Gyrodactylus magadiensis, Santos & Maina & Avenant-Oldewage, 2019

Santos, Quinton Marco Dos, Maina, John Ndegwa & Avenant-Oldewage, Annemariè, 2019, Gyrodactylus magadiensis n. sp. (Monogenea, Gyrodactylidae) parasitising the gills of Alcolapia grahami (Perciformes, Cichlidae), a fish inhabiting the extreme environment of Lake Magadi, Kenya, Parasite (Paris, France) 26 (76), pp. 1-13 : 6-9

Gyrodactylus magadiensis n. sp.

urn:lsid:zoobank.org:act:89E29993-EC14-4AA3-AAE2-C569D91B5FBD

Type host: Alcolapia grahami (Boulenger, 1912) ( Perciformes , Cichlidae )

Type locality: Lake Magadi , Eastern Rift Valley, Kenya (1 ° 53, 28.4 ,, S, 36 ° 18, 09.6 ,, E)

Infection site: Gills

Type material: Holotype: Mounted in Canada Balsam and deposited in the Iziko South African Museum , Cape Town , South Africa (accession no. SAM – A091374 ) . Paratypes: four specimens deposited in the Iziko South African Museum , Cape Town, South Africa (accession no. SAMC – A091375 to SAMC – A091378 ) ; four specimens deposited in the Natural History Museum , London, UK (accession nos. NHMUK 2019.12 .6.1 to NHMUK 2019.12.6.4); and four specimens deposited in the Royal Museum for Central Africa in Tervuren, Belgium (accession nos. M. T.39080 to M. T.390803) .

ITS rDNA sequences: Representative sequence submitted to GenBank (accession no. MN 738699).

Etymology: The species is named after Lake Magadi from which the specimens were collected.

Morphological description

( Figs. 2 and 3 , Table 3 )

Description based on 24 individuals. Specimens 267.1

(202–387.2) long, and 65 (41.4–100.1) wide at level of anterior beginning of uterus. Pharyngeal bulb 21.1 (13.8–29.7) long, with anterior bulb 19.7 (13.6–28.2) wide and posterior bulb 20.7 (14.7–32.3) wide. Intestinal crura not spreading further than anterior edge of testes. Male copulatory organ (MCO) 11.4 (9.6–13.9) long and 8.5 (6.9–10.2) wide, situated posteriorly to pharyngeal bulb, armed with one central spine and six spinelets (two large and four small) ( Figs. 2C , 3G ).

Hamuli ( Figs. 2A , 3A and B ) slender, 62.8 (53.6–73.7) long; shaft even more slender 38.6 (34.8–43.6) long; narrow point 24.2 (19.9–29.5) long ending in a sharp point. Hamulus not sharply curved, aperture angle 59.9 ° (50.1 ° –78.1 °); root straight, 22.3 (16.9–29.9) long. Dorsal bar simple, 13 (9.9–17.78) long and 2.6 (2.2–3.6) wide ( Figs. 2A , 3A and B ). Ventral bar 27.5 (22.6–33.3) long, 20.8 (14.6–26.4) wide; ventral bar processes small, anterolateral, rounded and slightly curved outward, 3 (2–4) long; ventral bar membrane ovoid, tongue-shaped with notch centrally at posterior, 18.7 (15.9–22.8) long ( Figs. 2A , 3D–F ). Marginal hooks 27.7 (23.4–30) long; hook shaft 23.1 (18.9–26) long with slight rounded swelling terminally (distally); marginal hook sickle slightly curved and tilted forward, 5.4 (4.7–6.1) long; point long and continuously curved from sickle, 4 (3–4.7) wide and distal width 3.4 (2.9–4) ( Figs. 2B , 3C ). Heel rounded strongly toward shaft; toe trapezoidal to square 1.8 (1.5–2.2) long, with sharp indentation on inferior edge between toe tip and shaft attachment point; long bridge prior to reaching marginal sickle shaft; long lateral edge of toe. Marginal hook aperture 4.4 (3.6–5.1); hook instep height 0.8 (0.62–1); filament loop 8 (6.5–9.2) long.

Molecular identity of Gyrodactylus magadiensis n. sp.

All 10 specimens produced identical sequence data for the ITS fragment analysed. The amplified region was 882 bp in length, with the size of the 18S, ITS 1, 5.8S, ITS 2, and 28S rDNA fragments 24, 385, 158, 291, and 24 bp long, respectively. Alignment of the sequence to other data retrieved from GenBank produced a 1088 bp alignment, of which 636 positions were conserved, 446 variable, and 399 parsimony informative. Gyrodactylus magadiensis n. sp. was only distantly related to most other Gyrodactylus species ( Table 4 ), most closely to Gyrodactylus branchicus Malmberg, 1964 (23.2%) and most distantly to Gyrodactylus katamba García-Vásquez, Guzmán-Valdivieso, Razo-Mendivil, and Rubio-Godoy 2018 (25.4%). Distances of 0.45–25.4% were observed between species included in these analyses, while intraspecific distances of 0.00–1.14% were seen. The latter would suggest that taxa with more than 1.14% sequence divergence are distinct species, indicating that sequences for distinct species with less than that (in this case G. katamba and Gyrodactylus lamothei 8

Q. M. Dos Santos et al.: Parasite 2019, 26, 76 Mendoza-Palmero, Sereno-Uribe and Salgado-Maldonado, 2009, and G. branchicus and G. rarus Wagener, 1910 ) need to be revised to produce a robust criteria to identify species based on ITS rDNA. Topologies of phylogenetic analyses based on ML and BI methods produced similar results, thus a single combined tree is shown in Figure 4 . In all cases, G. magadiensis n. sp. formed a distinct, well supported linage from its congeners. Gyrodactylus magadiensis n. sp. appeared to be most closely related to a clade of G. katamba and G. lamothei in all cases.

Differential diagnosis

In comparison to other Gyrodactylus species described from African cichlid fishes, the marginal hooks of G. magadiensis n. sp. are most similar to those of Gyrodactylus cichlidarum Paperna, 1968 , Gyrodactylus yacatli García-Vásquez, Hansen, Christison, Bron and Shinn, 2011 and Gyrodactylus ulinganisus García-Vásquez, Hansen, Christison, Bron and Shinn, 2011 in that the sickle is smoothly curved (except G. yacatli ) and the toe is almost square. The marginal hooks of the new species can be distinguished from these species in that the toe is more pronounced than in G. cichlidarum and G. ulinganisus ; the indentation on inferior edge between the toe tip and shaft attachment point is more pronounced than in G. cichlidarum and G. ulinganisus ; the bridge prior to reaching the marginal sickle shaft is longer than in G. cichlidarum and G. ulinganisus ; the lateral edge of the toe is longer than in G. yacatli ; and the sickle is angled forward (similar only to G. yacatli ). The heel of G. magadiensis n. sp. is also notably rounded, only slightly similar to that of Gyrodactylus thysi Vanhove, Snoeks, Volckaert and Huyse, 2011 , Gyrodactylus thlapi Christison, Shinn and van As, 2005 and the illustration of Gyrodactylus niloticus Cone, Arthur and Bondad-Reantaso, 1995 by Cone et al. [ 9] (junior synonym of G. cichlidarum [ 13]).

In terms of the ventral bar, G. magadiensis n. sp. can be differentiated from other Gyrodactylus species infecting African cichlids based on the distinct tongue shape of the membrane, medial notch in posterior of membrane, rounded lateral ends of the bar itself, and anterolateral processes rounded and slightly curved outward. These features are most similar to the ventral bar of G. cichlidarum , but specifically the shape of the membrane can easily distinguish these species. The long and narrow nature of the hamuli are reminiscent of those of G. malalai , Gyrodactylus ergensi Přikrylová, Matějusová, Musilová and Gelnar, 2009 and Gyrodactylus nyanzae Paperna, 1973 . However, the hamuli of G. magadiensis n. sp. can be distinguished by the lack of an indentation of the root above the attachment of the dorsal bar as in G. malalai and G. ergensi , and the more robust root in comparison to G. nyanzae . The MCO of G. magadiensis n. sp. has six spinelets, whereas most of the other species for African cichlids have 4, 5 or 7 (with the exception of Gyrodactylus shariffi Cone, Arthur and Bondad-Reantaso, 1995 and G. cichlidarum which can have six).

Figures

Figure 2. Line drawings of the haptoral sclerites and MCO of Gyrodactylus magadiensis n. sp. from Alcolapia grahami in Lake Magadi, Kenya. (A) Haptoral sclerites with hamulus (ha), dorsal bar (db), and ventral bar (vb); (B) marginal hook; (C) male copulatory organ (MCO). Scale bars – (A) 20 µm; (B and C) 5 µm.

Figure 3. Light (LM) and scanning electron (SEM) micrographs of the haptoral sclerites and male copulatory organ (MCO) of Gyrodactylus magadiensis n. sp. (A) Haptoral sclerites with hamulus (ha), dorsal bar (db), and marginal hooks (mh), GAP (LM); (B) hamulus (ha) and dorsal bar (db) after soft tissue digestion (SEM); (C) isolated marginal hook (SEM); (D) dorsal bar (LM); (E) dorsal view of dorsal bar (SEM); (F) ventral view of dorsal bar (SEM); (G) male copulatory organ (MCO) with large central spine and six spinelets, two large and four small (LM). Scale bars – (A and B) 20 µm; (C and G) 5 µm; (D–F) 10 µm.

Figure 4. Evolutionary history of Gyrodactylus magadiensis n. sp. based on Bayesian Inference approaches using ITS sequences for selected gyrodactylids. Statistical support for Bayesian inference (BI) and maximum likelihood (ML) methods indicated at branch nodes with posterior probabilities and bootstrap support indicated, respectively (ML/BI).