Seven new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) parasitizing the gills of Congolese cichlids from northern Lake Tanganyika

Seven new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) isolated from the gills of six cichlid host species belonging to four tribes and sampled from the Congolese coastline of Lake Tanganyika (LT) are described: Cichlidogyrus adkoningsi sp. nov. from Cyphotilapia frontosa (tribe Cyphotilapiini); C. koblmuelleri sp. nov. from Cardiopharynx schoutedeni (Ectodini); C. habluetzeli sp. nov. from C. schoutedeni and C. frontosa; C. antoineparisellei sp. nov. from Interochromis loocki (Tropheini); C. masilyai sp. nov. from Petrochromis orthognathus (Tropheini); C. salzburgeri sp. nov. from P. trewavasae, and C. sergemorandi sp. nov. from Tylochromis polylepis (Tylochromini). This study represents the first parasitological examination of cyphotilapiine cichlid hosts. Representatives of the Tanganyikan ectodine, tropheine, and tylochromine cichlids previously sampled from various localities in the lake yielded nine, twelve, and two described species of Cichlidogyrus, respectively. The study further includes a morphological characterization of the male copulatory organ of six undescribed species of Cichlidogyrus found on the gills of the tropheines I. loocki and P. orthognathus, and on those of Callochromis melanostigma and Xenotilapia flavipinnis (both Ectodini). Geographical variation in the monogenean fauna of I. loocki was observed. The most closely related cichlid species investigated in this study harboured Cichlidogyrus spp. exhibiting some similarities in their sclerotized structures. Thus, our paper provides additional evidence of the high species richness of Cichlidogyrus and the link with their hosts’s phylogenetic affinities in LT.


INTRODUCTION
With an estimated 3,000 species distributed from Central and South America, across Africa to Madagascar, and to the Middle East and the Indian subcontinent (Chakrabarty, 2004), cichlid fishes represent one of the most species-rich families of vertebrates, accounting for about 10% of total teleost diversity (Takahashi & Koblmüller, 2011;Wanek & Sturmbauer, 2015). The Great African Rift Lakes Malawi, Victoria, and Tanganyika harbour cichlid flocks exhibiting high morphological, ecological, and genetic diversity (Takahashi & Sota, 2016). The exact number of species inhabiting these three lakes is still unknown, but approximately 2,000 species have been described (Koblmüller, Sefc & Sturmbauer, 2008). Lake Tanganyika (LT), located in the Great Rift Valley in central East Africa, is the deepest and oldest lake in Africa (Cohen et al., 1997) and the second deepest and oldest lake in the world (Salzburger et al., 2005). It holds the most diverse cichlid assemblages, comprised of several lineages of mostly endemic species classified into more than 50 genera and 12-14 tribes (Snoeks, 2000;Koblmüller, Sefc & Sturmbauer, 2008;Takahashi & Sota, 2016). Over 250 cichlid species are known to inhabit this lake (Takahashi & Koblmüller, 2011). Cichlids represent a textbook model in evolutionary biology (Kocher, 2004). Their mechanisms of speciation by rapid radiation make them crucial to the study of biological diversification, dynamics, and functions (Barluenga & Meyer, 2010;Takahashi & Koblmüller, 2011). Cichlid monogeneans are a promising tool for elucidating the speciation of both fish and parasites (Vanhove et al., , 2016. Among the 14 monogenean parasite genera known to infect cichlids, six (Urogyrus Bilong Bilong, Birgi & Euzet, 1994;Enterogyrus Paperna, 1963;Onchobdella Paperna, 1968;Scutogyrus Pariselle & Euzet, 1995;Cichlidogyrus (Dactylogyridae Bychowski, 1933), and Gyrodactylus von Nordmann, 1832 (Gyrodactylidae Van Beneden & Hesse, 1863)) were reported from African cichlids Pariselle et al., 2011;Mendoza-Palmero et al., 2017). More than 100 African and Levantine cichlid species have been investigated for the presence of monogenean parasites Vanhove et al., 2016). Cichlidogyrus Paperna, 1960 is the most species-rich genus and is mostly restricted to African and Levantine hosts (a few species were isolated from non-cichlid hosts, see for instance Birgi & Lambert (1986)) . To date, 111 valid species of Cichlidogyrus have been recognized in African cichlids (see the overview of Tanganyikan and non-Tanganyikan species of Cichlidogyrus published recently by ). Some Tanganyikan cichlid tribes remain to be investigated for their gill flatworms.
Lake Tanganyika harbours representatives of a few non-endemic tribes resulting from colonisation from the lacustrine environment. This is the case of Tylochromini Poll, 1986 with Tylochromis polylepis (Boulenger, 1900) as its sole representative in the lake. Members of Tylochromis Regan, 1920 inhabit rivers, lakes, and coastal lagoons throughout central and western Africa. Muterezi  studied the gill monogeneans of T. polylepis and described two species of Cichlidogyrus from Congolese host specimens, that is, C. mulimbwai and C. muzumanii Muterezi  In addition, they presented drawings of the hard parts (haptor and reproductive organs) of an undescribed species referred to as Cichlidogyrus sp. 'T. polylepis 3'.
The aim of this paper is to study gill monogenean diversity in cichlids belonging to four tribes from the Congolese lakeshore of northern LT. We describe seven new species of Cichlidogyrus and provide the morphological characterization of six undescribed congeners.

MATERIAL AND METHODS
Cichlid specimens were obtained in September 2013 and August 2016 from LT along the shoreline of the Democratic Republic of the Congo (DRC) (Fig. 1). In total, 26 fish specimens belonging to eight cichlid species of four tribes were purchased from fish markets or captured using gill nets during snorkelling or diving. Fish were placed in a cool box containing ice, transported to the laboratory, and dissected immediately.
Cichlid hosts were identified in situ on the basis of morphological characters by Walter Salzburger (Zoological Institute, University of Basel, Switzerland), Donatien Muzumani Risasi (Centre de Recherche en Hydrobiologie, Uvira, DRC), and Maarten Van Steenberge (the Royal Museum for Central Africa (MRAC), Tervuren and the Royal Belgian Institute of Natural Sciences, Brussels, Belgium). We performed molecular analysis on the samples, and obtained sequence data from the partial cytochrome b (cyt-b) mitochondrial gene to confirm the identity of the investigated cichlids. Fin clips from the cichlid specimens were preserved in 96% ethanol. Cichlid DNA was extracted using the DNeasy Tissue kit (Qiagen, Hilden, Germany) according to the manufacturer's protocol. The partial cyt-b gene was amplified following Mendlová et al. (2012). The PCR products were loaded onto a 1% agarose gel and subsequently purified, and sequencing was performed following . Nucleotide sequences were edited using Sequencher software v. 5.0 (Gene Codes, Ann Arbor, MI, USA). The identification of cichlid species based on the sequence similarity approach was carried out using the Basic Local Alignment Search Tool (https://blast.ncbi.nlm.nih.gov/Blast.cgi: blastn, default settings), available through the website of the National Centre for Biotechnology Information (NCBI Resource Coordinators, 2017). The newly generated sequences were deposited in GenBank under the accession numbers MH297985-MH298008. Gill arches were separated via dorsal and ventral section using standard parasitological procedures and transferred into a Petri dish containing water. Monogeneans were detached from the gills and isolated according to Musilová, Řehulková & Gelnar (2009) using an MST130 stereoscopic microscope and mounted on slides with glycerine ammonium picrate mixture (GAP) (Malmberg, 1957). Parasite identification was conducted using original descriptions, the systematic revision of dactylogyridean parasites of African cichlids by , and the recent overview focusing on the genitals of African Cichlidogyrus spp. by . Measurements and photographs were taken using an Olympus BX51 phase-contrast microscope and Olympus Stream Image Analysis v. 1.9.3 software. All measurements are included in the species descriptions. They are in micrometres, and are given as the mean followed by the range and the number of measurements (n) in parentheses (measurements of some undescribed species are given as the length of the structure in question followed by the number of measurements in parentheses). Drawings of the haptoral sclerotized parts and copulatory organs were made on flattened specimens using an Olympus BX51 microscope equipped with a drawing tube and edited with a graphic tablet compatible with Adobe Illustrator CS6 v. 16.0.0 and Adobe Photoshop v. 13.0. The terminology of haptoral sclerotized parts (anchors and hooks; also termed gripi and uncinuli, respectively) follows Gussev (1983). The numbering of hook pairs (Roman letters I-VII) is that recommended by Mizelle (1936). This method is preferred in adult specimens because it takes into consideration both antero-posterior and dorso-ventral positions of hooks (Kritsky, Thatcher & Boeger, 1986;Řehulková, Mendlová & Šimková, 2013). The lengths of hook pairs (short or long) was assigned following . The classification of haptoral groups follows Vignon, Pariselle & Vanhove (2011). The metrics used for the hard structures are shown in Fig. 2. The type material was deposited in the Invertebrate collection of the MRAC, Tervuren, Belgium; the Finnish Museum of Natural History (MZH), Helsinki, Finland; and the Muséum National d'Histoire Naturelle (MNHN), Paris, France. Host nomenclature follows FishBase (Froese & Pauly, 2017). The list of museum specimens used for comparison with the new species is presented in Table 1. Sampling was carried out under mission statements 022/ MINEURS/CRH-U/2013 and 031/MINRST/CRH-U/2016 from the Centre de Recherche en Hydrobiologie-Uvira. In the absence of relevant animal welfare regulations in the D.R. Congo, the same strict codes of practice enforced within the European Union were applied. This study was approved by the Animal Care and Use Committee of the Faculty of Science, Masaryk University, Brno (Czech Republic), approval nuber CZ01308.
The electronic version of this article in portable document format will constitute a published work according to the International Commission on Zoological Nomenclature (ICZN), and hence the new names contained in the electronic version are effectively published under that Code from the electronic edition alone. This published work and the nomenclatural acts it contains have been registered in ZooBank, the online registration system for the ICZN. The ZooBank LSIDs (Life Science Identifiers) can be resolved, and the associated information viewed through any standard web browser by appending the  LSID to the prefix http://zoobank.org/. The LSID for this publication is: urn:lsid:zoobank. org:pub:7076794A-B9EB-4FFC-AC49-66C304EC5BFB. The online version of this work is archived and available from the following digital repositories: PeerJ, PubMed Central, and CLOCKSS.

Molecular identification of cichlid hosts
The mitochondrial cytochrome b (cyt-b) gene fragment of 25 cichlid specimens was successfully amplified. The length of each consensus sequence was 419 bp. The Blast search processed on the NCBI website confirmed the species identification of the cichlid species investigated for the presence of gill parasitic flatworms.
Diagnosis. Cichlidogyrus koblmuelleri sp. nov. belongs to the same group as C. adkoningsi sp. nov. as it shares the small size of all hook pairs. The new species most closely resembles C. discophonum described from A. dewindti (see Rahmouni, Vanhove & Šimková, 2017) regarding the morphology of the dorsal and ventral anchors and the absence of a heel. However, it differs from the latter by (i) the longer copulatory duct (59-65 mm in C. koblmuelleri sp. nov. vs 41-47 mm in C. discophonum), and (ii) the longer and differently shaped accessory piece (curved with two superimposed parts, one of them thicker and longer than the other ending in a hook, 37-40 mm in C. koblmuelleri sp. nov. vs short with two thick distinct parts, twisted distally, ending in hook, 15-22 mm in C. discophonum). Like C. adkoningsi sp. nov. and the other Cichlidogyrus spp. of the ectodine cichlids listed in the previous diagnosis, C. koblmuelleri sp. nov. exhibits long dorsal bar auricles. However, they are longer in the new species than those of C. glacicremoratus (25-28 mm in C. koblmuelleri sp. nov. vs 14-18 mm in C. glacicremoratus). Moreover, C. koblmuelleri sp. nov. is mainly distinguishable from C. glacicremoratus by (i) the longer and differently shaped copulatory duct (C-shaped copulatory duct, 59-65 mm in C. koblmuelleri sp. nov. vs wavy copulatory duct, with thick Host accession numbers: MH297989-94.
Prevalence & intensity of infection: four fish specimens infected/six fish specimens examined, one to three parasite specimens per infected host.  Diagnosis. Cichlidogyrus habluetzeli sp. nov. belongs to the group of species with long hook pairs I-IV, VI and VII, large hook pair I, a copulatory duct without a swollen proximal portion, and a sclerotized vagina (see above). This group is restricted to a single species, the Tanganyikan C. centesimus (see Vanhove, Volckaert & Pariselle, 2011
Prevalence & intensity of infection in the type host: three fish specimens infected/six fish specimens examined, one to six parasite specimens per infected host.
Prevalence & intensity of infection: two fish specimens infected/two fish specimens examined, one to seven parasite specimens per infected host. Etymology: the species epithet 'antoineparisellei' honours the French parasitologist Dr. Antoine Pariselle, researcher at the Institut de Recherche pour le Développement, who extensively studied the monogeneans of African fish, trained countless people in fish parasitology, and described more than fifty species of Cichlidogyrus, of which three parasitize I. loocki.
Diagnosis. Cichlidogyrus masilyai sp. nov. belongs to the same group as C. adkoningsi sp. nov. and C. koblmuelleri sp. nov. (see above). The new species shows a similar morphotype to several representatives of Cichlidogyrus described from non-Tanganyikan haplochromine cichlids such as C. bifurcatus from Astatotilapia flaviijosephi (Lortet, 1883) (Paperna, 1960), C. haplochromii from H. guiarti (Pellegrin, 1904)  and C. zambezensis, in addition to C. gillardinae from the Tanganyikan haplochromine A. burtoni (Günther, 1894) (Muterezi . Further, the exceptional shape of the dorsal bar in the new species, that is, well-arched, C-shaped, is observed for the first time in Cichlidogyrus spp. infecting a tropheine cichlid. The new species exhibits the same hook pairs, similarly sized dorsal and ventral anchors, a non-sclerotized vagina, and an accessory piece ending in a pincer-like structure as in C. buescheri, a parasite of I. loocki. However, the shape of the dorsal and ventral anchors is different, that is, the shaft is more clearly marked in C. masilyai sp. nov. compared to that observed in C. buescheri. Further, it differs from C. buescheri by (i) the shorter and differently shaped dorsal bar (C-shaped, 22-24 mm in C. masilyai sp. nov. vs moderately arched, 31-45 mm in C. buescheri), (ii) the copulatory duct (thin, slightly curved proximally, straight halfway, folded distally, 31-34 mm in C. masilyai sp. nov. vs curved duct with narrow extremity, 49-58 mm in C. buescheri), (iv) the heel (poorly developed, lateral to the bulb, 1-2 mm in C. masilyai sp. nov. vs large heel of irregular shape at the basis of the bulb, 6-11 mm in C. buescheri), and (v) the accessory piece (seems to be unattached to basal bulb and thin, 24-29 mm in C. masilyai sp. nov. vs wide, directly attached to the basal bulb, 31-52 mm in C. buescheri). Host accession numbers: MH298003-06.
Prevalence & intensity of infection: two fish specimens infected/four fish specimens examined, one to two parasite specimens per infected host. Diagnosis. Cichlidogyrus salzburgeri sp. nov. belongs to the group of Cichlidogyrus which are characterized by a shorter hook pair I (pair V with larval size) and longer pairs II-IV, VI, and VII, a copulatory duct without a swollen distal portion, and a non-sclerotized vagina. Of all Cichlidogyrus spp., only C. halli Price & Kirk, 1967 and the Tanganyikan C. sturmbaueri (Vanhove, Volckaert & Pariselle, 2011) and C. rectangulus (Rahmouni, Vanhove & Šimková, 2017) are included in this group. Therefore, the new species is the third representative described from endemic Tanganyikan cichlids displaying this hook configuration. C. salzburgeri sp. nov. differs from its congeners C. buescheri, C. schreyenbrichardorum, and C. vealli isolated from I. loocki, and from the undescribed species previously identified on some representatives of Petrochromis, by the shape of the anchors, specifically the marked bases in the ventral ones . The dorsal bar in C. salzburgeri sp. nov. with its well-developed auricles is reminiscent of C. muterezii described from S. diagramma (see . However, C. salzburgeri sp. nov. differs from the latter by (i) the hook pairs (shorter hook pair I and longer pairs II-IV, VI, and VII in C. salzburgeri sp. nov. vs short hook pairs I-IV, VI, and VII in C. muterezii) and (ii) the pincer-like ending in the accessory piece, a feature missing in C. muterezii. Further, according to the comparative morphology of the reproductive organs, C. salzburgeri sp. nov. differs from C. franswittei found on the gills of P. marginatus and P. curvifrons (see  by (i) the hook pairs (shorter hook pair I and longer pairs II-IV, VI, and VII in C. salzburgeri sp. nov. vs short hook pairs I-IV, VI, and VII in C. franswittei), (ii) the shorter dorsal anchors (26-29 mm in C. salzburgeri sp. nov. vs 31-40 mm in C. franswittei), (iii) the shorter copulatory duct (39-42 mm in C. salzburgeri sp. nov. vs 47-57 mm in C. franswittei), and (iv) the shorter accessory piece (28-30 mm in C. salzburgeri sp. nov. vs 31-46 mm in C. franswittei). C. salzburgeri sp. nov. is distinguishable from the newly described species C. masilyai sp. nov. by (i) the longer dorsal bar (35-38 mm in C. salzburgeri sp. nov. vs 22-24 mm in C. masilyai sp. nov.), (ii) the length of its auricles (21-24 mm in C. salzburgeri sp. nov. vs 8-11 mm in C. masilyai sp. nov.), (iii) the differently shaped copulatory duct (straight, large copulatory duct and large distal opening in C. salzburgeri sp. nov. vs thin, slightly curved proximally, straight halfway, folded distally in C. masilyai sp. nov.), and (v) the differently shaped accessory piece (linked to basal bulb, thin proximally, straight, ending pincer-like with one extremity shorter than the other in C. salzburgeri sp. nov. vs thin and slightly curved in the middle part ending in pincer-like structure in C. masilyai sp. nov.).
Prevalence & intensity of infection: one fish specimen infected/two fish specimen examined, four parasite specimens on infected fish.
Etymology: the specific epithet 'salzburgeri' honours the biologist Dr. Walter Salzburger, professor at the University of Basel (Switzerland), for his work on cichlid evolution and in appreciation of his assistance during the fieldtrip.
Diagnosis. Regarding the morphology of the hook pairs and the vagina, C. sergemorandi sp. nov. belongs to the same morphological group as C. antoineparisellei sp. nov. (see above). The newly described species possesses a dorsal bar with short auricles, a spirally shaped copulatory duct, and an accessory piece separated from the basal bulb, features observed in many representatives described on tylochromine cichlids such as C. mulimbwai and C. muzumanii, parasites of the same cichlid host from LT (Muterezi , and the non-Tanganyikan C. berrebii, C. kothiasi, and C. pouyaudi from T. jentinki (Steindachner, 1894) (Pariselle & Euzet, 1994), and C. chrysopiformis Host accession number: MH298008.
Prevalence & intensity of infection: two fish specimens infected/three fish specimens examined, one to five parasite specimens per infected host.
Etymology: the specific epithet of the new species 'sergemorandi' honours the French evolutionary biologist and ecologist Dr. Serge Morand from CNRS and CIRAD (France), and CILM (Laos) for his work on ecology and the evolution of parasites.

Morphological characterisation of the MCO of the undescribed species
On the basis of the MCO features, we characterize six new undescribed species, namely C. sp. 'C. melanostigma', C. sp. 'X. flavipinnis 1', and C. sp. 'X. flavipinnis 2' (all from ectodine hosts), and C. sp. 'I. loocki 5', C. sp. 'P. orthognathus 2', and C. sp. 'P. orthognathus 3' (all from tropheine hosts) (Table 2; Fig. 10A-10F). These species could not be formally described because of the lack of material. Further, the haptoral parts of some specimens were not clearly visible for drawings. However, the general shape of the MCO provided sufficient morphological information to distinguish these species that can be considered as new to science. The morphological characterization of the MCO of the undescribed species of Cichlidogyrus recognized on Congolese host specimens did not allow us to confirm the presence/absence of a sclerotized vagina.  In the gills of the ectodine C. melanostigma we found a single monogenean species, namely C. sp. 'C. melanostigma'. Its MCO lacks a heel and possesses an ovoid basal bulb prolonged into a curved copulatory duct ending in a large opening: MCO = 46 (45-47; n = 2); Ct = 47-48 (n = 2). The accessory piece is curved, L-shaped, attached to the basal bulb and ending in a thick hook, Ap = 36-37 (n = 2). Further, a visible second wall lines the surface of the copulatory duct, which confers a twisted appearance. Cichlidogyrus sp. 'C. melanostigma' resembles C. banyankimbonai described from S. diagramma regarding the large distal opening of the copulatory duct (see . However, the MCO of C. sp. 'C. melanostigma' lacks a heel, unlike that of C. banyankimbonai. In addition, C. sp. 'C. melanostigma' exhibits a differently shaped accessory piece ending in a hook, a feature not observed in C. banyankimbonai. According to the comparative morphology of the MCO, C. sp. 'C. melanostigma' is reminiscent of C. discophonum from A. dewindti, both parasites of ectodine cichlids (see Rahmouni, Vanhove & Šimková, 2017). The two species lack a heel and possess a curved copulatory duct, and an accessory piece ending in a hook. However, C. sp. 'C. melanostigma' exhibits a longer accessory piece (36-37 mm in C. sp. 'C. melanostigma' vs 15-22 mm in C. discophonum). Further, the copulatory duct in C. sp. 'C. melanostigma' appears double walled and ends in a large opening, while there is a thick proximal part which tapers distally in C. discophonum. Also, the accessory piece in C. sp. 'C. melanostigma' is L-shaped, while C. discophonum possesses an accessory piece composed of two parts twisted distally. Regarding these differences, we consider C. sp. 'C. melanostigma' to be a different species from C. discophonum and new to science.
Cichlidogyrus sp. 'X. flavipinnis 1' Fig. 10B The MCO of C. sp. 'X. flavipinnis 1' exhibits a small heel and a thick, well curved copulatory duct, MCO = 37 (n = 1); He = 2 (n = 1); Ct = 36 (n = 1). The subterminal opening of the copulatory duct seems to be located at the last third. Such a feature has never been reported in Cichlidogyrus species described so far. Thus, we cannot confirm whether C. sp. 'X. flavipinnis 1' really exhibits this characteristic in its copulatory duct, or it is only an artefact due to isolation or fixation procedures. The accessory piece attached to the basal bulb is thick, curved both proximally and distally with a finger-like ending, Ap = 29 (n = 1). Cichlidogyrus sp. 'X. flavipinnis 1' is most similar to C. sp. 'C. melanostigma'. Both species occur on closely related ectodine host species, that is, X. flavipinnis and C. melanostigma. However, C. sp. 'X. flavipinnis 1' presents a heel, a feature missing in C. sp. 'C. melanostigma', in addition to the differently shaped proximal endings of the accessory piece (finger-like in C. sp. 'X. flavipinnis 1' vs thick hook in C. sp. 'C. melanostigma'). Therefore, we consider C. sp. 'X. flavipinnis 1' and C. sp. 'C. melanostigma' as two different species.
Cichlidogyrus sp. 'X. flavipinnis 2' Fig. 10C The second undescribed species isolated from X. flavipinnis has a shorter MCO compared to that of C. sp. 'X. flavipinnis 2', and a slightly curved copulatory duct with a narrow extremity, MCO = 22 (n = 1); Ct = 24 (n = 1). Heel reduced to inconspicuous, He = 1 (n = 1). The accessory piece is proximally thick and irregularly shaped, attached to the basal bulb by a small additional part, distally with pincer-like ending, Ap = 16 (n = 1). The heel structure in C. sp. 'C. melanostigma', C. sp. 'X. flavipinnis 1', and C. sp. 'X. flavipinnis 2' is absent to inconspicuous. Further, C. sp. 'X. flavipinnis 2' is easily distinguishable from C. sp. 'C. melanostigma' and C. sp. 'X. flavipinnis 1' (i) by its shorter MCO and a dissimilar copulatory duct with a narrow extremity, and (ii) by the differently sized accessory piece and its characteristic pincer-like shape at its extremity, the distal parts of which are finger and hook-like in C. sp. 'X. flavipinnis 1' and C. sp. 'C. melanostigma', respectively. On the basis of these differences, we consider C. sp. 'X. flavipinnis 2' to be different from C. sp. 'C. melanostigma' and C. sp. 'X. flavipinnis 1' and to represent a new species to science.
Cichlidogyrus 'I. loocki 5' Fig. 10D Specimens of I. loocki harboured a second parasite species and, according to the morphology of the MCO, we consider it as new to science. Cichlidogyrus sp. 'I. loocki 5' exhibits a long MCO with a heel attached to the side of an irregularly shaped basal bulb, MCO = 79 (n = 1); He = 6 (n = 1). The copulatory duct of constant width is long, wavy, and well curved proximally, Ct = 104 (n = 1). The accessory piece is separated proximally into two thin parts, curved halfway with a twisted gutter-like appearance, distally with an additional small outgrowth and an irregular blunt ending, Ap = 64 (n = 1). However, we cannot reliably confirm the blunt shape in the distal part of the accessory piece since we cannot reject the possibility that this feature is an artefact of parasite fixation.
According to the morphology of the MCO, C. sp. 'I. loocki 5' is most similar to C. georgesmertensi from P. babaulti in having a long and wavy copulatory duct, in addition to a curved accessory piece attached to the basal bulb (see . However, C. sp. 'I. loocki 5' exhibits a heel attached to the side of the basal bulb like in C. masilyai sp. nov., while in C. georgesmertensi, it is located at the bottom of the basal bulb as in most species of Cichlidogyrus. Further, no gutter-like appearance or additional outgrowth in the distal part of the accessory piece were reported for C. georgesmertensi. Cichlidogyrus sp. 'I. loocki 5' can be compared to C. vealli (see Pariselle et al., 2015b). Indeed, the new undescribed species shares the host I. loocki with C. vealli, but the two parasites were sampled in different localities (northern lakeshore vs southern tip of the lake in the case of C. vealli). Moreover, in C. sp. 'I. loocki 5', the extremity of the MCO is narrower than that of C. vealli. Also, the undescribed species shows an additional small outgrowth at the proximal third of its MCO, a feature missing in its congener. Further, the accessory piece in C. sp. 'I. loocki 5' presents a gutter-like structure only in the middle part and a blunt extremity. In C. vealli, this feature exists throughout the accessory piece. On the basis of these differences, we consider C. sp. 'I. loocki 5' to be a different species from C. vealli.
Cichlidogyrus sp. 'P. orthognathus 3' Fig. 10F Cichlidogyrus sp. 'P. orthognathus 3' exhibits a short MCO with a reduced heel, MCO = 33 (31-34; n = 2); He = 2-3 (n = 2). The copulatory duct is thick, starting in an ovoid basal bulb, curved halfway with a big distal opening, Ct = 30 (28-31; n = 2). The accessory piece is linked to the basal bulb, thick and spirally coiled ending in a hook, Ap = 21 (20-22; n = 2). The general shape of the MCO of C. sp. 'P. orthognathus 3' is reminiscent of C. raeymaekersi, a species described from the tropeine S. diagramma (see . C. raeymaekersi shows a short and wide copulatory duct with a poorly developed heel, and a thick spirally coiled accessory piece attached to the basal bulb as observed in C. sp. 'P. orthognathus 3'. However, the latter possesses a copulatory duct with an ovoid basal bulb with a distal wide part, different from the elongated bulb and the bevelled ending in C. raeymaekersi, which makes C. sp. 'P. orthognathus 3' distinct from C. raeymaekersi.

DISCUSSION
The cichlid fishes of LT have undergone spectacular diversification, filling a diversity of ecological niches within a short time period, and therefore represent one of the most interesting models of adaptive radiation (Tsuboi et al., 2016). Research on cichlids is nowadays combined with the investigation of their parasite diversity in order to study the speciation of both cichlids and their specific parasites (Vanhove et al., , 2016. Currently, only 32 Cichlidogyrus spp. are known from cichlids inhabiting LT (see the overview by ). The present study, based on morphological characters, increases knowledge of the diversity of host specific monogenean species in the cichlids living the northern sub-basin of the lake. We provide descriptions of seven gill monogenean species parasitizing six Congolese representatives of four cichlid tribes in LT. They are C. adkoningsi sp. nov. on C. frontosa (Cyphotilapiini); C. koblmuelleri sp. nov. on C. schoutedeni (Ectodini); C. habluetzeli sp. nov. on C. frontosa and C. schoutedeni; C. antoineparisellei sp. nov. on I. loocki; C. masilyai sp. nov. on P. orthognathus; C. salzburgeri sp. nov. on P. trewavasae (both Tropheini); and finally C. sergemorandi sp. nov. on T. polylepis (Tylochromini). We characterized also six undescribed parasite species on the basis of the morphology of their MCO. They are C. sp. 'C. melanostigma' from C. melanostigma; C. sp. 'X. flavipinnis 1' and C. sp. 'X. flavipinnis 2' from X. flavipinnis (both Ectodini); C. sp. 'I. loocki 5' from I. loocki; and finally C. sp. 'P. orthognathus 2' and C. sp. 'P. orthognathus 3' from P. orthognathus (all Tropheini).
First, we identified the cichlid species using morphology and DNA sequence data from the mitochondrial cyt-b region. Nowadays, DNA barcoding targeting mitochondrial regions such as the COI (cytochrome oxidase I) or cyt-b genes for cichlid fish identification is well established and documented (Kullander et al., 2014;Breman et al., 2016). Molecular analyses confirmed the morphological identification of the cichlids analysed for the presence of monogenean parasites in this study.
Then, we morphologically characterized the newly described species of Cichlidogyrus on the basis of the sclerotized parts of their attachment (haptor) and reproductive organs (MCO and sclerotized vagina when visible). The sclerotized structures of dactylogyridean monogeneans have been extensively investigated in various ecological and evolutionary contexts. Several studies have reported the influence of such sclerotized structures on host specificity, parasite specialization, and reproductive isolation among congeners through niche ecology (Šimková & Morand, 2008;Vignon, Pariselle & Vanhove, 2011;Messu Mandeng et al., 2015). Because of the limitations of light microscopy as regards some morphological characters, sclerotized structures are increasingly studied using enzymatic digestion followed by scanning electron microscopy. In the case of Cichlidogyrus, we can cite recent studies of Fannes, Vanhove & Huyse (2017) and Igeh, Dos Santos & Avenant-Oldewage (2017). Using this method, they redescribed three Cichlidogyrus spp. (C. tiberianus, C. dossoui, and C. philander), and provided morphological details on the haptoral and reproductive hard parts, which are not visible with light microscopy.
Regarding our study, most sclerites of C. adkoningsi sp. nov. found on C. frontosa are reminiscent of species previously described from ectodine cichlids (see diagnosis). Despite these similarities, C. adkoningsi sp. nov., which represents the first record of a gill ectoparasite on a Tanganyikan cyphotilapiine, is easily distinguishable from its Tanganyikan congeners by the shape and dimensions of its sclerotized structures (such as the dorsal bar and its very characteristic long auricles, and the MCO with its irregularly shaped heel and S-shaped accessory piece ending in a hook). Similarly, C. habluetzeli sp. nov., a common species found on the same host and on the gills of C. schoutedeni, exhibits the same morphotype as species infecting ectodines, as well as other Cichlidogyrus species described from various Tanganyikan tribes. Morphologically, most of the sclerotized structures of C. habluetzeli sp. nov. are bigger than in similar species. Yet, the dorsal bar (with its small hollow outgrowths on the anterior face and its straight auricles), in addition to the straight copulatory duct, heel, and accessory piece, are structures reminiscent of those of C. aspiralis, C. pseudoaspiralis, C. centesimus (Vanhove, Volckaert & Pariselle, 2011;Rahmouni, Vanhove & Šimková, 2017), C. casuarinus , and finally C. nshomboi . However, some features are present in some species and missing in others. This is the case with the spirally-ornamented wall of the MCO observed exclusively in C. casuarinus, C. centesimus, and C. nshomboi, or the sclerotized vagina present in all the species listed above (including C. habluetzeli sp. nov.) except for C. pseudoaspiralis (Vanhove, Volckaert & Pariselle, 2011;Muterezi Bukinga et al., 2012;Pariselle et al., 2015a;Kmentová et al., 2016b;. Regarding the haptoral configuration, C. habluetzeli sp. nov. with its hook pairs (long pairs I-IV, VI, and VII with large pair I) joins the group that harbours, so far, a single member, C. centesimus.
In recent studies on the monogenean diversity of Tanganyikan cichlids, similarities in the haptoral and reproductive organs of Cichlidogyrus spp. parasitizing phylogenetically closely related cichlid hosts are far from unusual. In the present study, for instance, C. habluetzeli sp. nov. and C. koblmuelleri sp. nov. infecting C. schoutedeni are morphologically similar to some congeners of ectodine cichlids. This is also true for the undescribed species C. sp. 'C. melanostigma' and C. discophonum from A. dewindti sampled in north-eastern LT. In fact,  reported that two cichlid hosts Eretmodus marksmithi Burgess, 2012 and Tanganicodus irsacae Poll, 1950, both belonging to the Eretmodini, host two morphologically similar monogenean species C. jeanloujustinei and C. evikae, respectively. Moreover, monogenean communities composed of morphologically similar Cichlidogyrus species were reported in Burundese O. nasuta and its congeners from more southern localities. This observation was explained by the large distribution of ectodine hosts in the lake (Vanhove, Volckaert & Pariselle, 2011; CONCLUSION Lake Tanganyika has an impressive degree of cichlid parasite diversity with numerous species as yet undescribed. Cichlidogyrus includes (to date) 39 species from LT, including the new species described in the present study, and 79 species from other locations. Species of Cichlidogyrus infecting closely related cichlid fishes are often morphologically similar, but taxonomically distinct. Further morphological and molecular studies are necessary to elucidate the origin of the various lineages of Cichlidogyrus in LT and their evolutionary history.

MZH
Finish Museum of Natural History, Helsinki, Finland.

MRAC
Royal Museum for Central Africa, Tervuren, Belgium.