald, 1975; 33—Eimeria nesowai from Lom and Dyková, 1995; 34—Eimeria nucleocola from Lom and Dyková, 1981; 35—Eimeria ottojiroveci from Lom and Dyková, 1981; 36—Eimeria palavensis Marquès and Capapé, 2001; 37—Eimeria patagonensis from Timi and Sardella, 1998; 38—Eimeria perciformis from Diouf and Toguebaye, 1994; 39—Eimeria petrovici from Daoudi et al.,1987; 40—Eimeria phyllopterycis from Upton et al., 2000; 41—Eimeria pleurostici from Molnar and Rodhe, 1988; 42—Eimeria rohdei from Lom and Dyková, 1995; 43—Eimeria roussillona from Lom and Dyková, 1981; 44—Eimeria ryptici from Diouf and Toguebaye, 1994; 45—Eimeria sardinae from Lom and Dyková, 1992; 46—Eimeria sillaginis from Molnár and Rodhe, 1988; 47—Eimeria smaris from Daoudi et al., 1989; 48—Eimeria southwelli from Halawani, 1930. Scale bar = 10 µm. Figure 2(27, 28, 30, 31, 32, 34, 35, 39, 43, and 48) are not to scale.

Figure 3. Diagrammatic illustrations of coccidian’s oocysts redrawn from publications referred after species name. 49—Eimeria sparis from Sitja-Bobadilla et al., 1996; 50—Eimeria syacii from Diouf and Toguebaye, 1994; 51—Eimeria symphodi from Daoudi et al. 1989a; 52—Eimeria syngnathi from Bykhovskaya-Pavlovskaya et al., 1964; 53—Eimeria triglae from Daoudi et al., 1989; 54—Eimeria variabilis from Lom and Dyková, 1992; 55—Epieimeria isabellae from Lom and Dyková, 1992; 56—Epieimeria lomae from Daoudi et al., 1987; 57—Epieimeria ocellata from Landsberg, 1993; 58—Epieimeria puytoraci from Daoudi et al., 1989a; 59—Goussia aculeati from Lom and Dyková, 1992; 60—Goussia arrawarra from Molnár and Rodhe, 1988; 61—Goussia auxidis from Jones, 1990; 62—Goussia bayae from Matsche et al., 2019; 63—Goussia caseosa from Lom and Dyková, 1992; 64—Goussia clupearum from Lom and Dyková, 1992. Scale bar = 10 µm. Figure 3(52, 56, and 61) are not to scale.

Figure 4. Diagrammatic illustrations of coccidian’s oocysts redrawn from publications referred after species name 65—Goussia cruciata from Lom and Dyková, 1995; 66—Goussia dakarensis from Diouf and Toguebaye, 1993; 67—Goussia decapteri from Diouf and Toguebaye, 1993; 68—Goussia echinata from Friend, Lovy and Hershberger, 2016; 69—Goussia emissolei from Diuof and Toguebaye, 1993; 70—Goussia ethmalotis from Obiekezie (1986); 71—Goussia exoceti from Diouf and Toguebaye, 1993; 72—Goussia floridana Landsberg, 1993; 73—Goussia gadi from Lom and Dyková, 1992; 74—Goussia kuehae from Székely et al., 2013; 75—Goussia luciae from Lom and Dyková, 1982; 76—Goussia lucida from Lom and Dyková, 1992; 77—Goussia microcanthi from Molnár and Rodhe, 1988; 78—Goussia senegalensis from Diouf and Toguebaye, 1993; 79—Goussia soumbediounensis from Diouf and Toguebaye, 1993; 80—Goussia sparis from Sitja-Bobadilla et al., 1996; 81—Goussia squali from Lom and Dyková, 1992; 82—Goussia thelohani from Lom and Dyková, 1995; 83—Goussia trachinoti from Diouf and Taguebaye, 1993. Scale bar = 10 µm. Figure 4(75) is not to scale.

3.2. Phylogenetic Analysis

Phylogenetic affinities of marine piscine coccidians are depicted in Supplementary Figures S1–S5. Most of the available sequences belong to Goussia clupearum (Figure S1), forming the clupearum group described by Xavier et al. [62]. Many of the unidentified sequences of coccidians infecting marine fish clustered with piscine epicellular Goussia and Eimeria (Figures S2 and S3). As reported By Xavier et al. [85], most of the coccidians so far sequenced from elasmobranchs (both rays and sharks) were basal to many Eimeriorina species infecting other non-piscine vertebrates (Figure S4). Additionally, two of such sequences were instead basal to piscine Eimeria (Figure S3). Finally, two sequences of unidentified Coccidia clustered with nodular Goussia mostly sequenced by Rosenthal et al. [4] (Figure S5).

4. Discussion

A total of 100 species of coccidians were described and reported from 60 families of marine fishes. Most species have been described from marine teleosts, with only 14 species described from marine elasmonbrachs. While roughly only a handful of marine Coccidia belong to genus Epieimeria, Calyptospora, and Crystallospora, species of the genus Goussia and Eimeria seem to typically infect marine hosts.

Most of the Goussia and Eimeria infecting marine fish species were either only reported in the works where they were described, or have been subsequently reported in only one other study (ca. 65% of the species in each genus). Therefore, it is not surprising that the current knowledge on the geographic distribution of marine Coccidia is so limited. For example, the majority of species of Goussia (60%) have only been reported from the Atlantic region, and an important fraction (ca. 16%) have also only been reported from the Pacific. Likewise, the vast majority of species of Eimeria have either been reported from the Atlantic region (25%), the Mediterranean (26%), or the Pacfic Ocean (25%). Additionally, species that were more frequently reported, besides having a wider known geographic distribution, usually have more known hosts. For example, Goussia cruciata, Goussia clupearum, and Eimeria sardinae have been reported from the Mediterranean Sea and both the Atlantic and Pacific oceans, thus appearing to be fairly cosmopolitan. The three species also appear to be host generalists, with at least Goussia clupearum and Eimeria sardinae being known to infect hosts belonging to more than one family, and Goussia cruciata being known to infect fish from at least two genera within Carangidae. Goussia thelohani was also reported from the Mediterranean Sea and the Atlantic and Pacific oceans from two different fish families, despite only being reported in four studies. Eimeria southwelli infecting rays from at least two different families has also been reported from the Mediterranean Sea and the Atlantic and Pacific oceans. These observations lead us to conclude that neither geographic range nor host range are sufficiently studied in the vast majority of marine coccidians. However, it is important to note that the existence of cryptic diversity could be common in widespread coccidians, as was found for Goussia clupearum [62,63], for which several closely related lineages were found, with most specific to each host species. It is noteworthy that G. cluperaum also exhibits high morphological variability, indicating that it may be a species complex (see overview by Xavier and Saraiva [86] regarding the “clupearum” group). A similar scenario has also been proposed for G. cruciata, although genetic data are not available to test this hypothesis [75].

Although marine coccidians began to be described more than one century ago, genetic data on marine fish coccidians have only started to be produced since 2010s, with various genetic sequences presently available in GenBank. However, genetic analysis of marine fish Coccidia has been largely disconnected from the morphological analysis of specimens, and genetic data are only available for six formally described marine coccidian species. Though generally, genetic data are still largely missing for piscine Coccidia (both freshwater and marine), phylogenetic reconstructions based on 18S rRNA permitted raising the hypothesis that Coccidia infecting aquatic organisms are basal to those infecting terrestrial taxa [87], and that Calyptospora might have diverged earlier than Goussia and Eimeria [88]. Current knowledge shows that neither Eimeria nor Goussia are monophyletic. Specifically, piscine Goussia spp. were shown to be polyphyletic with different evolutionary lineages, with the species infecting the gut clustering mostly according to their development (i.e., nodular, dispersed, and epicellular) [4]. Goussia infecting other organs (Goussia leucisci isolated from the kidney of the roach and Goussia siliculiformis sequenced from the gut mesentery of the freshwater bream) were considered to have evolved independently [4]. Furthermore, several studies genetically characterized Goussia clupearum (the type species from the genus) from different marine fishes and tissues, indicating that it is possibly a complex of species which are sister taxa to the Calyptospora [62,63]. Interestingly, G. clupearum and Calyptospora exhibit high levels of intraspecific genetic variability [62,63,88].

Our phylogenetic reconstruction, combining all available sequences of marine Coccidia, showed that most unidentified genetic lineages likely belong to Goussia (n = 11) and have phylogenetic affinities with epicellular and nodular Goussia. Those clustering with epicellular Goussia included some Coccidia sequenced from other organs than the gut, with such lineages clustering together. Three sequences retrieved from several tissues of Pagrus caeruleostictus formed a basal clade to Calyptospora; however, they could correspond to a different Goussia. For example, Goussia clupearum seems to be closely related to this group. Only four unidentified coccidian sequences clustered within Eimeria, one likely being E. variabilis (see [89]). Finally, the lineages sequenced from elasmobranchs are the most enigmatic, some being basal to Eimeria (n = 2) and others being basal to other Eimeriorina Coccidia (including Eimeria and Schellackia), infecting marine/freshwater turtles, terrestrial reptiles, birds, and mammals [85]. Unfortunately, none of the Coccidia sequenced from elasmobranchs have been formally identified. However, these patterns suggest that Coccidia infecting this host group comprise older lineages than the ones infecting other vertebrates.

5. Conclusions

Our synopsis shows that the current knowledge regarding marine fish Coccidia is still limited. It seems that a taxonomic gap does exist, exaggerated by a shortage of taxonomists [90]. This is not unexpected due to the innacessible nature of the marine environement which hinders the access to fresh fish tissues which would enable species descriptions and accurate identifications. On the contrary, genetic data are starting to be available for many coccidians infecting marine fish; however, it is necessary to merge the gap between the genetic data being produced and appropriate morphological characterization. It is also worth noting that phylogenetic inferences are currently restricted to information from a single gene (18S rRNA) and that developing new genetic markers that amplify across Coccidia is therefore essential.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ani13132119/s1, Figure S1. Bayesian phylogenetic reconstruction of available sequences of Goussia clupearum, Calyptospora and other unidentified lineages based on 558 bp of the 18S rRNA gene and HKY+G sequence model of evolution. Figure S2. Bayesian phylogenetic reconstruction of available sequences of epicellular Goussia and closely related unidentified sequences, based on 508 bp of the 18S rRNA gene and GTR+G sequence model of evolution. Figure S3. Bayesian phylogenetic reconstruction of available sequences of Eimeria and closely related unidentified sequences, based on 569 bp of the 18S rRNA gene and GTR+G sequence model of evolution. Figure S4. Bayesian phylogenetic reconstruction of available sequences of Coccidia infecting elasmobranchs based on 515 bp of the 18S rRNA gene, using GTR+G sequence model of evolution. Figure S5. Bayesian phylogenetic reconstruction of available sequences of nodular and dispersed Goussia and closely related unidentified sequences, based on 565 bp of the 18S rRNA gene and GTR+G sequence model of evolution.

Author Contributions

Conceptualization, A.S. and R.X.; methodology, A.S., J.C.E. and R.X.; formal analysis, A.S., J.C.E., C.C. and R.X.; writing—original draft preparation, A.S. and R.X.; figures redrawing, J.C.E.; writing—review and editing, A.S., J.C.E. and R.X.; funding acquisition, A.S. and R.X. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by: the European Union’s Horizon Europe research and innovation programme under grant agreement No. 101079467 (project GRINNAQUA). Views and opinions expressed are however those of the author(s) only and do not necessarily reflect those of the European Union. The European Union cannot be held responsible for them; FCT—Foundation for Science and Technology within the scope of UIDB/04423/2020 and UIDP/04423/2020. R.X. was supported by FCT under the Programa Operacional Potencial Humano—Quadro de Referência Estratégico, National funds from the European Social Fund and Portuguese Ministério da Educação e Ciência (2020.00854.CEECIND/CP1601/CT0001).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data are reported in the manuscript.

Acknowledgments

The authors acknowledge colleagues Ivonna Mladineo and Jerko Hrabar who helped us to obtain some literature, and thank Lúcia Ramires and Ana Saraiva for processing the photos from drawings. The authors also thank David James Harris for his revision of the text.

Conflicts of Interest

The authors declare no conflict of interest.

References

Tenter, A.M.; Barta, J.R.; Beveridge, I.; Duszynski, D.W.; Mehlhorn, H.; Morrisson, D.A.; Thompson, R.C.A.; Conrad, P.A. The conceptual basis for a new classification of the coccidia. Int. J. Parasitol. 2002, 32, 595–616. [Google Scholar] [CrossRef]
Jirku, M.; Modry, D.; Slapeta, J.R.; Koudela, B.; Lukes, J. The phylogeny of Goussia and Choleoeimeria (Apicomplexa; Eimeriorina) and the evolution of excystation structures in coccidia. Protist 2002, 153, 379–390. [Google Scholar] [CrossRef]
Dogga, S.K.; Bartosova-Sojkova, P.; Lukes, J.; Soldati-Favre, D. Phylogeny, Morphology, and Metabolic and Invasive Capabilities of Epicellular Fish Coccidium Goussia janae. Protist 2015, 166, 659–676. [Google Scholar] [CrossRef] [Green Version]
Rosenthal, B.M.; Dunams-Morel, D.; Ostoros, G.; Molnar, K. Coccidian parasites of fish encompass profound phylogenetic diversity and gave rise to each of the major parasitic groups in terrestrial vertebrates. Infect. Genet. Evol. 2016, 40, 219–227. [Google Scholar] [CrossRef] [Green Version]
Benajiba, M.H.; Marquès, A.; Lom, J.; Bouix, G. Ultrastructure and sporogony of Eimeria (syn. Epieimeria) anguillae (Apicomplexa) in the eel (Anguilla anguilla). J. Eukaryot. Microbiol. 1994, 41, 215–222. [Google Scholar] [CrossRef]
Sitjà-Bobadilla, A.; Palenzuela, O.; Alvarez-Pellitero, P. Light microscopic description of Eimeria sparis sp. nov. and Goussia sparis sp. nov.(Protozoa: Apicomplexa) from Sparus aurata L. (Pisces: Teleostei). Parasitol. Res. 1996, 82, 323–332. [Google Scholar] [CrossRef]
Dyková, I.; Lom, J. Fish coccidia; an annotated list of described species. Folia Parasitol. 1983, 30, 193–208. [Google Scholar]
Froese, R.; Pauly, D. FishBase World Wide Web Electronic Publication. 2023. Available online: www.fishbase.org (accessed on 19 April 2023).
Ronquist, F.; Huelsenbeck, J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19, 1572–1574. [Google Scholar] [CrossRef] [Green Version]
Darriba, D.; Taboada, G.L.; Doallo, R.; Posada, D. jModelTest 2: More models, new heuristics and parallel computing. Nat. Methods 2012, 9, 772. [Google Scholar] [CrossRef] [Green Version]
Duszynski, D.W.; Solangi, M.A.; Overstreet, R.M. A new and unusual eimerian (protozoa: Eimeriidae) from the liver of the Gulf killifish, Fundulus grandis. J. Wildl. Dis. 1979, 15, 543–552. [Google Scholar] [CrossRef] [Green Version]
Overstreet, R.M.; Hawkins, W.E.; Fournie, J.W. The coccidian genus Calyptospora n. g. and family Calyptosporidae n. fam.(Apicomplexa), with members infecting primarily fishes. J. Eukaryot. Microbiol. 1984, 31, 332–339. [Google Scholar] [CrossRef]
Lom, J.; Dyková, I. Protozoan Parasites of Fishes; Elsevier: Amsterdam, The Netherlands, 1992; p. 315. [Google Scholar]
Oliveira, M.F.T.; Hawkins, W.E.; Overstreet, R.M.; Fournie, J.W. Calyptospora funduli (Apicomplexa, Calyptosporidae) in the Liver of the Gulf Toadfish, Opsanus beta. J. Helminthol. Soc. Wash. 1993, 60, 273–277. [Google Scholar]
Setna, S.B.; Bana, M.R.H. Eimeria harpodoni n. sp., a new coccidium from harpodon nehereus (ham. & buch.). J. R. Microsc. Soc. 1935, 55, 165–169. [Google Scholar] [CrossRef]
Diouf, J.N.; Toguebaye, B.S. Study of some marine fish coccidia of the genus Eimeria Schneider, 1815 (Apicomplexa, Coccidia) from Senegal coasts. Acta Protozool. 1994, 33, 239–250. [Google Scholar]
Hine, P.M. Eimeria anguillae Leger & Hollande, 1922 parasitic in New Zealand eels. N. Z. J. Marin. Freshw. Res. 1975, 9, 239–243. [Google Scholar] [CrossRef] [Green Version]
Dyková, I.; Lom, J. Fish coccidia: Critical notes on life cycles, classification and pathogenicity. J. Fish Dis. 1981, 4, 487–505. [Google Scholar] [CrossRef]
Daoudi, F.; Radujkovic, B.; Marquès, A.; Bouix, G. Nouvelles especes de coccidies (Apicomplexa, Eimeriidae) des genres Eimeria Schneider, 1875, et Epieimeria Dykova et Lom, 1981, parasites de poissons marins de la baie de Kotor (Yougoslavie). Bull. Mus. Natl. D’histoire Nat. Paris (4e Série Sect. A) 1987, 9, 321–332. [Google Scholar] [CrossRef]
Daoudi, F.; Radujković, B.; Marquès, A.; Bouix, G. Parasites of marine fish of Montenegro: Coccidia. Acta Adriat. 1989, 30, 13–30. [Google Scholar]
Molnár, K.; Rhode, K. New coccidians from freshwater fishes of Australia. J. Fish Dis. 1988, 11, 161–169. [Google Scholar] [CrossRef]
Lom, J.; Dyková, I. Some Marine Fish Coccidia of the Genera Eimeria Schneider, Epieimeria Dykova and Lom and Goussia Labbe. J. Fish Dis. 1982, 5, 309–321. [Google Scholar] [CrossRef]
Radujkovic, B.M.; Raibaut, A. Parasites des poissons marins du Montenegro: Liste des especes de poissons avec leur parasites. Acta Adriat. 1989, 30, 307–319. [Google Scholar]
Daoudi, F.; Marquès, A. Eimeria bouixi n. sp. and Eimeria dicentrarchi n. sp. (Sporozoa-Apicomplexa), parasites from the fish Dicentrarchus labrax (Linne, 1758) in Languedoc. Ann. Sci. Nat. Zool. Biol. Anim. 1986, 8, 237–242. [Google Scholar]
Hardcastle, A. Eimeria brevoortiana, a new sporozoan parasite from menhaden (Brevoortia tyrannus), with observations on its life history. J. Parasitol. 1944, 30, 60–68. [Google Scholar] [CrossRef]
Lom, J.; Dyková, I. New Species of the Genus Eimeria (Apicomplexa, Coccidia) from Marine Fish. Z. Parasitenkd.-Parasitol. Res. 1981, 66, 207–220. [Google Scholar] [CrossRef]
Molnár, K.; Rohde, K. Seven new coccidian species from marine fishes in Australia. Syst. Parasitol. 1988, 11, 19–29. [Google Scholar] [CrossRef]
Upton, S.J.; Gardner, S.L.; Duszynski, D.W. The round stingray, Urolophus halleri (Rajiformes: Dasyatidae), as a host for Eimeria chollaensis sp. nov.(Apicomplexa: Eimeriidae). Can. J. Zool. 1988, 66, 2049–2052. [Google Scholar] [CrossRef] [Green Version]
Duszynski, D.W.; Upton, S.J.; Couch, L.; Coccidia (Eimeria and Isospora) of Elasmobranchs. NSF Grant PEET DEB 9521687. 2000. Available online: http://eimeria.unl.edu/chond.html (accessed on 19 April 2023).
Bykhovskaya-Pavlovskaya, I.; Gusev, A.; Dubinina, M.; Izyumova, N.; Smirnova, T.; Sokolovskaya, I.; Stein, G.; Schulman, S.; Epstein, V. Key to Parasites of Freshwater Fish of the USSR; Translation Published by Israel Program for Scientific Translations; Academy of Sciences of the USSR. Zoological Institute: Jerusalem, Israel, 1964. [Google Scholar]
Gjurcevic, E.; Kuzir, S.; Bazdaric, B.; Matanovic, K.; Debelic, I.; Marino, F.; Drasner, K.; Rosenthal, B.M. New data on Eimeria dicentrarchi (Apicomplexa: Eimeriidae), a common parasite of farmed European sea bass (Dicentrarchus labrax) from the mid-eastern Adriatic. Vet. Arh. 2017, 87, 77–86. [Google Scholar]
Davies, A.J. Coccidian parasites of intertidal fishes from Wales: Systematics, development, and cytochemistry. J. Protozool. 1978, 25, 15–21. [Google Scholar] [CrossRef]
Halawani, A. On a New Species of Eimeria (E. southwelli) from Aëtobatis narinari. Ann. Trop. Med. Parasitol. 1930, 24, 1–3. [Google Scholar] [CrossRef]
Van den Berghe, L. On a new coccidium, Eimeria raiarum sp. n., with special reference to the biology of the oocysts. Parasitology 1937, 29, 7–11. [Google Scholar] [CrossRef]
Upton, S.; Bristol, J.; Gardner, S.L.; Duszynski, D. Eimeria halleri sp. n. (Apicomplexa: Eimeriidae) from the round stingray, Urolophus halleri (Rajiformes: Dasyatidae). Proc. Helminthol. Soc. Wash. 1986, 53, 110–112. [Google Scholar]
Fitzgerald, P.R. New Coccidia from Spiny Dogfish Shark (Squalus acanthias) and Great Sculpin (Myoxocephalus polyacanthocephalus). J. Fish. Res. Board Can. 1975, 32, 649–651. [Google Scholar] [CrossRef]
Lom, J.; Dyková, I. Studies on protozoan parasites of Australian fishes. Notes on coccidian parasites with description of three new species. Syst. Parasitol. 1995, 31, 147–156. [Google Scholar] [CrossRef]
Marquès, A.; Capapé, C. Eimeria palavensis n. sp. (Apicomplexa: Eimeriidae) from the Blackmouth Catshark, Galesus melastomus (Pisces: Scyliorhinidae). Acta Adriat. 2001, 42, 65–70. [Google Scholar]
Timi, J.T.; Sardella, N.H. Myxosporeans and coccidians parasitic on engraulid fishes from the coasts of Argentina and Uruguay. Parasite 1998, 5, 331–339. [Google Scholar] [CrossRef] [Green Version]
Upton, S.J.; Stamper, M.A.; Osborn, A.L.; Mumford, S.L.; Zwick, L.; Kinsel, M.J.; Overstreet, R.M. A new species of Eimeria (Apicomplexa, Eimeriidae) from the weedy sea dragon Phyllopteryx taeniolatus (Osteichthyes: Syngnathidae). Dis. Aquat. Org. 2000, 43, 55–59. [Google Scholar] [CrossRef] [Green Version]
Daoudi, F.; Radujkovic, B.; Marquès, A.; Bouix, G. New species of Coccidia Eimeriidae belonging to genera Eimeria Schneider, 1875, and Epieimeria Dykova et Lom, 1981, parasites of Mediterranean marine fishes. Bull. Mus. Natl. Hist. Nat. Fr. 4 Ser. A Zool. Biol. Ecol. Anim. 1989, 11, 743–753. [Google Scholar]
Costa, G.; MacKenzie, K.; Pike, A.W. New host and locality records for two protozoan (Myxosporea, Coccidia) parasites of marine fishes. J. Parasitol. 1991, 77, 318–319. [Google Scholar] [CrossRef]
Diouf, J.; Toguebaye, B. Eimeria sardinae Reichenow, 1921 (Apicomplexa, Coccidia) infection in Sardinella maderensis (Lowe, 1839) (Clupeidae) from the Senegal coast. Bull. Eur. Assoc. Fish Pathol. 1994, 14, 41–43. [Google Scholar]
Morrison, C.M.; Hawkins, W.E. Coccidians in the Liver and Testis of the Herring Clupea harengus L. Can. J. Zool.-Rev. Can. Zool. 1983, 62, 480–493. [Google Scholar] [CrossRef]
Pinto, J.S. Parasitic castration in males of Sardina pilchardus (Walb) due to testicular infestation by the coccidia Eimeria sardinae (Thél.). Rev. Fac. Ciências Lisb. 1956, 44, 209–228. [Google Scholar]
Margolis, L.; Arthur, J.R. Synopsis of the Parasites of Fishes of Canada. Bull. Fish. Res. Board. Can. 1979, 199, 269. [Google Scholar]
McGladdery, S.E. Potential of Eimeria sardinae (Apicomplexa: Eimeridae) oocysts for distinguishing between spawning groups and between first- and repeat-spawning Atlantic herring (Clupea harengus harengus ). Can. J. Fish. Aquat. Sci. 1987, 44, 1379–1385. [Google Scholar] [CrossRef]
Tolonen, A.; Karlsbakk, E. The parasite fauna of the Norwegian spring spawning herring (Clupea harengus L.). ICES J. Mar. Sci. 2002, 60, 77–84. [Google Scholar] [CrossRef]
Reed, C.; MacKenzie, K.; van der Lingen, C.D. Parasites of South African sardines, Sardinops sagax, and an assessment of their potential as biological tags. Bull. Eur. Ass. Fish Pathol. 2012, 32, 41–48. [Google Scholar]
Özer, A.; Öztürk, T.; Yurakhno, V.; Kornyychuk, Y.M. First report of Eimeria sardinae (Apicomplexa: Coccidia) from the Turkish coast of the Black Sea. J. Fish. Aquat. Sci. (Su Ürünleri Derg.) 2014, 31, 151–153. [Google Scholar]
Cheung, P. Eimeria southwelli Halawani, 1930 (Apicomplexa: Coccidia) from a new host, the cownose ray, Rhinoptera bonasus Mitchill. J. Aquaric. Aquat. Sci. 1993, 6, 68–75. [Google Scholar]
Stamper, M.A.; Lewbart, G.A.; Barrington, P.R.; Harms, C.A.; Geoly, F.; Stoskopf, M.K. Eimeria southwelli infection associated with high mortality of cownose rays. J. Aquat. Anim. Health 1998, 10, 264–270. [Google Scholar] [CrossRef]
Diouf, J.N.; Toguebaye, B.S. Eimeria spari n. sp. (Apicomplexa, Emeriidae) parasite of Sparus caeruleostictus (Valenciennes, 1830), (Pisces, Sparidae) from the coast of Senegal. Parasite 1996, 3, 351–355. [Google Scholar] [CrossRef] [Green Version]
Alvarez-Pellitero, P.; Palenzuela, O.; Sitja-Bobadilla, A. Ultrastructure and cytochemistry study of Eimeria sparis (Protozoa: Apicomplexa) stages from the intestine of gilthead sea bream Sparus aurata L.(Pisces: Teleostei). Parasitol. Res. 1997, 83, 126–136. [Google Scholar] [CrossRef]
Duszynski, D.W.; Couch, L.; Upton, S.J.; Coccidia (Eimeriidae) of Perciformes. NSF–PEET DEB 9521687. 2000. Available online: http://eimeria.unl.edu/perci.html (accessed on 19 April 2023).
Bahri, S. Protozoan and myxozoan infections in wild gilthead seabream (Sparus aurata L.) from North Lake of Tunis, Tunisia. Acta Parasitol 2012, 57, 114–121. [Google Scholar] [CrossRef] [Green Version]
Davies, A.J.; Ball, S.J. The biology of fish Coccidia. Adv. Parasit. 1993, 32, 293–366. [Google Scholar] [CrossRef]
Landsberg, J.H. Two new species of coccidian parasites (Apicomplexa, Eimeriorina) from red drum Sciaenops ocellatus. Dis. Aquat. Org. 1993, 16, 83–90. [Google Scholar] [CrossRef]
Jones, J.B. Goussia auxidis (Dogiel, 1948) (Apicomplexa, Calyptosporidae) from Tuna (Pisces, Scombridae) in the South-Pacific. J. Fish Dis. 1990, 13, 215–223. [Google Scholar] [CrossRef]
Matsche, M.A.; Adams, C.R.; Blazer, V.S. Newly described coccidia Goussia bayae from white perch Morone americana: Morphology and phylogenetics support emerging taxonomy of Goussia within Piscine Hosts. J. Parasitol. 2019, 105, 1–10. [Google Scholar] [CrossRef]
Khan, R.A. Parasites causing disease in wild and cultured fish in Newfoundland. Icel. Agric. Sci. 2009, 22, 29–35. [Google Scholar]
Xavier, R.; Cardoso, J.; Barroso, R.; Nogueira, S.; Cruz, C.; Pereira, A.; Saraiva, A. Effects of Goussia infecting the blue whiting and phylogenetic placement of Goussia infecting marine fish off Northern Portugal. Parasitol. Res. 2020, 119, 2139–2147. [Google Scholar] [CrossRef]
Xavier, R.; Barroso, R.; Cardoso, J.; Cruz, C.; Pereira, A.; Saraiva, A. Phylogenetic Affinities and Infection Patterns of Goussia Infecting Sardina pilchardus from the NE Atlantic. Acta Parasitol. 2021, 66, 693–698. [Google Scholar] [CrossRef]
MacKenzie, K. Coccidiosis of the Liver of Blue Whiting; Conseil international pour l’exploration de la mer: Copenhague, Danemark, 1984; p. 4. [Google Scholar]
Kalfa-Papaioannou, A.; Athanassopoulou-Raptopoulou, F. Incidence of coccidiosis in horse-mackerel (Trachurus trachurus, T. mediterraneus, T. picturatus) and sardines (Clupea pilchardus) from the North Aegean Sea. Zent. Vet. Reihe B 1984, 31, 530–536. [Google Scholar] [CrossRef]
Diouf, J.N.; Toguebaye, B.S. Studies of coccidian parasites of fish from the coast of Senegal (West Africa): New species of the genus Goussia (Apicomplexa, Eucoccidiida, Calyptosporidae). Zool. Scr. 1993, 22, 117–126. [Google Scholar] [CrossRef]
Costa, G.; Mackenzie, K. Histopathology of Goussia clupearum (Protozoa, Apicomplexa, Coccidia) in Some Marine Fish from Scottish Waters. Dis. Aquat. Org. 1994, 18, 195–202. [Google Scholar] [CrossRef]
Abollo, E.; Calvo, M.; Pascual, S. Hepatic coccidiosis of the blue whiting, Micromesistius poutassou (Risso), and horse mackerel, Trachurus trachurus (L.), from Galician waters. J. Fish Dis. 2001, 24, 335–343. [Google Scholar] [CrossRef]
Azevedo, C. Fine structure of sporogonic stages of Goussia clupearum (Apicomplexa: Eimeriidae) in the liver of infected fish (Belone belone L.), using light and electron microscopy. Parasitol. Res. 2001, 87, 326–330. [Google Scholar] [CrossRef]
Friend, S.E.; Lovy, J.; Hershberger, P.K. Disease surveillance of Atlantic herring: Molecular characterization of hepatic coccidiosis and a morphological report of a novel intestinal coccidian. Dis. Aquat. Org. 2016, 120, 91–107. [Google Scholar] [CrossRef]
Diouf, M.; Benajiba, M.H.; Senhaji, M. Goussia cruciata (Thelohan, 1892) a hepatic coccidian parasite of the horse mackerel Trachurus trachurus (Linnaeus, 1758) from the Mediterranean coasts of northern Morocco. Bull. Eur. Assoc. Fish Pathol. 2000, 20, 219–223. [Google Scholar]
Diouf, M.; Ferrer, J.M.; Benajiba, M.H. Structure and population dynamics of Goussia cruciata (Thelohan, 1892), hepatic coccidiosis agent of the horse mackerel, Trachurus trachurus (Linnaeus, 1758) from the Moroccan Mediterranean coasts. Bull. Eur. Assoc. Fish Pathol. 2005, 25, 2–8. [Google Scholar]
Gestal, C.; Azevedo, C. Ultrastructure of Goussia cruciata (Apicomplexa: Coccidia) infecting the liver of horse mackerel, Trachurus trachurus (L.), from Ibero-Atlantic waters. J. Fish Dis. 2005, 28, 125–132. [Google Scholar] [CrossRef]
Costa, G.; Santamaria, M.T.G.; Vasconcelos, J.; Perera, C.B.; Melo-Moreira, E. Endoparasites of Trachurus picturatus (Pisces: Carangidae) from the Madeira and Canary Islands: Selecting parasites for use as tags. Sci. Mar. 2013, 77, 61–68. [Google Scholar] [CrossRef] [Green Version]
Gonzalez-Kother, P.; Gonzalez, M.T. The first report of liver coccidian Goussia cruciata in jack mackerel, Trachurus murphyi, from the South Pacific and its relationship with host variables. Parasitol. Res. 2014, 113, 3903–3907. [Google Scholar] [CrossRef]
Obiekezie, A. Goussia ethmalotis n. sp. (Apicomplexa: Sporozoea), a coccidian parasite of the West African shad, Ethmalosa fimbriata Bowditch 1825, (Pisces: Clupeidae). Z. Parasitenkd. 1986, 72, 827–829. [Google Scholar] [CrossRef]
Grabda, E. Eimeria jadvigae n. sp. (Apicomplexa: Eucoccidia), a parasite of swimming bladder of Coryphaenoides holotrachys (Guenther, 1887) off the Falklands. Acta Ichthyol. Pisc. 1983, 8, 131–140. [Google Scholar] [CrossRef] [Green Version]
Kent, M.L.; Fournie, J.W.; Snodgrass, R.E.; Elston, R.A. Goussia girellae n. sp. (Apicomplexa: Eimeriorina) in the opaleye, Girella nigricans. J. Protozool. 1988, 35, 287–290. [Google Scholar] [CrossRef]
Gibson-Kueh, S.; Thuy, N.T.N.; Elliot, A.; Jones, J.B.; Nicholls, P.K.; Thompson, R.C.A. An intestinal Eimeria infection in juvenile Asian seabass (Lates calcarifer) cultured in Vietnam—A first report. Vet. Parasitol. 2011, 181, 106–112. [Google Scholar] [CrossRef] [Green Version]
Gibson-Kueh, S.; Yang, R.; Thuy, N.T.N.; Jones, J.B.; Nicholls, P.K.; Ryan, U. The molecular characterization of an Eimeria and Cryptosporidium detected in Asian seabass (Lates calcarifer) cultured in Vietnam. Vet. Parasitol. 2011, 181, 91–96. [Google Scholar] [CrossRef] [Green Version]
Szekely, C.; Borkhanuddin, M.H.; Shaharom, F.; Embong, M.S.A.; Molnar, K. Description of Goussia kuehae n. sp. (Apicomplexa: Eimeriidae) infecting the Asian seabass, Lates calcarifer (Bloch) (Perciformes: Latidae), cultured in Malaysian fish farms. Syst. Parasitol. 2013, 86, 293–299. [Google Scholar] [CrossRef] [Green Version]
Gestal, C.; Azevedo, C. Ultrastructural aspects of hepatic coccidiosis caused by Goussia lusca n. sp (Apicomplexa: Coccidia) infecting Trisopterus luscus (Gadidae) from the NE Atlantic Ocean. Dis. Aquat. Org. 2006, 71, 25–31. [Google Scholar] [CrossRef]
Morrison, C.M.; Poynton, S. A coccidian in the kidney of the haddock, Melanogrammus aeglefinus (L.). J. Fish Dis. 1989, 12, 591–593. [Google Scholar] [CrossRef]
Morrison, C.M.; Poynton, S.L. A new species of Goussia (Apicomplexa, Coccidia) in the kidney tubules of the cod, Gadus morhua L. J. Fish Dis. 1989, 12, 533–560. [Google Scholar] [CrossRef]
Xavier, R.; Santos, J.L.; Verissimo, A. Phylogenetic evidence for an ancestral coevolution between a major clade of coccidian parasites and elasmobranch hosts. Syst. Parasitol. 2018, 95, 367–371. [Google Scholar] [CrossRef]
Xavier, R.; Saraiva, A. Coccidiosis of the liver of the blue whiting. In ICES Identification Leaflets for Diseases and Parasites in Fish and Shellfish; ICES: Copenhagen, Denmark, 2021; Volume 72, p. 7. [Google Scholar]
Jirku, M.; Jirku, M.; Obornik, M.; Lukes, J.; Modry, D. Goussia Labbe, 1896 (Apicomplexa, Eimeriorina) in Amphibia: Diversity, Biology, Molecular Phylogeny and Comments on the Status of the Genus. Protist 2009, 160, 123–136. [Google Scholar] [CrossRef]
Whipps, C.M.; Fournie, J.W.; Morrison, D.A.; Azevedo, C.; Matos, E.; Thebo, P.; Kent, M.L. Phylogeny of fish-infecting Calyptospora species (Apicomplexa: Eimeriorina). Parasitol. Res. 2012, 111, 1331–1342. [Google Scholar] [CrossRef] [Green Version]
Xavier, R.; Severino, R.; Perez-Losada, M.; Gestal, C.; Freitas, R.; Harris, D.J.; Verissimo, A.; Rosado, D.; Cable, J. Phylogenetic analysis of apicomplexan parasites infecting commercially valuable species from the North-East Atlantic reveals high levels of diversity and insights into the evolution of the group. Parasites Vectors 2018, 11, 63. [Google Scholar] [CrossRef] [Green Version]
Engel, M.S.; Ceríaco, L.M.P.; Daniel, G.M.; Dellapé, P.M.; Löbl, I.; Marinov, M.; Reis, R.E.; Young, M.T.; Dubois, A.; Agarwal, I.; et al. The taxonomic impediment: A shortage of taxonomists, not the lack of technical approaches. Zool. J. Linn. Soc. 2021, 193, 381–387. [Google Scholar] [CrossRef]

Table 1. Marine fish species and their reported coccidian species.

	Host Species	Coccidian Species
ELASMOBRANCHII
Carcharhiniformes
Leptochariidae	Leptocharias smithii	Goussia emissolei
		Goussia soumbediounensis
Pentanchidae	Galeus melastomus	Eimeria palavensis
Scyliorhinidae	Scyliorhinus caniculus	Goussia lucida
	Scyliorhinus stellaris	Goussia lucida
Sphyrnidae	Euphyra blochii	Eimeria zygaenae
Triakidae	Mustelus canis	Goussia lucida
	Mustelus mustelus	Goussia lucida
Lamniiformes
Lamnidae	Lamna nasus	Eimeria gigantea
Myliobatiformes
Aetobatidae	Aetobatus narinari	Eimeria southwelli
Myliobatidae	Myliobatis aquila	Eimeria euzeti
Rhinopteridae	Rhinoptera bonasus	Eimeria southwelli
Urotrygonidae	Urobatis halleri	Eimeria chollaensis
		Eimeria halleri
Rajiformes
Rajidae	Dipturus batis	Eimeria raiarum
	Raja clavata	Eimeria ottojiroveci
	Raja miraletus	Eimeria kayarensis
		Eimeria ottojiroveci
Squaliformes
Squalidae	Squalus acanthias	Goussia lucida
		Goussia squali
	Squalus blainvillei	Goussia lucida
ACTINOPTERI
Anguilliformes
Anguillidae	Anguilla anguilla	Eimeria anguillae
	Anguilla australis	Eimeria anguillae
	Anguilla dieffenbachiii	Eimeria anguillae
	Anguilla rostrata	Eimeria anguillae
Congridae	Conger conger	Epieimeria isabellae
Atheriniformes
Atherinidae	Atherina boyeri	Eimeria atherinae
Atherinopsidae	Menidia beryllina	Calyptospora funduli
Aulopiformes
Synodontidae	Harpadon nehereus	Eimeria harpodoni
Batrachoidiformes
Batrachoididae	Opsanus beta	Calyptospora funduli
Beloniformes
Belonidae	Belone belone	Goussia clupearum
Exocoetidae	Hirundichthys affinis	Goussia exoceti
Scomberesocidae	Colobatis saira	Goussia auxidis
Blenniiformes
Blenniidae	Blennius pholis	Eimeria dingleyi
Clinidae	Clinus superciliosus	Eimeria clini
Carangaria
Latidae	Lates calcarifer	Goussia kuehae
Polynemidae	Galeoides decadactylus	Goussia dakarensis
Carangiformes
Carangidae	Caranx rhonchus	Goussia clupearum
		Goussia cruciata
		Goussia decapteri
	Pseudocaranx dentex	Goussia cruciata
	Selene vomer	Goussia clupearum
	Trachinotus ovatus	Goussia trachinoti
	Trachurus capensis	Goussia cruciata
	Trachurus latham	Goussia cruciata
	Trachurus mediterraneus	Goussia cruciata
	Trachurus murphyi	Goussia cruciata
	Trachurus picturatus	Goussia cruciata
	Trachurus trachurus	Goussia clupearum
		Goussia cruciata
	Trachurus trecae	Goussia cruciata
Centrarchiformes
Girellidae	Girella nigricans	Goussia girellae
Latridae	Morwong fuscus	Eimeria cheilodactyli
		Eimeria dykovae
Microcanthidae	Microcanthus strigatus	Goussia microcanthi
Clupeiformes
Clupeidae	Alosa immaculata	Goussia clupearum
	Brevoortia tyrannus	Eimeria brevoortina
	Clupea harengus	Eimeria nishin
		Eimeria sardinae
		Goussia clupearum
	Clupea pallasii	Eimeria nishin
	Ethmalosa fimbriata	Eimeria ethmalosae
		Goussia ethmalotis
	Sardina pilchardus	Eimeria sardinae
		Goussia clupearum
	Sardinella aurita	Eimeria sardinae
		Goussia clupearum
	Sardinella maderensis	Eimeria sardinae
		Goussia clupearum
	Sardinops sagax	Eimeria sardinae
	Sprattus sprattus	Eimeria sardinae
		Goussia clupearum
Dussumieriidae	Etrumeus micropus	Eimeria etrumei
		Goussia clupearum
Engraulidae	Engraulis anchoita	Eimeria patagomemsis
	Engraulis encrasicolus	Eimeria sardinae
		Goussia clupearum
Cyprinodontiformes
Fundulidae	Fundulus grandis	Calyptospora funduli
	Fundulus heteroclitus	Calyptospora funduli
	Fundulus jenkinsi	Calyptospora funduli
	Fundulus pulvereus	Calyptospora funduli
	Fundulus similis	Calyptospora funduli
Eupercaria
Gerreidae	Gerres subfasciatus	Eimeria nesowai
Haemulidae	Brachydeuterus auritus	Goussia dakarensis
	Pomadasys incisus	Eimeria perciformes
	Pomadasys perotaei	Goussia dakarensis
Labridae	Bodianus speciosus	Eimeria catalana
	Labrus viridis	Eimeria roussillona
	Symphodus cinereus	Eimeria banyulensis
		Eimeria catalana
	Symphodus mediterraneus	Eimeria banyulensis
		Eimeria catalana
	Symphodus melops	Eimeria variabilis
	Symphodus ocellatus	Eimeria petrovici
	Symphodus rostratus	Eimeria symphodi
	Symphodus tinca	Epieimeria puytoraci
		Goussia thelohani
Moronidae	Dicentrarchus labrax	Eimeria bouixi
		Eimeria dicentrarchi
	Morone americana	Goussia bayae
Scaridae	Scarus hoefleri	Eimeria catalana
Sciaenidae	Sciaenops ocellatus	Epieimeria ocellata
		Goussia floridana
Sillaginidae	Sillago ciliata	Eimeria ciliatae
		Eimeria sillaginis
		Goussia arrtawarra
Sparidae	Acanthopagrus australis	Goussia thelohani
	Diplodus prayensis	Goussia clupearum
	Diplodus vulgaris	Goussia clupearum
	Pagellus bellottii	Eimeria ashburneri
		Goussia senegalensis
	Pagellus erythrinus	Eimeria maggieae
	Pagrus caeruleostictus	Eimeria ashburneriEimeria sparis
	Pagrus pagrus	Goussia clupearum
	Rhabdosargus sarda	Goussia thelohani
	Sparus aurata	Eimeria sparis
		Goussia sparis
	Spicara maena	Eimeria kotorensis
	Spicara smaris	Eimeria smaris
	Spiraca melanurus	Goussia clupearum
Gadiformes
Gadidae	Gadus morhua	Goussia gadi
		Goussia spraguei
	Melanogrammus aeglefinus	Goussia gadi
		Goussia spraguei
	Merlangius merlangus	Eimeria merlangi
	Micromesistius poutassou	Goussia clupearum
	Pollachius virens	Eimeria gadi
	Trisopterus esmarkii	Eimeria raibauti
	Trisopterus luscus	Goussia clupearum
		Goussia lusca
	Trisopterus minutus	Eimeria raibauti
Gaidropsaridae	Enchelyopus cimbrius	Goussia gadi
	Gaidropsarus mediterraneus	Crystallospora crystalloides
		Eimeria hexagona
	Gaidropsarus vulgaris	Crystallospora crystalloides
		Goussia motellae
Macrouridae	Coryphaenoides ferrieri	Goussia gadi
	Macrourus berglax	Goussia caseosa
	Macrourus holotrachys	Goussia gadi
Gobiidae	Caffrogobius nudiceps	Eimeria gobii
	Gobius paganellus	Eimeria variabilis
Holocentriformes
Holocentridae	Sargocentron hastatum	Eimeria adioryxi
Mulliformes
Mullidae	Mullus barbatus	Goussia luciae
	Pseudopeneus prayensis	Goussia clupearum
Perciformes
Agonidae	Tilesina gibbosa	Eimeria citriformis
Ammodytidae	Ammodytes tobianus	Goussia bigemina
Cottidae	Myoxocephalus poliacanthocephalus	Eimeria myoxocephali
	Myoxocephalus scorpius	Eimeria lairdi
		Eimeria nucleocola
	Myoxocephalus stelleri	Eimeria evaginata
Gasterosteidae	Gasterosteus aculeatus	Goussia aculeati
Opisthocentridae	Opinthocentrus ocellatus	Eimeria dogieli
Scorpaenidae	Scorpaena notate	Eimeria insignis
	Scorpaena porcus	Eimeria scorpaenae
		Epieimeria lomae
Serranidae	Epinephelus goreensis	Eimeria perciformes
	Serranus cabrilla	Eimeria ivanae
	Serranus scriba	Eimeria ivanae
Triglidae	Chelidonichthys gabonensis	Eimeria gabonensis
	Chelidonichthys lucerna	Eimeria triglae
	Trigla lyra	Eimeria triglae
Pleuronectiformes
Cyclopsettidae	Syacium micrurum	Eimeria syacii
Scombriformes
Scombridae	Allothunnus fallai	Goussia auxidis
	Auxis rochei	Goussia auxidis
		Goussia clupearum
	Euthynnus alleteratus	Goussia clupearum
	Katsuwonus pelamis	Goussia auxidis
	Scomber australasicus	Goussia auxidis
	Scomber colias	Goussia clupearum
	Scomber japonicus	Eimeria pneumatophori
	Scomber scombrus	Goussia clupearum
	Thunnus alalunga	Goussia auxidis
	Thunnus albacares	Goussia auxidis
Syngnathiformes
Syngnathidae	Phyllopteryx taeniolatus	Eimeria phyllopterycis
	Syngnathus abaster	Eimeria syngnathi
Tetraodontiformes
Monachantidae	Monachantus chinensis	Eimeria rohdei
Tetraodontidae	Marilyna pleurosticta	Eimeria pleurostici

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Share and Cite

MDPI and ACS Style

Saraiva, A.; Eiras, J.C.; Cruz, C.; Xavier, R. Synopsis of the Species of Coccidians Reported in Marine Fish. Animals 2023, 13, 2119. https://doi.org/10.3390/ani13132119

AMA Style

Saraiva A, Eiras JC, Cruz C, Xavier R. Synopsis of the Species of Coccidians Reported in Marine Fish. Animals. 2023; 13(13):2119. https://doi.org/10.3390/ani13132119

Chicago/Turabian Style

Saraiva, Aurélia, Jorge C. Eiras, Cristina Cruz, and Raquel Xavier. 2023. "Synopsis of the Species of Coccidians Reported in Marine Fish" Animals 13, no. 13: 2119. https://doi.org/10.3390/ani13132119

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Menu

Synopsis of the Species of Coccidians Reported in Marine Fish

Abstract

Simple Summary

Abstract

1. Introduction

2. Materials and Methods

3. Results

3.1. Species List

3.2. Phylogenetic Analysis

4. Discussion

5. Conclusions

Supplementary Materials

Author Contributions

Funding

Institutional Review Board Statement

Informed Consent Statement

Data Availability Statement

Acknowledgments

Conflicts of Interest

References

Share and Cite

Article Metrics

Article Access Statistics

Further Information

Guidelines

MDPI Initiatives

Follow MDPI