Three new species of Synodontella (Monogenea, Ancyrocephalidae), gill parasites of Synodontis spp. (Siluriformes, Mochokidae) from Côte d’Ivoire

Four species of Synodontella, including three new, are reported from three species of Synodontis (S. ocellifer, S. nigrita, and S. velifer) from north-western Côte d’Ivoire. Synodontella melanoptera Dossou & Euzet, 1993 was found on the gills of S. nigrita and S. velifer and was already known from the gills of S. melanopterus in Benin and the gills of S. obesus and S. rebeli in Cameroon. The new species are Synodontella speroadotevii n. sp. from S. nigrita (type-host), S. velifer and S. ocellifer, and Synodontella bagoueensis n. sp. and Synodontella akengboi n. sp., both from S. velifer (type-host for both), S. nigrita and S. ocellifer. The new species differ from the other species of Synodontella mainly in the morphology of their male copulatory organs (MCO): Synodontella speroadotevii has a two-part penis (one being a hollow tube and the other a flattened tube); Synodontella bagoueensis has a wide G-shaped penis with a sub-terminal opening; and Synodontella akengboi has a simple narrow J-shaped penis. Synodontella speroadotevii differs from Synodontella bagoueensis and Synodontella akengboi in the shape of the dorsal transverse bar, which shows no protuberance, and also in the morphology of the MCO. Synodontella bagoueensis differs from the other two species in that it has a dorsal transverse bar that is V-shaped and a G-shaped MCO. Synodontella akengboi differs from the two other species in having a J-shaped MCO and in the size of its ventral and dorsal anchors which, contrary to the other two species, are almost similar.


Introduction
Monogeneans that infect small catfishes of Mochokidae have been the focus of several studies [2,3,6,7,10,13] and, in Africa, only 10 species of Synodontella Dossou & Euzet, 1993 (hereafter Sy.) have thus far been reported from catfishes belonging to Synodontis Cuvier (hereafter S.) In 1968, Paperna and Thurston [10] described Sy. synodontii (Paperna & Thurston, 1968), the type species, from the gills of S. victoriae Boulenger in Uganda. In 1993, Dossou and Euzet [2] reported Sy. acropenis Dossou & Euzet, 1993 from the gills of S. sorex Günther, Sy. melanoptera Dossou & Euzet, 1993 from the gills of S. melanopterus Boulenger, and Sy. davidii Dossou & Euzet, 1993 from the gills of S. membranaceus (Geoffroy Saint-Hilaire) from Benin and Mali. In 1995, Douëllou and Chishawa [3] described Sy. zambezensis Douëllou & Chishawa, 1995 from S. zambezensis Peters from Lake Kariba in Zimbabwe. Raphahlelo et al. [13] confirmed the validity of these five species in their revision of the latter and Mbondo et al. [7] more recently redescribed Sy. melanoptera from the gills of S. obesus Boulenger and S. rebeli Holly in the Sanaga River (Cameroon). Mbondo  The study presented herein on the gill monogeneans of mochokid Synodontis catfishes is the first carried out in Côte d'Ivoire. The fish, all caught from the Bagoué River, were S. nigrita Valenciennes, S. velifer Norman, and S. ocellifer Boulenger. We found four species of monogeneans belonging to Synodontella. One of them, Sy. melanoptera, was already known from the gills of S. melanopterus, S. obesus, and S. rebeli [2,7], whereas the other three represent species new to science and are described here.

Materials and methods
Examined fish (Table 1) were caught with gillnets in the Bagoué River (north-western Côte d'Ivoire) from August 2018 to January 2019 at the following localities: Kanakono (10°1 8 0 N, 6°13 0 W); Samorossoba (6°21 0 W; 9°52 0 N); Samorosso (6°30 0 W; 9°34 0 N); N'Dara (6°24 0 W; 9°26 0 N) and Guinguereni (6°35 0 W; 9°32 0 N) (Fig. 1). Fish were identified on site upon capture using the key developed by Paugy et al. [12] and their gills resected into two sections, one ventral and one dorsal, and fixed and stored in liquid nitrogen. Upon return to the laboratory, gill arches were thawed and intensely rinsed to detach the monogeneans, which were individually collected and transferred directly onto a slide in a drop of glycerin ammoniumpicrate mixture (GAP) [5]. Each specimen was covered with a coverslip and, after complete diffusion of the mounting medium, sealed with Glyceel. A microscope (Motic BA310) with an integrated camera was used for observations. Identification of monogeneans was based on the morphology and size of the sclerotized pieces of the haptor and the copulatory complex.
Measurements were made as shown in Figure 2 following Dossou and Euzet [2]. All measurements (average followed in parentheses by minimum À maximum) are in micrometers (lm). Types were deposited in the Muséum National d'Histoire Naturelle, Paris, France (MNHN) and the Royal Museum for Central Africa, Tervuren, Belgium (RMCA).

Results
The four monogenean species found on the fish examined (Table 1) comply with the description of members of Synodontella given by Dossou and Euzet [2] in having the following characteristics: Ancyrocephalidae; presence of three pairs of cephalic glands; ocellae present or absent. Three of these species are new to science and are described below. Synodontella melanoptera Dossou & Euzet, 1993, was already known from S. melanopterus in Benin and S. rebeli and S. obesus in Cameroon; it is herein reported for the first time from Côte d'Ivoire from S. nigrita and S. velifer. Table 1. The four species of Synodontella (Sy.) encountered on the three species of Synodontis (S.) examined from the River Bagoué, Côte d'Ivoire. Infection parameters given as number of parasites per host species followed by prevalence and mean intensity in parentheses; host standard length given as mean followed by minÀmax, in cm.
Etymology: The species epithet "speroadotevii" honours Mr. Stanislas Spero-Adotevi, who has worked extensively for UNICEF in Africa.

Description
Based on 25 individuals (Fig. 3 The penis Pe = 88.1 (81-96), with ovoid bulb at its base, is in two parts of equal length. The first one is a simple, wide and slightly S-shaped tube with the opening at its extremity, the second one is a curved extension of the penis wall, highly sclerotized and not hollowed. Accessory piece, attached to basal ovoid bulb, is short, simple, wide and straight Ap = 34, 7 (30-41). No sclerotized vagina.

Remarks
Synodontella speroadotevii n. sp. differs from all its congeneric species mainly in the morphology of the penis, with its opening being in the middle of its course, which is unique amongst Synodontella spp. It also differs in its ventral transverse bar, which shows no median protuberance.

Remarks
Synodontella akengboi n. sp. is similar to Sy. zambezensis in the morphology of the dorsal transverse bar, which is slightly curved, and by having a ventral transverse bar with notches at both ends and a median protuberance. However, Sy. akengboi is mainly distinguishable from Sy. zambezensis by its ventral anchors and via the morphology of the male copulatory organ. The blade of the ventral anchors of Sy. akengboi is strongly arched vs angled at a right angle in Sy. zambezensis. The male copulatory organ of Sy. akengboi is a long tube (81.6 lm) and is thin and J-shaped with a simple shorter accessory piece, while the male copulatory organ of Sy. zambezensis consists of a fan-shaped tube at its distal end and possesses a thin accessory piece.

Discussion
In the present study, representatives of four species of monogeneans were collected from three host species. Three of these parasites are new to science. This finding brings to 13 the known total number of species of these monogeneans belonging to Synodontella described from the siluriform Mochokidae in Africa [2,3,6,7,10,13,14].
These new parasites were found on the gills of Synodontis nigrita, S. velifer, and S. ocellifer obtained from the Bagoué River. This type of parasitism, with three or more conspecific species of monogeneans parasites on a host species, is well known in Siluriformes. Indeed, N'Douba et al. [8,9] described in Côte d'Ivoire different species of monogeneans of the genera Quadriacanthus and Schilbetrema from Heterobranchus longifilis, H. isopterus, and Schilbe mandibularis. Similarly, Mbondo et al. [7] described Sy. melanoptera, Sy. apertipenis, and Sy. sanagaensis on the gills of S. rebeli from Cameroon.
In this study, we also observed Sy. melanoptera on S. nigrita and S. velifer, but not on S. ocellifer. This monogenean has already been reported in Benin from S. melanopterus and in Cameroon from both S. obesus and S. rebeli [2,7]. Accordingly, we can assume that Sy. melanoptera has a large geographical distribution in Africa given that it has been described from Benin, Cameroon, and Côte d'Ivoire. Likewise, this species, as is true with the other Synodontella spp., seems to have a wide host range including S. melanoptera, S. obesus, S. rebeli, S. nigrita, and S. velifer, and is thus stenoxenous [1]. Although S. nigrita, S. velifer, and S. ocellifer live in sympatry in the Bagoué river (at Samorossoba, Kanakono, Samorosso, N'Dara, and Guinguereni), we did not observe Sy. melanoptera from S. ocellifer even though, according to Paugy and Roberts [11], S. ocellifer is closely related to S. velifer and S. nigrita. The absence of Sy. melanoptera from S. ocellifer could be the result of a low sampling effort but can also be explained by an encounter problem in the compatibility filter [4].