Myxodavisia

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 : 76-80

Myxodavisia sp.

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 8.3% (15/180). The occurrence of infection is distributed as following, 03/2012: 3.3% (1/30); 04/2012: 6.7% (2/30); 05/2012: 6.7% (2/30); 06/2012: 16.7% (5/30); 07/2012: 6.7% (2/30); 08/2012: 10% (3/30) ( Table 10).

Mean intensity: 140±5.6 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 138.

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 cell debris.

). Abbreviations: SL, spore length; ST, spore thickness; PCL, polar capsule length; PCW, polar capsule wiđth; PA, posterior angle; ND, not đetermineđ.

Species Host (s) Site of Locality Spore Polar capsule PA (°)

infestation SL ST PCL PCW

Ceratomyxa sp.] (Present stuđy) Oblada Gall blađđer Bay of Bizerte (Tunisia) 7.9 ± 0.7 27.7 ± 2.6 3.2 ± 0.5 3.2 ± 0.5 155.4 ± 6.8 melanura (7.2/9) (24.43/30.96) (2.7/3.6) (2.7/3.6) (140/164)

Ceratomyxa sp. 2 Oblada Gall blađđer Bay of Bizerte ( Tunisia) 5.6 ± 0.2 14.6 ± 0.9 2.2 ± 0.3 1.9 ± 0.3 152 ± 14

Present stuđy) melanura (5.4/6) (13/15.6) (1.9/2.7) (1.5/2.4) (126/172)

. arcuata ( Thélohan, 1892) Pagellus Gall blađđer Northeast Atlantic, 6.8 ± 0.9 36.2 ± 2.7 3.7 ± 0.7 3.0 ± 0.2 ND

Kalavati & Mackenzie (1999) bogaraveo Međiterranean off France (6.0/9.0) (32.5/40.0) (2.5/5.0) (2.5/4.0)

anđ Italy

. arcuata Laamiri (2014) Sarpa salpa Gall blađđer Gulf of Tunis (Tunisia) 7.5 ± 0.4 35.6 ± 3.3 3.3 ± 0.4 3 ± 0.4 150.6 ± 4.2 (7/9) (30/40) (3/4) (2.5/3.5) (142/156)

. pallida Thélohan (1895) Boops boops Gall blađđer Međiterranean off France 5 25/30 ND ND ND

Sarpa salpa

. pallida Laamiri (2014) Sarpa salpa Gall blađđer Tunisia (Gulf of Tunis anđ 7.32 ± 0.61 28 ± 1.5 2.95 ± 0.47 2.92 ± 0.39 160.9± 4.6 Bay of Bizerte) (6.5/8) (26/30) (2.5/3.6) (2.5/3.6) (154/170). herouardi Georgévitch (1916) Sarpa salpa Gall blađđer Međiterranean off Monaco ND ND ND ND ND

. herouardi Laamiri (2014) Sarpa salpa Gall blađđer Tunisia(Gulf of Tunis anđ 10.5 ± 1.2 21.6 ± 1.6 3.91 ± 0.25 3.89 ± 0.27 172.5± 6.8 Bay of Bizerte) (8/12) (20/24) (3.5/4.5) (3.5/4.5) (165/180)

. diplodae Lubat et al. (1989) Diplodus Gall blađđer Međiterranean off 6 (5/7) 20 (18/22) 2.25 2 ND annularis Montenegro

. diplodae Katharios et al. Diplodus Gall blađđer Međiterranean off Greece 6.6 ± 0.5 24.0 ± 0.8 2.7 ± 0.2 2.7 ± 0.2 ND

2007) puntazzo

. sparusaurati Sitjá-Bobađilla et Sparus aurata Gall blađđer Međiterranean off Spain 5.65 ± 0.74 15.76 ± 1.01 2.79 ± 0.27 2.79 ± 0.27 ND

. (1995) anđ south Atlantic (4.5/7.5) (14/17.5) (2.2/3.4) (2.2/3.4)

. puntazzi Alama-Bermejo et al. Diplodus Gall blađđer Međiterranean off Spain 9.2 ± 0.7 29 ± 2.9 4.1 ± 0.4 4 ± 0.4 166.2 ± 7.4

2011) puntazzo (8.03/10.72) (23.83/34.5) (2.95/4.77) (2.9/4.6) (146.4/179.2)

. sp Alama-Bermejo et al. Diplodus Gall blađđer Međiterranean off Spain 9.8 ± 0.8 28.8 ± 3.7 4.1 ± 0.6 4.1 ± 1.1 164.8 ± 2

2011) annularis (7.1/13) (21.5/32.7) (3.2/5.2) (3.1/5.1) (147/ 176.2)

. sp. 1 Alama-Bermejo et al. Sparus aurata Gall blađđer Međiterranean off Spain 5 ± 0.5 17.2 ± 3.4 2.2 ± 0.4 2.1 ± 0.3 175.2 ± 4.1

2011) (3.9/5.6) (13.1/22.5) (1.6/2.7) (1.5/2.5) (166.9/179.9)

. sp. 2 Alama-Bermejo et al. Sparus aurata Gall blađđer Međiterranean off Spain 9.9 ± 0.6 20 ± 2.1 3.8 ± 0.3 3.8 ± 0.4 169.2 ± 6.5

2011) (8.7/11.4) (16.7/24.7) (3.2/4.5) (3.2/4.5) (155.4/178.8) sp. 1 Laamiri (2014) Sarpa salpa Gall blađđer Tunisia (Gulf of Tunis) 7.32± 0.52 67.98 ± 2.44 3.26 ± 0.23 3.26 ± 0.23 α =35.6 ± 12.3 (6.52/7.92) (64.9/70.1) (3/3.5) (3/3.5) (28/57) sp. 2 Laamiri (2014) Sarpa salpa Gall blađđer Tunisia (Gulf of Tunis) 9.73 ± 0.63 40.32 ± 3.83 4.2 ± 0.2 3.51 ± 0.39 150.2 ± 2.9 (9/10.5) (35/45) (4/4.5) (3/4) (146/155)

. sp. 3 Laamiri (2014) Sarpa salpa Gall blađđer Tunisia (Bay of Bizerte) 7.4 ± 0.8 30± 1.8 (28/33) 3 ± 0.41 3 ± 0.41 168.5 ± 4.2 (6.5/8.5) (2.5/3.5) (2.5/3.5) (162/172) Abbreviations: SL, spore length; ST, spore thickness; PCL, polar capsule length; PCW, polar capsule wiđth; PA, posterior angle; ND, not đetermineđ.

Species Host (s) Site of Locality Spore Polar capsule PA (°)

infestation SL ST PCL PCW

Ceratomyxa sp.] (Present stuđy) Serranus scriba Gall blađđer Tunisia (Gulf of Tunis) 8.6 ± 1.1 52.6 ± 5.8 4.2 ± 0.2 3.6 ± 0.2 153.8 ± (7/10.8) (42.8/61.1) (4/4.5) (3.2/4) 16.9 (120/174)

Ceratomyxa sp. 2 (Present stuđy) Serranus scriba Gall blađđer Tunisia (Gulf of Tunis) 6.2 ± 0.6 12.2 ± 1.4 3.1 ± 0.3 2.5 ± 0.1 169.8± 3.1 (5.2/7.2) (10.2/14) (2.6/3.5) (2.3/2.6) (165/173) angusta Meglitsch (1960) Caesioperca lepidoptera Gall blađđer New Zealanđ (Pacific 5.5 42 2.7 2.7 183 ocean) (5.1/6.2) (37/47.4) (2.3/3.4) (2.3/3.4) (176/193) gemmaphora Meglitsch (1960) Hypoplectrodes Gall blađđer New Zealanđ (Pacific 7(5.9/ 19.2 2.1 2.1 198 semicinctus ocean) 8.3) (14.2/23) (2/3.4) (2/3.4) (156/217) sp. type 1 Siau & Sakiti (1981) Epinephelus aeneus Gall blađđer Southeast Tunisian coasts (6/9) (27/60) 7 7 ND sp . type 2 Siau & Sakiti (1981) Epinephelus aeneus Gall blađđer Southeast Tunisian coasts (3.4/6.4) (11.9 / 17) 1.7 1.7 ND sp . type 1 Siau & Sakiti (1981) Epinephelus alexandrinus Gall blađđer Southeast Tunisian coasts 5.1 (12.7/25.5) (1.7/2.5) (1.7/2.5) ND sp . type 2 Siau & Sakiti (1981) Epinephelus alexandrinus Gall blađđer Southeast Tunisian coasts 3.4 (8.5/9.3) 1.7 1.7 ND sp . type 1 Siau & Sakiti (1981) Epinephelus guaza Kiđney Southeast Tunisian coasts (4.2/5.1) (11/12.7) 1.7 1.7 ND sp . type 2 Siau & Sakiti (1981) Epinephelus guaza Gall blađđer Southeast Tunisian coasts 5.1 9.3 1.2 1.2 ND. sp. Siau & Sakiti (1981) Epinephelus caninus Gall blađđer Southeast Tunisian coasts (3.4/6.4) (11.9/17) 1.7 1.7 ND epinephela Wu et al. (1993) Epinephelus akaara Gall blađđer China ( South China Sea ) 5.3(4.2/6) 35(30/44) 2.6(2.4/3) 2.6(2.4/3) ND guishanensis Wu et al. (1993) Epinephelus awora Gall blađđer China ( South China Sea ) 5.6 29.4 2 2 ND reniforma Wu et al. (1993) Epinephelus akaara Gall blađđer China ( South China Sea ) 5/7(5/9) 22.4 2.8(2.5/3) 2.8(2.5/3) ND cutmorei Gunter & Ađlarđ (2009) Epinephelus fasciatus Gall blađđer Australia ( Great Barrier 7.0 ± 0.9 16.1 ± 2.1 2.4 ± 0.25 2.3 ± 0.3 173.8 Reef ) (5.0/8.5) (12.0 21.5) (1.5/3.0) (1.5/3.0) (152/206) gleesoni Gunter & Ađlarđ (2009) Plectropomus leopardus Gall blađđer Australia ( Great Barrier 6.1 ± 0.5 19.9 ± 1.6 2.3 ± 0.2 2.2 ± 0.2 156.9 Reef ) (5.0/7.0) (16.0/22.0) (1.5/3.0) (1.5/2.5) (135/180) hooperi Gunter & Ađlarđ (2009) Epinephelus quoyanus Gall blađđer Australia ( Great Barrier 4.7 ± 0.3 12.9 ± 1.2 1.5 ± 0.2 1.4 ± 0.2 158.4 Reef ) (4.0/5.5) (10/15.5) (1.0/2.0) (1.0/2.0) (135/180) nolani Gunter & Ađlarđ (2009) Epinephelus quoyanus Gall blađđer Australia ( Great Barrier 5.1 ± 0.8 18.9 ± 5.2 1.6 ± 0.3 1.6 ± 0.25 174.1 Reef ) (3.5/7.0) (12.5/29.5) (1.0/2.0) (1.0/2.0) (144/212) whippsi Gunter & Ađlarđ (2009) Cephalopholis boenak Gall blađđer Australia ( Great Barrier 5.2 ± 0.4 14.2 ± 1.7 2.0 ± 0.2 1.6 ± 0.2 174.3 Reef ) (4.5/6.5) (11.5/18.5) (1.5/2.5) (1.5/2.0) (157/180) yokoyamai Gunter & Ađlarđ Epinephelus maculatus Gall blađđer Australia ( Great Barrier 5.4 ± 0.5 25.2 ± 2.6 2.2 ± 0.2 2.2 ± 0.2 165.7

2009) Reef) (4.5/6.5) (20.5/31.0) (2.0/2.5) (2.0/2.5) (140/180) hamour Mansouret al. (2014) Epinephelus coioides Gall blađđer Sauđi Arabia (Arabian Gulf) 7 ±0.3 16.5 ± 0.4 4 ± 0.2 3 ± 0.3 ND

(6/8) (15/18) (3/5) (2/4)

husseini Abđel-Baki et al. (2015) Cephalopholis hemistiktos Gall blađđer Sauđi Arabia 9 ± 0.2 (8/ 16 ± 4.5 ± 0.1 4.5 ± 0.1 ND

(Arabian Gulf) 9) 0.3(14/18) (4/5) (4/5) Myxospores. Spores typical for the genus Myxodavisia (n = 30 fresh spores). Mature spores are laterally elongate and elliptic to crescent-shaped spore-body in sutural view ( Figs. 5 A–E, 8E), measuring 8.9±1.2 (7.6–11.1) µm in length, 21.5±1.4 (19.3–23.5) µm in thickness and 8.6±0.9 (7.6–10.5) µm in width. The two shell valves are thin-walled with smooth surface, extended into long hollow lateral appendages that taper gradually towards a pointed ends and measuring 21± 3.3 (17.4–26.6) µm in length, the cavity of which is discontinuous with the spore cavity. The suture line is straight, visible between the valves with distinct sutural ridge most evident at anterior and posterior ends of spore ( Figs. 5 F,8E–F). Spore cavity with binucleate mass of sporoplasm which is often finely granulated, situated symmetrically and almost fill the entire spore cavity ( Figs. 5 E, 8E). The two polar capsules are spherical to sub-spherical, measuring 3.2±0.3 (2.8–3.6) µm in length and 3.0±0.1 (2.8–3.2) µm in width (n = 30), They are positioned medially in anterior part of spore in sutural view ( Figs. 5 A–E, 8E) and centrally of spore cavity in apical view ( Figs. 5 F–G, 8F). The polar filament coils four to five turns arranged along the longitudinal axis of the capsule.

Taxonomic affinities. As far as we know and according to the “synopsis” compiled by Zhao et al. (2008), none Myxodavisia spp. has been described before neither from Serranidae family nor from the Mediterranean Sea. When we compare the recent spores to the closely resembled species, we find that numerous Myxodavisia spp. are worthy for comparison. These species are: M. spinosa Davis, 1917 (previously Ceratomyxa spinosa ), M. cella Jameson, 1931 (cited from Zhao et al. 2008), M. brachiophora and M. diplocrepis Laird, 1953 , M. ophidioni Zaika, 1966 (cited from Zhao et al. 2008), M. anoplopoma Moser & Noble, 1975 , M. narvi Aseeva, 2002 and M. longifilus Asseva, 2003 ( Table 7).

The present species distinguishes from the mentioned above species by the site of infection. Based on spore morphology, it separates from M. spinosa by having bigger spores and smaller polar capsules, however, its lateral appendages are very shorter with dissimilar shape compared to those of M. spinosa (20.89 µm vs 70 µm). The available measurements of M. cella coincide within the dimensional ranges of the present species, but morphologically its distinct central chamber is more ovoid to globular unlike the current studied form. The spores of M. brachiophora are thinner, their central chambers are so globular and their polar capsules are situated asymmetrically on the contrary to our species. The present finding differentiates from M. diplocrepis by having a wider spores, its lateral appendages are longer and its polar capsules are the most spherical whereas those of M. diplocrepis are pyriform. The spores of M. ophidioni are thinner with ovoid shape and possess two bigger polar capsules. M. anoplopoma separates superficially from M. sp by having longer and thinnerspores with ovoid shape. Furthermore, its lateral appendages are longer and its polar capsules are bigger. The spores and the polar capsules of M. narvi are wider. Despite the resemblance in form and shape between the recent species and M. longifilus , the spores of this later are much thinner.

Related to the host organ, among the 30 species of Myxodavisia identified so far, only 5 species have been reported from the gall bladders of their hosts ( Zhao et al. 2008; Sarkar 2010). These species are: M. cynoglossi and M. sauridae Narasimhamurti, Kalavati, Anuradha & Padma Dorothy, 1990 (cited from Zhao et al. 2008), M. filiformis Padma Dorothy, Kalavati & Vaidchi, 1998 , M. murtii Nandi, Kalavati, Das & Nandi, 2004 and M. haldarae Sarkar, 2010 ( Table 7). A propos the spore feature morphology, M. cynoglossi and M. haldarae have both longer and thinner spores. Furthermore, the polar capsules of M. cynoglossi are almost double bigger in length than those of our species. While the appendages of M. haldarae are longer, those of M. sauridae and M. murtii are very shorter compared to those of the current species. In addition, their polar capsules are larger with a higher number of polar filament turns. In their revision, Zhao et al. (2008) mentioned that M. sauridae and M. murtii bearded a great resemblance to those of Ceratomyxa species. The current species differentiates from M. filiformis by having shorter spores, lateral appendages and spherical polar capsules. M. filiformis has pyriform and larger polar capsules that contain a lower number of polar filament turns. Thus, in view of the morphological and morphometric differences, host and locality records, it has concluded that the recent myxozoan Myxodavisia sp. is a different species that has reported for the first time from Serranidae fish family in the Mediterranean Sea.

Figures

FIGURE 5. Photomicrographs of Myxodavisia sp. from the gall bladder of Serranus scriba. (A) Mature spores in sutural view presenting the spherical polar capsules (pc) and the straight to slightly curved suture line (sl). (B – D) Fresh smear of mature spores with variable forms. (E) Mature spore showing the sporoplasmic nuclei (sn) and the Capsulogenic nucleus (cn). (F – J) Fresh mature spores in apical view, notice the presence of sutural ridges (sr) in both posterior and anterior ends and the lateral appendages (la). Scale bar = 20 µm in D, 10 µm in A – C, E – J.