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 : 69-72

Ceratomyxa sp. 1 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 11.7% (21/180). The frequency of infection is distributed as following, 03/2012: 3.3% (1/30); 04/2012: 6.7% (2/30); 05/2012: 20% (6/30); 06/2012: 20% (6/30); 07/2012: 13.3% (4/30); 08/2012: 6.7% (2/30) ( Table 10).

Mean intensity: 154±44 spores/20µl bile/infected fish (++++++) ( Table 10).

Vouchers: Digitized photos of spores are deposited in the parasitological collection of the Museum National d’Histoire Naturelle (MNHN), Paris, Coll. No. ZS 136.

Morphological description. Vegetative stages. No vegetative stages are observed. The bile is turbid due to the presence of large number of free floating spores with bile salts and cell debris. Infrequently, the spores of this parasite are remarked in the bile mixed with scarce Triangula sp. infection ( Fig. 3 H).

Myxospores. Spores typical for the genus Ceratomyxa (n = 30 fresh spores). Mature spores are crescentshaped to arched with anterior margin convex and posterior slightly concave one in sutural view, transversely elongate in lateral view ( Figs. 3 A–I, 8A–B) measuring 8.6±1.1 (7.0–10.8) µm in length and 52.6±5.8 (42.8–61.1) µm in thickness. Posterior angle is slightly concave to slightly convex 153.8±16.9 (120–174°). Two elongated shell valves strikingly attenuate towards the extremities with pointed ends in sutural view ( Figs. 3 A–H, 8A) and with rounded ends in lateral view ( Figs. 3 I, 8B). They are sub-equal in some spores but the most, are unequal in size, with one tapering to a significantly greater degree than the other ( Figs. 3 A–I, 8A–B). The longer valve measuring 34.5±3.0 (30.6–40.5) µm while the shorter one 27.7±3.8 (20.6–33.2) µm. The suture line is straight and visible TABLE ³. Comparison of the spore measurements of the present Ceratomyxa sp.] ex S. scriba with taxonomic affinities species (measurements are in µm). Abbreviations: SL, Spore Length;, Spore Thickness; PCL, Polar Capsule Length; PCW, Polar Capsule Wiđth; ND, Not Determineđ.

Species Host (s) Locality Spore Polar capsule

SL ST PCL PCW Ceratomyxa sp.] (Present stuđy) Serranus scriba Tunisia (Gulf of Tunis) 8.6 52.6 4.2 3.6

(7/10.8) (42.8/61.1) (4/4.5) (3.2/4) sphaerulosa Thélohan (1892) *Mustelus vulgaris France (Roscoff, Monaco) (10/12) (90/100) (6/7) 5

*Galeus canis

Clupea harengus

Scullium canicula

attenuata Davis (1917) Scoliodon terranovae USA (Atlantic Ocean) 9 115 4.5 4.5 flagellifera Davis (1917) Carcharhinus sp. USA (Atlantic Ocean) 12 118 6 6 mesospora Davis (1917) * Cestracion USA (Atlantic Ocean) 8 (50/60) 4.5 4.5

zygaena

Cestracion tiburo

streptospora Davis (1917) Choetodipterus faber USA (Atlantic Ocean) 4 (34/39) 3 3

robusta Fujita (1923) *Atherestes Japan (Sea of Japan) (18/20) (115/120) 5.6 4.5

evermani

Lepidopsetta mochgorei

Microstomus kitt

tenuis Fujita (1923) * Hippoglossoides Japan (Sea of Japan) (10/15) (108/112) (4/5) (3/4)

hamiltoni

Limanda aspera Microstomus kitt

orientalis Dogiel (1948) Shulman *Sardinops sagax Russia (Sea of Japan) (7/11) (33/72) 3 3.3 1966) melanosticta

Clupea harengus pallasi

porrecta Dogiel (1948) Shulman *Gymnacanthus Russia ( Sea of Japan) (4/6) (50/60) 3 3 1966) herzensteini

Myoxocephalus brandti

Bero elegans

lepidopusi Meglitsch (1960) Lepidopus candatus New Zealanđ (Pacific Ocean) 9.9 91(72.6/99) 3(2.2/3.3) 3(2.2/3.3)

(7.7/11)

auerbachi Kabata (1962) Clupea harengus Scotlanđ (North sea) 10 75(57/92) 5(3/6) 5(3/6)

(7/13)

swaisi Abđel-Ghaffar et al. (2008a) Saurida undosquamis Egypt (Ređ sea) 7.8 51.5(43/55) 3.2 1.8

(7/9) (3/4) (1.5/2) carcharhini Glees -on & Ađlarđ Carcharhinus melanopterus Australia (Great Barrier 10 58.1 3.8 3.7 2011) Reef) (9/11.5) (46/77.5) (3.5/4) (3.5/4) Original host.

between valves ( Figs. 3 C–D). Sporoplasm homogenous with numerous sporoplasmosomes, are symmetrically situated, but extending only a short distance into each valve and contain two nuclei which each one occupied one side and rarely migrated both to one side ( Figs. 3 A–B). One capsulogenic nucleus is situated beneath one of the polar capsules ( Fig. 3 B). Two polar capsules are pyriform conspicuously separated from each other and measuring 4.2±0.2 (4.0–4.5) µm in length equaling 52.5% of spore length and 3.6±0.2 (3.2–4.0) µm in width (n = 30), they are positioned medially in the apex of spore in sutural view ( Figs. 3 A–I, 8A) and centrally of spore cavity in apical view. The polar filament forms four to five turns arranged along the longitudinal axis of the capsule. Occasionally, aberrant spores with 3 polar capsules and 3 valves are observed among the spores ( Fig. 3 J).

Taxonomic affinities. Our attempts at identification of the recent finding species follow the same considerations mentioned in the preceding species. In Mediterranean Sea, none of the Ceratomyxa spp. recorded in the study of Siau & Sakiti (1981) from some serranids in Southeast Tunisian coasts resemble morphologically or overlap within the measurements range of the current species ( Table 6). The only Mediterranean marine Ceratomyxa that shows some superficial similarity in shape and form to our species, is C. sphaerulosa Thélohan, 1892 reported from the gall bladders of numerous unrelated fishes hosts from Bergen in Norway and from Roscoff and Mediterranean off Monaco, France (Table 3). The recent species distinguishes from C. sphaerulosa by having two unequal shell valves and smaller spores and polar capsules. Furthermore, the sporoplasm deposits asymmetrically within the spores of this species on the contrary to the current studied form.

According to the parasitological reports, several species of Ceratomyxa have been properly reported from Serranidae family among the wide word; C. angusta , C. gemmaphora Meglitsch, 1960 , C. epinephela , C. reniforma , C. guishanensis Wu, Wu & Dingke, 1993 , C. brayi , C. whippsi , C. gleesoni , C. hooperi , C. nolani , C. yokoyamai Gunter & Adlard, 2009 , C. hamour Mansour, Al-Qahtani, Al-Quraishy & Abdel-Baki, 2014 and most recently C. husseini Abdel-Baki, Mansour, Al-Qahtani, Al Omar & Al-Quraishy, 2015 ( Table 6). From all these above mentioned congeneric species, the recent species is superficially similar in form to C. angusta , C. epinephela and C. yokoyamai . Nevertheless, only C. angusta has unequal shell valves as the present species, but its spores and spherical polar capsules seem to be significantly smaller. Likewise, both C. epinephela and C. yokoyamai are thinner in all levels and posses each one two spherical polar capsules.

Among the remaining Ceratomyxa spp. from clearly distinct geographical areas and hosts, C. sp. 1 is superficially closer to numerous species from unrelated marine fishes: C. attenuata , C. flagellifera , C. mesospora , C. streptospora Davis, 1917 , C. robusta , C. tenuis Fujita, 1923 , C. orientalis and C. porrecta Dogiel, 1948 (cited from Shulman 1966), C. lepidopusi Meglitsch, 1960 (previously C. elongata , see Gunter & Adlard 2010), C. auerbachi Kabata, 1962 , C. swaisi Abdel-Ghaffar, Ali, Al-Quraishy, Al-Rasheid, Al-Farraj, Abdel-Baki & Bashtar, 2008a and C. cacharhini Gleeson & Adlard, 2011 (Table 3).

However, every time the recent finding myxosporean exhibits one or more distinguishing characteristics. It differentiates from C. attenuata by having thinner spores and two pyriform polar capsules. Furthermore, the shell valves of this later species are unequal and dissimilar while one being about 15 shorter than the other and ending abruptly, the longer valve tapering gradually to a point disagreeing with the morphological features of our species. C. flagellifera is the closest to the current species in form and shape, however it has larger and thicker spores. Besides, its polar capsules are typically spherical and bigger. Although, most of the morphometric measurements coincide between the present species and C. mesospora , this later possess two equal valves and two spherical polar capsules. Furthermore, the sporoplasm are asymmetrically situated within its spores and sometimes being entirely confined to the larger valve on the contrary to the current finding. C. streptospora appears to have shorter and thinner spores compared to those of the present species and its polar capsules are spherical. C. robusta resembles to our species only in shape but no measurements overlap between both species. The spores of C. tenuis are much bigger. C. orientalis has two smaller polar capsules. The spores of C. porrecta are shorter, its shell valves are thinner and contain two spherical smaller polar capsules. The spores of both C. lepidopusi and C. auerbachi are thicker than those of our species, its valves are equal in size and its polar capsules are spherical. C. swaisi is separated from the current species by having smaller polar capsules. Moreover, the shell valves of the present finding are unequal in size and much narrower than those of C. swaisi . The average range of spores of C. carcharhini is bigger than that of our species and their polar capsules are spherical. In addition, C. carcharhini has morphologically a strongly convex anterior end and more concave posterior one compared to the slightly convex anterior end and slightly posterior one of the recent finding and is, therefore a distinct species. In light of these differences with closely related species and since no Ceratomyxa species recorded thus so far is identical, we propose to mention the recent myxozoan Ceratomyxa sp. 1 as a special species has found infecting, by the first time, the gall bladder of S. scriba in Mediterranean Sea.

Figures

FIGURE 3. Photomicrographs of Ceratomyxa sp. 1 from the gall bladder of Serranus scriba. (A – F) Variable forms of fresh mature spores in sutural view presenting the pyriform polar capsules (pc), the straight suture line (sl), the sporoplasmic nuclei (sn), the capsulogenic nucleus (cn) and the unequal valves. Scale bar = 10 µm.