Ceratomyxa

Laamiri, Sayef, 2017, Myxosporea (Cnidaria: Myxozoa) infecting the saddled seabream Oblada melanura (L. 1758) (Teleostei: Sparidae) and the painted comber Serranus scriba (L. 1758) (Teleostei: Serranidae) in Tunisia, Zootaxa 4269 (1), pp. 61-100 : 73-76

Ceratomyxa sp. 2 ex S. scriba

Host: Serranus scriba Linnaeus, 1758 painted comber ( Perciformes : Serranidae ).

Locality: Mediterranean off Tunisia, Sidi Daoud , Gulf of Tunis (37° 01’ N 10° 55’ E) .

Site of infection: Within gall bladder.

Prevalence: The overall prevalence is 6.7% (12/180). The infection rate is distributed as following, 03/2012: 0% (0/30); 04/2012: 0% (0/30); 05/2012: 13.3% (4/30); 06/2012: 13.3% (4/30); 07/2012: 6.7% (2/30); 08/2012: 3.3% (1/30) ( Table 10).

Mean intensity: 71.8±14.5 spores/20µl bile/infected fish (+++++) ( Table 10).

Vouchers: Digitized photos of syntype spores are deposited in the parasitological collection of the Museum National d’Histoire Naturelle (MNHN), Paris, Coll. No. ZS 137.

Morphological description. Vegetative stages. No early developmental or sporogonic stages are seen for this parasite. The bile is very turbid with cell debris mixed with white grease that bordered at the external wall side of the gall bladder.

Myxospores. Spores typical for the genus Ceratomyxa (n = 30 fresh spores). Mature spores are reniform, broadly oval to globular in sutural view with anterior margin convex and posterior straight one, cylindrical in apical view ( Figs. 4 A–B,D–F, 8C–D). They are small in size, measuring 6.2±0.6 (5.2–7.2) µm in length and 12.2±1.4 (10.2–14.0) µm in thickness. Posterior angle is slightly concave to straight 169.8±3.1 (165–173°). In some spores, the posterior margin is nearly parallel to the anterior one with very little valvular taper ( Figs. 4 B, 8D). The two shell valves are almost equal in size, smoothly ovoid in lateral view with rounded ends. The suture line is straight, visible between valves but not very conspicuous. Sporoplasm, homogenous with sporoplasmosomes, are symmetrically situated and do not fill the entire spore cavity ( Figs. 4 A–F, 8C–D). It contains two nuclei placed in one side ( Fig. 4 C). The two polar capsules are in the most cases pyriform, measuring 3.1±0.3 (2.6–3.5) µm in length equaling 49.7% of spore length and 2.5±0.1 (2.3–2.6) µm in width (n = 30), they are placed medially in anterior part of spore in sutural view ( Figs. 4 A–B, 8C) and centrally of spore cavity in apical view ( Figs. 4 D–F). The polar filament forms three turns arranged along the longitudinal axis of the capsule.

Taxonomic affinities. Numerous Ceratomyxa spp. share with the current isolate species one or more morphological similitude especially after the review of genus Leptotheca (Gunter & Adlard 2010) as we mentioned above. Firstly in the Mediterranean Sea, Ceratomyxa sp. 2 resembles superficially in shape, form and size to 5 Ceratomyxa : C. agilis Thélohan, 1892 , C. hepseti Thélohan, 1895 , Ceratomyxa sp. type 2 ex Epinephelus guaza Siau & Sakiti, 1981 , C. lubati Lubat, Radujkovic, Marques & Bouix, 1989 and Ceratomyxa sp. 2 ex Sparus aurata Alama-Bermejo, Raga & Holzer, 2011 ( Table 4).

Species Host (s) Locality Spore Polar capsule SL ST PCL PCW

Ceratomyxa sp. 2 Serranus scriba Tunisia (Gulf of Tunis) 6.2 12.2 3.1 2.5

Present stuđy) (5.2/7.2) (10.2/14) (2.6/3.5) (2.3/2.6)

agilis Thélohan (1892) Dasyatis pastinaca Međiterranean anđ (6/7) (11/12) ND ND Tyrrhenian coasts

hepseti Thélohan (1895) Atherina hepsetus Off France (7/8) (12/15) ND ND

fisheri Jameson (1929) Hydrolagus colliei Off USA (5.1/7.1) (9.3/13.3) ND ND

subelegans Lairđ (1953) *Callogobius atratus, Off New Zealanđ 11.6 22.6 2.5 2.5

Diplocrepis puniceus (8.6/12.5) (19.6/26.2) (2.1/2.9) (2.1/2.9)

mylionis Ishizaki (1960) Acanthopagrus schlegelii Japan 6.2 13.3 2.3 2.3

declivis Meglitsch (1960) Cyttus novaezelandiae New Zealanđ (Pacific Ocean) 5.9 14.4 2.4 2

(5.1/6.8) (13.5/15.2) (1.7/2.2) (1.7/2.2)

faba Meglitsch (1960) Caulopsetta scapha New Zealanđ (Pacific Ocean) 6.2 12.7 2.4 2.4

(5.6/6.7) (10.7/14.1) (2/3.1) (2/3.1)

pinguis Meglitsch (1960) *Peltorhamphus New Zealanđ (Pacific Ocean) 9.7 16.4 2.9 2.9

novaezeelandiae (8.3/10.8) (13.7/18.6) (2.4/3.9) (2.4/3.9) Arnoglossus scapha

coelorhyncha Yoshino & Noble Coelorhinchus off Irelanđ 6.7(6/8) 11.34 2.01 2.01

1973) coelorhinchus (9/13) (1.5/3) (1.5/3)

Ceratomyxa sp. type 2 Siau & Sakiti Epinephelus guaza Međiterranean off Tunisia 5.1 9.3 1.2 1.2

1981) anđ French

ovalis Kovaljova & Gaevskaya Trachurus murphyi Pacific Ocean (6/6.65) (9.97/10.64) (2/2.66) (2/2.66)

1983)

lubati Lubat et al. (1989) Chromis chromis off France 6(5.5-7) 14 3 2.75 (12.5/15)

buri, Yokoyama & Fukuđa (2001) Seriola quinqueradiata Japan 6.5 (5.5/7.5) 14.3 (11/16.5) 2.4 (2/3) 2.4 (2/3)

cottoidii Reeđ et al. (2007) Clinus cottoides South Africa 7.1 (6.5/8) 18.2 (17/22) 2.7 (2.3/3) 2.4 (2/3)

cutmorei Gunter & Ađlarđ (2009) Epinephelus fasciatus Australia (Great Barrier Reef) 7 (5/8.5) 16.1 (12/21.5) 2.4 (1.5/3) 2.3 (1.5/3)

ernsti Gunter et al. (2009) Sillago ciliata Australia (Great Barrier Reef) 5.76(4.67/6.84) 11.94(9.47/14.79) 1.66(1.3/2.13) 1.58 (1.3/2)

jonesi Gunter et al. (2009) Pseudolabrus guentheri Australia (Great Barrier Reef) 5.1(4.1/6.08) 12.99(11.17/16.45) 1.92(1.55/2.3) 1.81(1.42/2.29)

reidi Gunter et al. (2010a) Chaetodon vagabundus Australia (Great Barrier Reef) 6.8 (5.8/7.5) 17.5(14.3/20.7) 2.1 (1.7/2.4) 2 (1.7/2.5)

sp 2 Alama-Bermejo et al. (2011) Sparus aurata Spain 9.9 (8.7/11.4) 20(16.7/24.7) 3.8 (3.2/4.5) 3.8 (3.2/4.5)

Original host.

Although, the dimensions of the polar capsules of C. agilis have not been given, the available measurements of Ceratomyxa sp. 2 and this species overlap. However, the spores of C. agilis are less globular to elongate in shape, its suture line are oblique and its sporoplasm fill the whole spore cavity (specific feature of Leptotheca spp.). Generally, the average range of spores of C. hepseti is larger. Furthermore, according to the original description of this species, it was noted that C. hepseti had a triangular shape in sutural view (no available illustration), so it cannot be identical to the under studied species. The recent species separates from Ceratomyxa sp. type 2 ex. E. guaza by having bigger spores and larger pyriform polar capsules. Except the width of the polar capsules, all the measurements between the current species and C. lubati overlap, but the shape of this later is more arched compared to the globular one of the recent species. Moreover, the sporoplasm of C. lubati fill the entire spore cavity. C. sp 2 ex S. aurata can be distinguished from the present species in having larger spores and bigger spherical polar capsules.

Throughout the world, under consideration of the morphological characteristics of the current finding species, 15 representatives of the genus Ceratomyxa infecting marine fishes are compared to our species. These species are: C. fisheri Jameson, 1929 (formerly L. fisheri ), C. subelegans Laird, 1953 (formerly L. subelegans ), C. mylionis Ishizaki, 1960 (syn. L. mylionis ), C. declivis C. faba and C. pinguis (syn. L. pinguis ) Meglitsch, 1960, C. coelorhyncha Yoshino & Noble, 1973 (previously L. coelorhyncha ), C. ovalis Kovaljova & Gaevskaya, 1983 , C. buri Yokoyama & Fukuda, 2001 , C. cottoidii Reed, Basson, Van As & Dyková, 2007 , C. cutmorei Gunter & Adlard, 2009 , C. ernsti and C. jonesi Gunter, Whipps & Adlard, 2009 , C. reidi Gunter, Burger & Adlard, 2010 and C. hamour Mansour, Al-Qahtani, Al-Quraishy & Abdel-Baki, 2014 ( Tables 4, 6).

Comparative study of morphological and morphometric characteristics of the spore and polar capsule with the mentioned above species confirm that the recent species C. sp. 2 differentiates from all of them. Although, the measurements of polar capsules of C. fisheri are not given, the range size of body spores for both species overlap. However, according to the original illustration of C. fisheri , its sporoplasm fill the entire spore cavity and its polar capsules appear to be spherical unlike those of the current species. The spores of C. subelegans are bigger and possess two spherical polar capsules. The recent finding separates from all species C. mylionis , C. declivis , C. faba , C. pinguis , C. coelorhyncha , C. ovalis , C. lubati , and C. buri by having bigger and/or pyriform polar capsules. Furthermore, the posterior margin of C. declivis is more concave compared to the slightly concave to straight of the present form, C. pinguis have a bigger spores while those of C. cottoidii and C. cutmorei are thicker. Moreover, the polar capsules of the latter are either spherical. C. ernsti and C. jonesi differ from the recent species in having almost spherical and smaller polar capsules. The thickness of C. reidi is larger and its polar capsules are spherical and smaller. The spores of C. hamour are thicker and less globular in shape than those of our species. Therefore, taking into account all the differences with the closely related species, host and locality new records, the recent myxosporean Ceratomyxa sp. 2 is designated as a different species, has not previously described from S. scriba in the Mediterranean Sea.

Figures

FIGURE 4. Photomicrographs of Ceratomyxa sp. 2 from the gall bladder of Serranus scriba. (A – B) Fresh mature spores in sutural view. (C) Mature spore in lateral view with two pyriform polar capsules (pc) and two sporoplasmic nuclei (sn). (D – F) Mature spores in apical view. Scale bar = 10 µm.