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All issues Volume 31 (2024) Parasite, 31 (2024) 46 Full HTML
Open Access
Issue
Parasite
Volume 31, 2024
Article Number 46
Number of page(s) 19
DOI https://doi.org/10.1051/parasite/2024039
Published online 07 August 2024

© T.P. Gobbin et al., published by EDP Sciences, 2024

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction

Cichlid fish (Cichlidae) form one of the most species-rich families of vertebrates, occurring mainly in rivers and lakes in Africa and South America. They underwent spectacular adaptive radiations in many African lakes, including lakes Tanganyika, Malawi, and Victoria [10, 23, 53]. The species flocks that evolved in the African Great Lakes display a large diversity in morphology, ecology and behaviour, and high levels of endemism [10, 23, 50, 56, 62, 63]. There are also many cases in which cichlids failed to radiate upon colonising lakes [53, 62, 63]. Together, these characteristics have made African cichlids a rewarding model system for studying adaptation and speciation [23, 24]. In recent years, evidence has accumulated that the diversity of cichlids in the African Great Lakes is also associated with diversity of their parasites [15, 22, 44, 59]. Monogenean flatworms are a promising parasite group to study whether and how the diversification processes in cichlids and their parasites influence each other [41, 58]. This is because of their species richness in African cichlids, their narrow host-specificity compared to other cichlid parasites, and their direct lifecycle.

Most studies of monogenean parasites of African Great Lake cichlids have focused on Lake Tanganyika, the oldest of the three Great Lakes, that also has by far the oldest cichlid radiations (e.g. [42, 59]). From this lake, 39 species of Cichlidogyrus Paperna, 1960 [35, 46] and three species of Gyrodactylus von Nordmann, 1832 [60] have been described from cichlids. Of these, only one species from each genus has been found also on non-Tanganyikan hosts: Cichlidogyrus mbirizei Muterezi Bukinga, Vanhove, Van Steenberge & Pariselle, 2012 and Gyrodactylus sturmbaueri Vanhove, Snoeks, Volckaert & Huyse, 2011. These two species were reported for the first time outside of Lake Tanganyika by Lerssutthichawal et al. [25] in a cultured Oreochromis hybrid in Thailand, and by Zahradníčková et al. [66] in Pseudocrenilabrus philander (Weber, 1897) in Zimbabwe and South Africa, respectively. Conversely, only two monogenean species previously known from other cichlids outside Lake Tanganyika have been observed in a cichlid endemic to the Tanganyika basin: Cichlidogyrus halli (Price & Kirk, 1967) and Scutogyrus longicornis (Paperna & Thurston, 1969), both on Oreochromis tanganicae (Günther, 1984). This indicates that the monogenean assemblage of Tanganyika cichlids is quite distinct from that of other cichlids. Here, we focus on Lake Victoria, where the monogenean fauna has been investigated less extensively. Research on its monogeneans already peaked in the 1960s–70s [37, 42], yielding ten species of Cichlidogyrus, two species of Gyrodactylus, and a single species of Scutogyrus Pariselle and Euzet, 1985, all of which are also found on cichlids outside the Lake Victoria region, with the exception of Cichlidogyrus longipenis Paperna & Thurston, 1969. Only recently, Lake Victoria’s monogeneans received attention again, namely in ecological parasitology [15–17, 22, 26, 27]. Two of these studies distinguished Cichlidogyrus at the species level [15–17] and suggest that the species richness, level of endemism, and host-specificity of cichlid-infecting monogeneans may be lower in Lake Victoria than in Lake Tanganyika, a feature that Pariselle et al. [42] suggested to be linked to the younger age of the Lake Victoria cichlid species flock.

Lake Victoria is the youngest, and also the shallowest and most turbid of the three Great Lakes. It was completely dry until about 14,600 years ago [20]. Most of its current cichlid fauna evolved in situ after that dry period [19, 30, 55]. The Lake Victoria cichlid superflock evolved from a hybrid swarm derived from at least two riverine lineages that colonised the lake [30, 54]. This provided the genetic variation that, together with ample ecological opportunities, allowed rapid speciation [28, 49, 52]. Current cichlid species display a wide range of trophic specialisations [2, 3, 18, 29, 48, 51, 65]. Older cichlid lineages (only distantly related to the species that radiated in the lake) also colonised the lake, but did not speciate: Astatoreochromis alluaudi Pellegrin, 1904, Pseudocrenilabrus multicolor (Schöller, 1903), Oreochromis variabilis (Boulenger, 1906), and Oreochromis esculentus (Graham, 1928). These are currently sympatric with species of the Lake Victoria superflock.

Pending a global revision of the species-rich genus Cichlidogyrus using genetic data (more than 130 valid species described today: [12, 40, 45, 46]), the species belonging to this genus are grouped together by morphological similarities to facilitate their systematic analysis [43, 61]. Closely related species within the genus can be grouped by the morphology of their reproductive apparatus, whereas genera and subgeneric categories are more easily grouped by the morphology of their haptoral hard parts, one of the first criteria being the relative length of the hooks (i.e., total length of hooks I, III–VII relative to total length of hooks II [39, 40]). In the present study, for the first time in over 40 years, we systematically survey the monogenean fauna infecting the three anciently divergent haplochromine cichlid lineages of Lake Victoria: the radiation lineage (represented here by 18 species) and the two lineages that did not radiate (Astatoreochromis alluaudi and Pseudocrenilabrus multicolor). This results in four formal taxonomic descriptions and two redescriptions.

Materials and methods

Five locations in southern Lake Victoria, Tanzania, were sampled (Table 1, Fig. 1, Table S1): Makobe rocky island (−2.3654, 32.9228) in May–August 2010 and in June–October 2014; Kissenda (−2.5494, 32.8276), Python (−2.6237, 32.8567), Luanso (−2.6889, 32.8842) rocky islands, and the swampy inlet stream Sweya (−2.5841, 32.8970) in June–October 2014. Fish were caught by angling and with gillnets of variable mesh sizes and morphologically identified by Ole Seehausen [51]. At Makobe, we collected 13 cichlid species belonging to the Lake Victoria radiation lineage and one species (Astatoreochromis alluaudi) representing an older lineage that did not speciate. At Sweya, we collected A. alluaudi as well as Pseudocrenilabrus multicolor victoriae, representing the other lineage that did not diversify, and Astatotilapia nubila, from the Lake Victoria radiation lineage. At Kissenda and Python, we collected three and one additional species of the Lake Victoria radiation lineage, respectively. Two of those (Pundamilia sp. ‘pundamilia-like’ and Pundamilia sp. ‘nyererei-like’) are closely related to P. pundamilia Seehausen & Bouton, 1998 and P. nyererei (Witte-Maas & Witte, 1985) that occur at Makobe. At Luanso, we collected one species (Pundamilia sp. ‘Luanso’). These species pairs of Pundamilia represent replicate speciation events [31]. The sampled cichlid species vary in their micro-habitat and trophic specialisations [2, 3, 18, 51, 65] and also in the extent of genetic differentiation [31, 32]. Within the radiation, divergence is 14,600 years old, while the divergence between both non-radiating lineages, and between them and the ancestors of the radiations in Lake Victoria, Lake Malawi and other lakes, is 8–10 million years old [31, 32, 48]. Fish were immediately sacrificed with an overdose of 2-phenoxyethanol, numbered and preserved in ethanol (some directly preserved in 100% ethanol, others fixed in 4% formaldehyde and then transferred to 70% ethanol). Sampling was conducted with permission from the Tanzania Commission for Science and Technology (COSTECH - No. 2013-253-NA-2014-117). In the laboratory, the right gill arches were removed and screened for macroparasites by inspecting gill filaments with a mounted needle, under a dissecting stereoscope (Zeiss Stemi 2000, Zeiss, Oberkochen, Baden-Württemberg, Germany). Monogeneans were detached with tweezers and individually stored in 100% ethanol. Specimens were individually mounted onto a slide, treated with 20% sodium dodecyl sulphate (SDS) to soften tissues and then fixed in Hoyer’s medium. Specimens of Cichlidogyrus were examined with a microscope (phase-contrast Olympus BX41TF, Olympus, Hamburg, Germany and Leica DM2500, Leica, Wetzlar, Hessen, Germany) and sclerotised parts (nomenclature and numbering according to ICOPA IV; [8]) were measured with Olympus Stream Essentials v. 1.9 and with LAS 6.0 software (Fig. 2, all measurements given in μm). Drawings of sclerotised parts were made with CorelDraw 2019 software (Corel Corporation, Ottawa, Ontario, Canada) on the basis of microphotographs taken with a Leica DM2500 microscope and LAS 6.0 software. Type material of Cichlidogyrus longipenis Paperna & Thurston, 1969 [38] (RMCA_VERMES_35921) and C. bifurcatus Paperna, 1960 [35] (RMCA_VERMES_35703) was measured and compared to our specimens. Type and voucher specimens of the parasites were deposited in the Muséum National d’Histoire Naturelle, Paris, France (MNHN), the Royal Museum for Central Africa, Tervuren, Belgium (RMCA) and the Iziko South African Museum, Cape Town, Republic of South Africa (SAMC); symbio(para)types and host vouchers (terminology: see [4]) are stored at the Swiss Federal Institute of Aquatic Science and Technology, Kastanienbaum, Switzerland (EAWAG). Photo vouchers are deposited on MorphoBank (https://morphobank.org/permalink/?P4937). For more details on the host-parasite combinations and geographical range of the species of Cichlidogyrus used for differential diagnosis, see Řehulková et al. [47] and Cruz-Laufer et al. [6]. Epidemiological indices (P = prevalence, IF = intensity range, MI = mean intensity) were calculated according to Bush et al. [5].

thumbnail Figure 1

Geographical location of the five sampling sites in southern Lake Victoria, Tanzania: rocky islands Makobe (M), Kissenda (K), Python (P), Luanso (L), and the Sweya swampy inlet stream (S).

thumbnail Figure 2

Schematic overview of a specimen of Cichlidogyrus with its typical morphological sclerotised structures (MCO, male copulatory organ in the upper part of the parasite image, attachment organ in the bottom part) and measurements used in the descriptions of the new species. Abbreviations: A, anchor (a, total length; b, blade length; c, shaft length; d, guard length; e, point length); DB, dorsal bar (h, auricle length; w, maximum straight width; x, total length; y, distance between auricles); VB, ventral bar (x, length of one ventral bar branch; w, maximum width); H, hook length; Pe, penis curved length; He, heel straight length; Ap, accessory piece straight length.

Table 1

Haplochromine host species (n fish: number of host individuals) sampled in May-August 2010 and June-October 2014 at five localities (Makobe, Sweya, Kissenda, Luanso, Python) in southern Lake Victoria and the sample size of identified specimens of Cichlidogyrus (n Cichlidogyrus). The radiation lineage is labelled with a circle (●), the two lineages that did not speciate are labelled with a square (■) and a diamond (◆).

Results

During this survey, eight species of Monopisthocotyla were found on the gills of studied hosts. With the exception of a single specimen of Gyrodactylus sturmbaueri infecting Ptyochromis xenognathus (Greenwood, 1957) from Kissenda (reported in [15] and deposited under accession number RMCA_VERMES_43410), all monogeneans corresponded to the diagnosis of Cichlidogyrus given in Pariselle and Euzet [40]. Two of the identified species of Cichlidogyrus were already known (C. longipenis Paperna & Thurston, 1969 [38], C. bifurcatus Paperna, 1960 [35]), the four others are herein formally described, and we characterise a potential fifth new species, for which we refrain from formal description for want of sufficient specimens.

Cichlidogyrus longipenis Paperna & Thurston, 1969

Previous records: Cichlidogyrus sp. IV sensu Gobbin et al. [15, 16], see also [14]

Type host: Astatoreochromis alluaudi Pellegrin, 1904.

Type locality: Jinja, Uganda [38].

Infection site: Gills.

Other records: None.

Current records: Type host from Lake Victoria, Makobe Island and Sweya swampy inlet; Pundamilia sp. ‘pink anal’ from Lake Victoria, Makobe Island.

Infection parameters: Makobe: Astatoreochromis alluaudi P = 100% (9/9), IF = 2–17, MI = 10.7; Pundamilia sp. ‘pink anal’ P = 14.3% (2/14), IF = 1; Sweya: A. alluaudi P = 57.1% (4/7), IF = 1–14, MI = 4.5.

Material studied: 10 whole-mounted specimens in Hoyer’s solution and the syntype RMCA_VERMES_35921.

Material deposited: MNHN_HEL1476, MNHN_HEL1482, RMCA_VERMES_43419, SAMC-A092084.

Voucher hosts: Astatoreochromis alluaudi Pellegrin, 1904 from Makobe (EAWAG ID 103148 and 103567, Table S1).

Redescription (Table 2, Fig. 3): Two pairs of anchors of similar size and unequal shape (guard more developed in dorsal anchors). Ventral bar V-shaped. Dorsal bar with two auricles inserted at its dorsal surface. Hooks 7 pairs; I and III to VII short, except V of medium size (i.e., their total length relative to the total length of hook pairs II, see [39, 40]). Penis long, wavy, thinner at proximal and distal extremities, rounded basal bulb, no heel; simple accessory piece, attached to the basal bulb of the penis by a filament, ending in a curved hook. No sclerotised vagina.

thumbnail Figure 3

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus longipenis. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar; VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ (on the left as observed in most of our specimens, on the right the phenotype similar to the one reported by Paperna & Thurston, 1969): Ap, accessory piece; Pe, penis. Scale bar: 20 μm.

Table 2

Measurements of Cichlidogyrus bifurcatus and C. longipenis redescribed from haplochromine host species of Lake Victoria (N = number of specimens, n = number of observations per trait per species) compared to those provided by Paperna [35] and Paperna & Thurston [38] (expressed as ranges only, because means were not reported in the original descriptions). For C. longipenis, we also report measurements extrapolated from the drawing of the original description and our measurements from the syntype. All measurements in μm, given as the mean and range (in parentheses).

Remarks: The specimens described herein share the combination of the following characters only with C. longipenis [38]: hook pairs I and II to VII short (or of medium size), penis long (>60 μm) with simple accessory piece and no heel, no sclerotised vagina. The measurements of some of these characters differ between the original description and our data (Table 2). Some traits were measured as larger when compared to values reported in the original description: the length of the accessory piece (43.9–60.6 vs. 29–40 μm, respectively), penis (95.1–102.4 vs. 63–79 μm), ventral (35.3–48.2 vs. 20–38 μm) and dorsal anchors (39.2–53.5 vs. 23–33 μm), auricles (15.4–26.5 vs. 6–10 μm), dorsal bar (38.4–55.6 vs. 23–33 μm), ventral bar (40.3–62.1 vs. 53–73 μm). Even so, we are confident of our identification of these specimens as C. longipenis: as mentioned above, species identification in Cichlidogyrus is mainly based on the morphology of the reproductive apparatus [43, 61], which is similar in size and shape in our specimens compared to the type (Figs. 3 and 4). The observed size differences may be due to two non-exclusive factors. First, the mounting medium used: Fankoua et al. [9] demonstrated that the use of Hoyer’s medium increases the size and modifies the shape of sclerotized parts. Second, the way Paperna and Thurston [38] made the drawings and took the measurements for the original description: although measurements given in the original description are compatible with its drawings and scale bars (Table 2), there are significant differences between these measurements and those we took from the syntype (Table 2) (an exception is the ventral bar total length, which seems incomparable: we measured the length of a branch, while the original authors probably measured the total length of the bar). This is probably because Paperna and Thurston [38] did not use a camera lucida and made their drawings freehand, which may have led to magnification errors.

thumbnail Figure 4

Micrographs of the male copulatory organ of Cichlidogyrus longipenis, from a parasite individual of the present study (left) and from the holotype by Paperna & Thurston, 1969 (right), fixed in two different mediums. Scale bar: 20 μm.

Cichlidogyrus bifurcatus Paperna, 1960 [35]

Previous records: Cichlidogyrus sp. VI sensu Gobbin et al. [15, 16], see also [14].

Type host: Astatotilapia flaviijosephi (Lortet, 1883).

Type locality: Sea of Galilee (spelled Sea of Gallilee in the original description) [35].

Infection site: Gills.

Other previous records: Young Oreochromis aureus (L.) from the Sea of Galilee (initially identified as O. niloticus) [34]. Harpagochromis squamipinnis Regan, 1921 and “Haplochromis” sp. ‘aeneocolor’ Greenwood, 1973 from Lake George, and Kazinga channel; “H.” elegans Trewavas, 1933 and Haplochromis limax Trewavas, 1933 from Lake George; “Haplochromis” sp. from Lake Edward and Entebbe, Lake Victoria; Pseudocrenilabrus multicolor (Schöller, 1903) from Lake Mulehe and a stream near Masindi, Lake Albert system, Uganda [37].

Current records: Pseudocrenilabrus multicolor victoriae Seegers, 1990 and “Astatotilapia” nubila (Boulenger, 1906) from Lake Victoria, Sweya swampy inlet stream.

Infection parameters: Pseudocrenilabrus multicolor victoriae P = 11.5% (3/26), IF = 2; “Astatotilapia” nubila P = 6.7% (1/15), IF = 1.

Material studied: 7 whole-mounted specimens in Hoyer’s solution and the paratype RMCA_VERMES_35.703.

Material deposited: MNHN_HEL1470.

Voucher host: Pseudocrenilabrus multicolor victoriae Seegers, 1990 from Sweya (EAWAG ID 109436, Table S1).

Redescription (Table 2, Fig. 5): Two pairs of anchors of similar size, with guard approximately 2 times as long as shaft. Dorsal anchors with guard and shaft more asymmetrical and blade shorter than ventral anchors. Ventral bar V-shaped, with 2 branches with wing-shaped attachments along distal half. Dorsal bar thin, tapering towards its extremities, and 2 small auricles inserted at its dorsal surface. Hooks 7 pairs; I short (i.e., its total length less than 1.7 times the total length of hook pair II); III to VII short (i.e., their total length less than 2 times the total length of hook pair II), V and VI longer (see [39, 40]). Male copulatory organ (MCO) consisting of slightly curved penis with large basal bulb and constant diameter; accessory piece simple, terminally frayed; developed heel with crenelated distal edge. Vagina not sclerotised.

thumbnail Figure 5

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus bifurcatus. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar, VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ: AP, accessory piece; Pe, penis; He, heel. Scale bar: 20 μm.

Remarks: The specimens found in Lake Victoria on P. multicolor victoriae and “A.” nubila, identified as C. bifurcatus, display many similarities and some dissimilarities with C. bifurcatus described by Paperna in 1960 on A. flaviijosephi in the Sea of Galilee. They are similar in the shape and size of the MCO, the hooks, anchors and bars. Only some range extensions and minor differences in the size of some sclerotised parts are apparent, e.g., the length of the ventral bar (see Table 2), that may be due to two reasons, see remarks above under C. longipenis.

Cichlidogyrus pseudodossoui n. sp.

urn:lsid:zoobank.org:act:2AA5987B-7AE1-407E-8E58-CB6CEFC89360

Previous records: Cichlidogyrus sp. III sensu Gobbin et al. [15, 16], C. sp. “pseudodossoui” sensu Gobbin et al. [17], see also [14].

Type host: Astatoreochromis alluaudi Pellegrin, 1904.

Type locality: Off Makobe Island, Lake Victoria.

Holotype: MNHN_HEL1478.

Paratypes: MNHN_HEL1473, RMCA_VERMES_43421, SAMC-A092086.

Infection site: Gills.

Other hosts: Neochromis omnicaeruleus Seehausen & Bouton, 1998; Neochromis sp. ‘unicuspid scraper’; Ptyochromis xenognathus (Greenwood, 1957); Pundamilia nyererei (Witte-Maas & Witte, 1985); Pundamilia sp. ‘nyererei-like’; Pundamilia pundamilia Seehausen & Bouton, 1998; Pundamilia sp. ‘pundamilia-like’.

Other localities: Kissenda Island, Python Island, Sweya swampy inlet.

Infection parameters: Makobe: Astatoreochromis alluaudi P = 55.5% (5/9), IF = 1–2, MI = 1.2; Neochromis omnicaeruleus P = 6.2% (1/16), IF = 1; Neochromis sp. ‘unicuspid scraper’ P = 3.1% (1/32), IF = 1; Pundamilia pundamilia P = 1.6% (1/61), IF = 1; P. nyererei P = 4.6% (3/65), IF = 1–2, MI = 1.6; Kissenda: Ptyochromis xenognathus P = 9.1% (1/11), IF = 1; Pundamilia sp. ‘pundamilia-like’ P = 5.6% (1/18), IF = 1; Pundamilia sp. ‘nyererei-like’ P = 6.2% (1/16), IF = 2; Python: Pundamilia sp. ‘pundamilia-like’ P = 20% (1/5), IF = 2; Sweya: A. alluaudi P = 14.3% (1/7), IF = 1.

Material studied: 7 whole-mounted specimens in Hoyer’s solution.

Symbiotype: Astatoreochromis alluaudi Pellegrin, 1904 from Makobe (EAWAG ID 103148, Table S1).

Symbioparatypes: Astatoreochromis alluaudi Pellegrin, 1904 from Makobe (EAWAG ID 103571, Table S1); Neochromis omnicaeruleus Seehausen & Bouton, 1998 from Makobe (EAWAG ID 105655, Table S1); Ptyochromis xenognathus (Greenwood, 1957) from Kissenda (EAWAG ID 12306, Table S1).

Etymology: The species epithet refers to the similarity of this newly described species with its congener C. dossoui Douëllou, 1993.

Description (Table 3, Fig. 6): Two pairs of anchors of unequal size (ventral larger) and similar shape: short blade, and shaft and guard symmetrical in appearance and of similar size. Ventral bar V-shaped (rounded on its anterior edge). Dorsal bar with two developed auricles inserted at its dorsal surface. Hooks 7 pairs; I short; III to VII very long (see [39, 40]). MCO consisting of a J-shaped and thin penis starting at right angle from an ovoid bulb; accessory piece thick, Z-shaped, with a recurved tooth at its distal extremity; developed rounded heel. Vagina thick walled, bent at right angle, with annulated proximal third, broadened towards distal extremity.

thumbnail Figure 6

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus pseudodossoui n. sp. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar; VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ: AP, accessory piece; Pe, penis; He, heel; Vg, vagina. Scale bar: 20 μm.

Table 3

Measurements of the new species of Cichlidogyrus described from haplochromine host species of Lake Victoria (N = number of specimens, n = number of observations per trait per species). All measurements in μm, given as the mean and range (in parentheses).

Remarks: This new species belongs to the group showing the following characters: hooks I short, long hooks III–VII, penis J-shaped, accessory piece Z-shaped without auxiliary plate, and sclerotised vagina. This group also comprises the following 15 species: C. anthemocolpos Dossou, 1982 (on a few coptodonine species in West Africa), C. bonhommei Pariselle & Euzet, 1998 (on heterotilapiine species in West Africa), C. bouvii Pariselle & Euzet, 1997 (on an oreochromine species in West Africa), C. dossoui Douëllou, 1993 (on several coptodonine species, a haplochromine, a pelmatolapiine, a tilapiine species in Central and West Africa, and introduced with oreochromines elsewhere), C. douellouae Pariselle, Bilong Bilong & Euzet, 2003 (on an oreochromine in West Africa), C. ergensi Dossou, 1982 (on several coptodonine species, a pelmatolapiine species in West Africa and the Middle East), C. flexicolpos Pariselle & Euzet, 1995 (on several coptodonine species and a pelmatolapiine species in West Africa), C. gillesi Pariselle, Bitja Nyom & Bilong Bilong, 2013 (on a coptodonine species in Central Africa), C. hemi Pariselle & Euzet, 1998 (on a tilapiine species in West Africa), C. kouassii N’Douba, Thys van den Audenaerde & Pariselle, 1997 (on a coptodonine species in Southern-West Africa), C. legendrei Pariselle & Euzet, 2003 (on a pelmatolapiine species in Central Africa), C. lemoallei Pariselle & Euzet, 2003 (on a few pelmatolapiine species in Central Africa), C. ouedraogoi Pariselle & Euzet, 1996 (on a few coptodonine and a pelmatolapiine species in Central and West Africa), C. tiberianus Paperna, 1960 (on several coptodonine and oreochromine species, a few haplochromine and tilapiine species, a pelmatolapiine species in Central and West Africa and in the Middle East), and C. vexus Pariselle & Euzet, 1995 (on a few coptodonine species in West Africa). Cichlidogyrus pseudodossoui n. sp. mainly differs by the shape and length of its vagina (short, conical, and bent at right angle) from C. flexicolpos, C. lemoallei (vagina very long, thin and folded back in the middle); from C. ergensi, C. gillesi, C. kouassii, and C. ouedraogoi (vagina S-shaped); from C. anthemocolpos (U-shaped with a distal plate), C. bonhommei (thin walled, bent in two different perpendicular plans), C. hemi (straight, with constant diameter and annulated all along), C. legendrei (well developed), C. tiberianus (looped, 1 turn). Cichlidogyrus pseudodossoui n. sp. resembles C. dossoui in the shape of the accessory piece with a recurved distal end, the J-shaped thin penis starting in an ovoid bulb, and the rounded heel of the MCO. It is close to C. bouvii, C. dossoui, C. douellouae, and C. vexus, which all have a conically shaped vagina bending at a right angle. It differs from these species by the greater length of its dorsal bar auricles (which have a size range of 22.5–38.6 μm in C. pseudodossoui n. sp. vs. 10–15, 12–20, 11–17, 13–20 μm, respectively for the four other species) and above all of its hook pairs III–VII. These have a size range of 45.5–78.5 μm in C. pseudodossoui n. sp. vs. 31–43, 27–37, 31–43 μm, respectively for C. bouvii, C. douellouae, and C. vexus. These hook lengths also allow us to distinguish between C. dossoui and C. pseudodossoui n. sp. as follows: III: 36–45 vs. 45.5–69.8, IV: 38–50 vs. 43.7–74.5, V: 40–50 vs. 50.6–78.5, VI: 40–49 vs. 49.9–77.6, VII: 36–48 vs. 48.8–76.1.

Cichlidogyrus nyanza n. sp.

urn:lsid:zoobank.org:act:3CCDC28A-959D-4336-B752-951B0F0DFCC7

Previous records: Cichlidogyrus sp. I sensu Gobbin et al. [15, 16], C. sp. “nyanza” sensu Gobbin et al. [17], see also [14].

Type host: “Haplochromis” cyaneus Seehausen, Bouton & Zwennes, 1998.

Type locality: Off Makobe Island, Lake Victoria.

Holotype: MNHN_HEL1477.

Paratypes: MNHN_HEL1472, RMCA_VERMES_43420, SAMC-A092085.

Infection site: Gills.

Other hosts: “Haplochromis” cyaneus Seehausen, Bouton & Zwennes, 1998; Labrochromis sp. ‘stone’; Mbipia lutea Seehausen & Bouton, 1998; M. mbipi Seehausen, Lippitsch & Bouton, 1998; Neochromis gigas Seehausen & Lippitsch 1998; N. omnicaeruleus Seehausen & Bouton, 1998; N. rufocaudalis Seehausen & Bouton, 1998; Neochromis sp. ‘unicuspid scraper’; Paralabidochromis chilotes Greenwood, 1959; Ptyochromis xenognathus Greenwood, 1957; Ptyochromis sp. ‘striped rock sheller’; Pundamilia Seehausen & Bouton, 1998; Pundamilia sp. ‘pundamilia-like’; P. nyererei (Witte-Maas & Witte, 1985); Pundamilia sp. ‘nyererei-like’; Pundamilia sp. ‘Luanso’; Pundamilia sp. ‘pink anal’; Pseudocrenilabrus multicolor victoriae Seegers, 1990.

Other localities: Kissenda Island, Python Island, Luanso Island, Sweya swampy inlet.

Infection parameters: Makobe: “Haplochromis” cyaneus P = 83.3% (5/6), IF = 1–5, MI = 3.0; Labrochromis sp. ‘stone’ P = 9.1% (1/11), IF = 1–2, MI = 1.5; Mbipia lutea P = 60% (3/5), IF = 3–5, MI = 4.0; M. mbipi P = 66.6% (8/12), IF= 1–3, MI = 1.6; Neochromis gigas P = 600% (3/5), IF = 4–6, MI = 5.0; N. omnicaeruleus P = 75.0% (12/16), IF = 1–17, MI = 4.1, N. rufocaudalis P = 57.1% (4/7), IF = 1–4, MI = 2.7; Neochromis sp. ‘unicuspid scraper’ P = 59.4% (19/32), IF = 1–6, MI = 2.0; Paralabidochromis chilotes P = 30.7% (4/13), IF = 1; Ptyochromis sp. ‘striped rock sheller’ P = 25% (1/4), IF = 3; Pundamilia nyererei P = 7.7% (5/65), IF = 1–3, MI = 1.8; Pundamilia sp. ‘pink anal’ P = 35.7% (5/14), IF = 1–5, MI = 1.8; P. pundamilia P = 24.2% (15/62), IF = 1–6, MI = 2.4; Kissenda: Ptyochromis xenognathus P = 36.4% (4/11), IF = 1–5, MI = 3.5; Pundamilia sp. ‘nyererei-like’ P = 50.0% (8/16), IF = 1–2, MI = 1.4; Pundamilia sp. ‘pundamilia-like’ P = 50.0% (9/18), IF = 1–3, MI = 1.6; Python: Pundamilia sp. ‘pundamilia-like’ P = 20% (1/5), IF = 3; Luanso: Pundamilia sp. ‘Luanso’ P = 27.7% (5/18), IF = 1–3, MI = 1.6; Sweya: Pseudocrenilabrus multicolor victoriae P = 3.8% (1/26), IF = 1.

Material studied: 11 whole-mounted specimens in Hoyer’s solution.

Symbiotype: “Haplochromis” cyaneus Seehausen, Bouton & Zwennes, 1998 from Makobe (EAWAG ID 105317, Table S1).

Symbioparatypes: “Haplochromis” cyaneus Seehausen, Bouton & Zwennes, 1998 from Makobe (EAWAG ID 105323 and 105128, Table S1).

Etymology: The species epithet, a noun in apposition, refers to the word for lake in several regional languages of East Africa.

Description (Table 3, Fig. 7): Two pairs of anchors of similar size and shape, with short shaft, dorsal anchor sometimes with fenestrations at the junction of shaft and guard. Ventral bar U-shaped with thick branches. Dorsal bar with two auricles inserted at its dorsal surface. Hooks 7 pairs; I and III to VII short (see [39, 40]). MCO consisting of a large penis with constant diameter but thicker wall at its basis, bent at distal third, accessory piece simple, S-shaped, attached to the basal bulb of the penis by a thin filament; no heel. No sclerotised vagina.

thumbnail Figure 7

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus nyanza n. sp. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar; VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ: AP, accessory piece; Pe, penis. Scale bar: 20 μm.

Remarks: Short hook pairs I and III–VII, a simple MCO (see description above), and the absence of a sclerotised vagina are features that Cichlidogyrus nyanza n. sp. shares with several congeners infecting haplochromine cichlids in Central and Southern-East Africa, such as C. banyankimbonai Pariselle & Vanhove, 2015; C. frankwillemsi Pariselle & Vanhove, 2015; C. franswittei Pariselle & Vanhove, 2015; C. georgesmertensi Pariselle & Vanhove, 2015; C. gillardinae Muterezi Bukinga, Vanhove, Van Steenberge & Pariselle, 2012; C. gistelincki Gillardin, Vanhove, Pariselle, Huyse & Volckaert, 2012; C. irenae Gillardin, Vanhove, Pariselle, Huyse & Volckaert, 2012; C. muterezii Pariselle & Vanhove 2015; C. raeymaekersi Pariselle & Vanhove, 2015, and C. steenbergei Gillardin, Vanhove, Pariselle, Huyse & Volckaert, 2012. The new species described herein differs from all of these in showing both an accessory piece reaching beyond the distal end of the penis and no heel. Cichlidogyrus haplochromii and C. tilapiae, previously reported from Lake Victoria (on several haplochromine and a few oreochromine species) also display short hooks and a simple MCO, but have no heel, such as in C. nyanza n. sp., which differs from them in the shape of the accessory piece (of which the terminal end is blunter in C. nyanza n. sp. than the hook-like extension of C. haplochromii Paperna & Thurston, 1969 or the pointed extremity in C. tilapiae Paperna, 1960) and the shape of the ventral anchors (less incised in C. nyanza n. sp.).

Cichlidogyrus furu n. sp.

urn:lsid:zoobank.org:act:C1E2FD2F-0BB1-4154-8C96-552C261283CC

Previous records: Cichlidogyrus sp. II sensu Gobbin et al. [15, 16], C. sp. “furu” sensu Gobbin et al. [17], see also [14].

Type host: Pundamilia nyererei (Witte-Maas & Witte, 1985).

Type locality: Off Makobe Island, Lake Victoria.

Holotype: MNHN_HEL1475.

Paratypes: MNHN_HEL1471, RMCA_VERMES_43418.

Infection site: Gills.

Other hosts: Astatoreochromis alluaudi Pellegrin, 1904; “Astatotilapia” nubila (Boulenger, 1906); “Haplochromis” cyaneus Seehausen, Bouton & Zwennes, 1998; Mbipia lutea Seehausen & Bouton, 1998; M. mbipi Seehausen, Lippitsch & Bouton, 1998; Neochromis omnicaeruleus Seehausen & Bouton, 1998; N. rufocaudalis Seehausen & Bouton 1998; Neochromis sp. ‘unicuspid scraper’; Paralabidochromis chilotes Greenwood, 1959; Pseudocrenilabrus multicolor victoriae Seegers, 1990; Ptyochromis xenognathus Greenwood, 1957; Pundamilia sp. ‘Luanso’; Pundamilia nyererei (Witte-Maas & Witte, 1985); Pundamilia sp. ‘pink anal’; P. pundamilia Seehausen & Bouton, 1998; Pundamilia sp. ‘nyererei-like’ and Pundamilia sp. ‘pundamilia-like’ from Kissenda.

Other localities: Kissenda Island, Luanso Island, Sweya swampy inlet.

Infection parameters: Makobe: Astatoreochromis alluaudi P = 22.2% (2/9), IF = 1–2, MI = 1.5; “Haplochromis” cyaneus P = 16.7% (1/6), IF = 1; Mbipia lutea P = 20.0% (1/5), IF = 1; M. mbipi P = 75.0% (9/12), IF = 1–3, MI = 1.4; Neochromis omnicaeruleus P = 31.2% (5/16), IF = 1–3, MI = 1.6; N. rufocaudalis P =28.6% (2/7), IF = 1; Neochromis sp. ‘unicuspid scraper’ P = 18.2% (6/33), IF = 1; Paralabidochromis chilotes P = 7.7% (1/13), IF = 1; Pundamilia pundamilia P = 11.3% (7/62), IF = 1–3, MI = 1.6; P. nyererei P = 23.1% (15/65), IF = 1–5, MI = 1.6; Pundamilia sp. ‘pink anal’ P = 21.4% (3/14), IF = 1–5; MI = 2.6; Kissenda: Ptyochromis xenognathus P = 18.2% (2/11), IF = 1–2, MI = 1.5; Pundamilia sp. ‘nyererei-like’ P = 43.7% (7/16), IF = 1–3, MI = 1.6; Pundamilia sp. ‘pundamilia-like’ P = 33.3% (6/18), IF = 1–3, MI = 1.5; Luanso: Pundamilia sp. ‘Luanso’ P = 44.4% (8/18), IF = 1–5, MI = 2.1; Sweya: “Astatotilapia” nubila P = 6.7% (1/15), IF = 3; Pseudocrenilabrus multicolor victoriae P = 7.7% (2/26), IF = 1.

Material studied: 10 whole-mounted specimens in Hoyer’s solution.

Symbiotype: Pundamilia nyererei (Witte-Maas & Witte, 1985) from Makobe (EAWAG ID 103397, Table S1).

Symbioparatypes: Pundamilia nyererei (Witte-Maas & Witte, 1985) from Makobe Island (EAWAG ID 103312 and 103397, Table S1).

Etymology: The species epithet is the word referring to haplochromine cichlids in Kiswahili, used as a noun in apposition.

Description (Table 3, Fig. 8): Two pairs of anchors of similar size and unequal shape (guard, and length difference between shaft and guard, more pronounced in dorsal anchors). Ventral bar V-shaped with thin branches. Dorsal bar thin with two auricles inserted at its dorsal surface. Hooks 7 pairs; I and III to VII short, except for pair V which is of medium size (see [39, 40]). Penis an S-shaped tube, sclerotised from its basal bulb until halfway its total length, opens at its distal third and ends in a groove; accessory piece simple, attached to the rounded basal bulb of the penis by a thin filament; developed heel. No sclerotised vagina.

thumbnail Figure 8

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus furu n. sp. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar; VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ: AP, accessory piece; Pe, penis; He, heel. Scale bar: 20 μm.

Remarks: Cichlidogyrus furu n. sp. shares the short hook pairs III–VII and the non-sclerotised vagina with C. nyanza n. sp. and several other congeners infecting haplochromine cichlids (see above). It is unique among species of Cichlidogyrus in having a penis ending in a groove. This feature had already been described in other dactylogyridean monogenean species (e.g. Synodontella speroadotevii Bouah, N’Douba & Pariselle 2019; [1]). Two specimens (deposited as vouchers under MNHN_HEL1480 and MNHN_HEL1481), taken from one Pundamilia sp. ‘pink anal’ from Makobe (stored as 104372 at EAWAG) and one Pundamilia sp. ‘nyererei-like’ from Kissenda (stored as 104754 at EAWAG) differ from C. furu n. sp. in having the penis entirely sclerotised (Figs. 9 and 10) but were otherwise very similar to C. furu n. sp. Since measurements of this morphotype fall into the range of C. furu n. sp. and we cannot exclude that the peculiar trait resulted from mounting, we report it as Cichlidogyrus cf. furu n. sp. and not as a new species.

thumbnail Figure 9

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus cf. furu n. sp. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar; VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ: AP, accessory piece; Pe, penis; He, heel. Scale bar: 20 μm.

thumbnail Figure 10

Micrographs of the male copulatory organ of Cichlidogyrus furu n. sp. (left) and of C. cf. furu n. sp. (right), fixed in Hoyer’s medium. Scale bar: 20 μm.

Cichlidogyrus vetusmolendarius n. sp.

urn:lsid:zoobank.org:act:A526328E-270B-4B95-921C-FB1A3C528586

Previous records: Cichlidogyrus sp. V sensu Gobbin et al. [15, 16], C. sp. “vetusmolendarius” sensu Gobbin et al. [17], see also [14].

Type host: Pseudocrenilabrus multicolor victoriae Seegers, 1990.

Type locality: Off Makobe Island, Lake Victoria.

Holotype: MNHN_HEL1483.

Paratypes: MNHN_HEL1479, MNHN_HEL1474, RMCA_VERMES_43422.

Infection site: Gills.

Other hosts: Mbipia lutea Seehausen & Bouton 1998; Pundamilia pundamilia Seehausen & Bouton, 1998; Pundamilia nyererei (Witte-Maas & Witte, 1985); Pundamilia sp. ‘nyererei-like’; Pundamilia sp. ‘pink anal’; Pundamilia sp. ‘pundamilia-like’.

Other localities: Kissenda Island, Sweya swampy inlet.

Infection parameters: Makobe: Pundamilia nyererei P = 1.5% (1/65), IF = 1; P. pundamilia P = 1.6% (1/62), IF = 1; Pundamilia sp. ‘pink anal’ P = 7.1% (1/14), IF = 1; Kissenda: Pundamilia sp. ‘nyererei-like’ P = 6.2% (1/16), IF = 2; Pundamilia sp. ‘pundamilia-like’ P = 5.5% (1/18), IF = 1; Sweya: “Astatotilapia” nubila P = 6.7% (1/15), IF = 2 Pseudocrenilabrus multicolor victoriae P = 11.5% (3/26), IF = 1.

Material studied: 10 whole-mounted specimens in Hoyer’s solution.

Symbiotype: Pseudocrenilabrus multicolor victoriae Seegers, 1990 (EAWAG ID 106984, Table S1).

Symbioparatypes: “Astatotilapia” nubila (Boulenger, 1906) from Sweya (EAWAG ID 109405, Table S1); Mbipia lutea Seehausen & Bouton 1998 from Makobe (EAWAG ID 13313, Table S1); Pseudocrenilabrus multicolor victoriae Seegers, 1990 (EAWAG ID 105869, Table S1).

Etymology: The species epithet refers to the type host, a representative of a relatively old haplochromine lineage compared to most other hosts studied (“vetus”, Latin adjective meaning “old”), and to the shape of the first pair of hooks, similar to the wings of a windmill (“molendarius”, Latin adjective derived from “molendinum”).

Description (Table 3, Fig. 11): Two pairs of anchors of unequal shape and size (guard longer in dorsal anchors). Ventral bar long and thin, V-shaped. Dorsal bar thin with two auricles inserted at its dorsal surface. Hooks 7 pairs; I thick and long with a large shaft; III and VII short (22.8 and 23.3 μm), IV to VI longer (27.3, 31.0 and 28.0 μm) (see [39, 40]). Penis short, thin, with a straight direction and spirally coiled on itself (1.5 turns). Accessory piece simple, winding around the penis, and attached to the basal bulb of the penis by a thin and spirally coiled filament (1.5 turns). Poorly developed heel. No sclerotised vagina.

thumbnail Figure 11

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus vetusmolendarius n. sp. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar; VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ: AP, accessory piece; Pe, penis; He, heel. Scale bar: 20 μm.

Remarks: This new species belongs to the group showing the following characters: hooks pair I very large, no visible vagina. The only previously described species from Lake Victoria haplochromines that falls into this morphological group is C. dionchus Paperna & Thurston, 1969, which differs from C. vetusmolendarius n. sp. in the shape of its accessory piece (which is curved instead of coiled in C. vetusmolendarius n. sp., and broadens terminally and subsequently ends in a hook-like extremity), its clearly elongated heel (poorly developed in C. vetusmolendarius n. sp.) and its dorsal anchors with proportionally longer point and blade. This group also comprises: C. arfii Pariselle & Euzet, 1995 (on a pelmatolapiine in West Africa), C. berradae Pariselle & Euzet, 2003 (on a few coptodonine and a pelmatolapiine species of Central Africa), C. bulbophallus Geraerts & Muterezi Bukinga, 2020 (on a haplochromine species in Central Africa), C. centesimus Vanhove, Volckaert & Pariselle, 2011 (on a few ectodines in East Africa), C. digitatus Dossou, 1982 (on several coptodonine, a pelmatolapiine and a tilapiine species in Central and West Africa), C. halinus Paperna, 1969 (on an oreochromine species in West Africa), C. maeander Geraerts & Muterezi Bukinga, 2020 (on a haplochromine and a tilapiine species in Central Africa), C. nuniezi Pariselle & Euzet, 1998 (on a tilapiine species in West Africa), C. papernastrema Price, Peebles & Bamford, 1969 (on a coptodonine, a tilapiine and an oreochromine species in Central and Southern Africa), C. philander Douëllou, 1993 (on a haplochromine in Southern Africa), C. quaestio Douëllou, 1993 (on a few haplochromine, a tilapiine and a coptodonine species in Southern Africa), and C. yanni Pariselle & Euzet, 1995 (on several coptodonine species and a pelmatolapiine species in West Africa). Among these species, only C. maeander has a spirally coiled accessory piece winding around the penis like C. vetusmolendarius n. sp. Both species share features of the haptoral sclerotised parts, namely: guards at least twice as long as shafts in both anchors, with the guard more pronounced in the dorsal anchors; dorsal anchors on average longer than ventral ones; auricles implanted at the dorsal surface of the dorsal bar; long first hook pair. Also their accessory pieces resemble each other. Cichlidogyrus vetusmolendarius n. sp. differs from C. maeander in ventral anchor length (29–41 vs 43–44 μm, respectively), and in the shape of the MCO. In C. vetusmolendarius n. sp., the MCO consists in a penis that is short, thin, straight and spirally coiled on itself (1.5 turns), and that displays a poorly developed heel; whereas in C. maeander it is described as “penis [stylet] short, forming enlarged bulb at base; base attached to pronounced heel; penis [stylet] distally curved, with pointed end” [12].

Discussion

All the cichlid species sampled are host to Cichlidogyrus spp. (Monopisthocotyla), Lamproglena monodi Capart, 1944 (Copepoda), Ergasilus lamellifer Fryer, 1961 (Copepoda), and glochidia larvae of freshwater mussels (Bivalvia) attached to their gills [15, 22]. Of the hosts, A. alluaudi has previously been investigated in taxonomic work for its monogenean gill parasites, next to nine members of the haplochromine radiation and four non-haplochromine cichlid species present in Lake Victoria (overview in [42]). Hence, our survey more than doubles the number of cichlid species from Lake Victoria that have been scrutinised for their gill parasitofauna and their monogenean parasites identified to species level or formally described. This expansion of host coverage, although not including a formal description at the time, already allowed Gobbin, Vanhove et al. [15] to propose several patterns with regard to the diversity of Cichlidogyrus in Lake Victoria haplochromines. First, the non-radiating haplochromines harbour a monogenean fauna that is distinct from their radiating counterparts. This is not surprising, given that the non-radiating A. alluaudi was the sole host known for the only species of Cichlidogyrus that is currently hypothesised to be endemic to Lake Victoria, C. longipenis. Second, the dactylogyrid monogeneans infecting members of the haplochromine radiation were rarely found on cichlids not belonging to the radiation, in line with the trends observed in the overview of Pariselle, Muterezi Bukinga et al. [42].

Recent research on the evolutionary ecology of cichlid-parasite interactions in Lake Victoria proposed that the communities of dactylogyrid flatworms infecting the lake’s haplochromine radiation differ from those parasitising species of two ancient non-radiating haplochromine lineages in the same locations [15]. Cichlid species that are members of the young radiation seemed to share the same set of dactylogyrid flatworm species among each other, but also occasionally with the ancient haplochromine lineages (represented by A. alluaudi and P. multicolor victoriae). Here, we aimed to underpin these observations with formal taxonomic assessment of the gill monogeneans in question. Of the ten species previously reported in Lake Victoria, we found only two in the present study (C. bifurcatus and C. longipenis). This can be explained by the difference in locations and/or host lineages surveyed. We surveyed members of Haplochromini from the southern part of Lake Victoria (Tanzania), while previous studies surveyed the northern part (Uganda) and mostly focused on other tribes (such as Oreochromini and Tilapiini) [36–38]. We hypothesise that host lineage, rather than geographic locality, is the more important factor in determining infection variation because the two abovementioned species of Cichlidogyrus have been documented in the same host species in the present study and in the previous ones. This study increases the number of nominal monogenean species that are exclusively known from Lake Victoria from one (C. longipenis) to five. The fact that only four (or five, when including C. cf. furu n. sp.) new species are found when characterising the monogenean fauna of 20 host species, from five different locations, is in line with the trends suggested by Pariselle, Muterezi Bukinga et al. [42]: the discovery rate and proportion of endemism in Cichlidogyrus are lower in the young Lake Victoria compared to the ancient Lake Tanganyika. Indeed, when comparing Lake Victoria’s littoral haplochromines with Tropheini, a lineage of littoral Tanganyika haplochromines, the species richness and uniqueness of their monogenean parasites are starkly lower in the former (see e.g., [59], indicating typically at least one, and up to seven, unique parasite species per host species, with only closely related congeneric hosts, rarely, sharing parasite species). This contrasts with the species richness of the cichlid hosts which is twice higher in Lake Victoria than in Lake Tanganyika [11, 56]. Unlike the haplochromine cichlids in Lake Tanganyika, Lake Victoria haplochromines were now found to also harbour species displaying some long hook pairs (I–VII in C. pseudodossoui n. sp., I in C. vetusmolendarius n. sp.) and a more complex accessory piece of the MCO (C. pseudodossoui n. sp. and C. vetusmolendarius n. sp.). Furthermore, it is the first time that a penis ending in an open groove was observed in Cichlidogyrus, in C. furu n. sp., adding to the known diversity in the morphology of monogeneans infecting African Great Lake haplochromines. Also noteworthy about Cichlidogyrus furu n. sp. is that, while the relative lengths of hook pairs III to VII were previously often considered together [39, 61], in this species, pair V is clearly longer than the others. Size differences within hook pairs III to VII have also been reported from recently discovered congeners in the Congo river basin [12, 21]. In agreement with Rahmouni, Vanhove et al. [45] and Geraerts, Muterezi Bukinga et al. [12], this further illustrates that the different haptor configurations proposed for the classification of species of Cichlidogyrus into four morphotype groups, mostly based on West African representatives (see [43, 61]) cannot accommodate all the recently described species from Central, East and Southern Africa. Phylogenetic analyses with increased species coverage indicated that the length of the haptoral hooks is systematically informative [7]. The genetic data required for this could also help in clarifying whether some morphological features could be key to understand the shared history of these species. This may be the case for the tube-shaped penis and simple accessory piece of C. bifurcatus, C. longipenis, and C. nyanza n. sp., that are shared with many congeners infecting haplochromines (see [13, 34, 57]), and for the long hooks V shared by C. furu n. sp., C. calycinus Kusters, Jorissen, Pariselle & Vanhove, 2018, and C. omari Jorissen, Pariselle & Vanhove, 2018 [21]. Pending confirmation of this phylogenetic signal, we note the morphological similarity of these species with typical parasites of haplochromines (reported from representatives of e.g. Haplochromis Hilgendorf, 1888, Orthochromis Greenwood, 1954, Pharyngochromis Greenwood, 1979, Pseudocrenilabrus Fowler, 1934, Sargochromis Regan, 1920, Serranochromis Regan, 1920 and Tropheini), namely a simple male copulatory organ and similar size and shape of ventral and dorsal anchors. On the other hand, C. pseudodossoui n. sp. resembles species described from mainly West African cichlid hosts belonging to Heterotilapiini, Pelmatolapiini, Gobiocichlini, Coptodonini, and Oreochromini, and hence probably belongs to an entirely different lineage of Cichlidogyrus. This suggests that members of Cichlidogyrus colonised Lake Victoria haplochromines or their ancestors at least twice. Lake Victoria was colonised by at least four lineages belonging to two tribes (Haplochromini and Oreochromini) [30]. The taxonomic coverage of the current phylogenetic reconstruction for Cichlidogyrus across Africa does not suffice to test whether this provides a likely pathway for the origins of the Lake Victoria cichlid monogeneans. However, in the context of the phylogeny of Cichlidogyrus, we can already observe that the haptors of the Lake Victoria parasites have auricles attached to the dorsal side of the dorsal bar. This is considered a derived state, in contrast to the auricles being a continuation of the anterior side of the dorsal bar, as in the earlier diverged parasites of the only very distantly related tylochromine cichlids [33]. While the dominance of C. bifurcatus on P. multicolor victoriae, and of C. longipenis on A. alluaudi, in contrast to the communities of Cichlidogyrus of the other investigated hosts, clearly demonstrate community-level differences between member species of the haplochromine radiation and other Lake Victoria haplochromines, none of these monogeneans seems specialised to a single host species. We concur with Pariselle, Muterezi Bukinga et al. [42] that this low host-specificity may be a consequence of the young age of the lake and its fish assemblage. It would therefore be interesting to expand sampling to adjacent lakes and river systems, to test the hypothesis that their haplochromine cichlids harbour the same or closely related species of Cichlidogyrus [30, 64].

Acknowledgments

This research was funded by the University of Bern, the Swiss National Science Foundation, and the University of Groningen (Ubbo Emmius Programme). Infrastructure was provided by the Natural History Museum in Lugano and by the European Marine Biological Research Centre (EMBRC) Belgium (FWO-Vlaanderen project GOH3817N). MPMV received support from the Special Research Fund of Hasselt University (BOF20TT06). We thank Chahrazed Rahmouni and Michiel Jorissen for insights on morphological identification.

Conflicts of interest

The authors declare that they have no conflicts of interest.

Supplementary material

Table S1: Host species, identification number (according to FishEc collection at Eawag, Switzerland), location (island at southern Lake Victoria), date of capture and death, capture water depth (m) of cichlid specimens that harboured the species of Cichlidogyrus (re)described in this study. Access here

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Cite this article as: Gobbin TP, Vanhove MPM, Seehausen O, Maan ME & Pariselle A. 2024. Four new species of Cichlidogyrus (Platyhelminthes, Monopisthocotyla, Dactylogyridae) from Lake Victoria haplochromine cichlid fishes, with the redescription of C. bifurcatus and C. longipenis. Parasite 31, 46.

All Tables

Table 1

Haplochromine host species (n fish: number of host individuals) sampled in May-August 2010 and June-October 2014 at five localities (Makobe, Sweya, Kissenda, Luanso, Python) in southern Lake Victoria and the sample size of identified specimens of Cichlidogyrus (n Cichlidogyrus). The radiation lineage is labelled with a circle (●), the two lineages that did not speciate are labelled with a square (■) and a diamond (◆).

In the text
Table 2

Measurements of Cichlidogyrus bifurcatus and C. longipenis redescribed from haplochromine host species of Lake Victoria (N = number of specimens, n = number of observations per trait per species) compared to those provided by Paperna [35] and Paperna & Thurston [38] (expressed as ranges only, because means were not reported in the original descriptions). For C. longipenis, we also report measurements extrapolated from the drawing of the original description and our measurements from the syntype. All measurements in μm, given as the mean and range (in parentheses).

In the text
Table 3

Measurements of the new species of Cichlidogyrus described from haplochromine host species of Lake Victoria (N = number of specimens, n = number of observations per trait per species). All measurements in μm, given as the mean and range (in parentheses).

In the text

All Figures

thumbnail Figure 1

Geographical location of the five sampling sites in southern Lake Victoria, Tanzania: rocky islands Makobe (M), Kissenda (K), Python (P), Luanso (L), and the Sweya swampy inlet stream (S).
In the text
thumbnail Figure 2

Schematic overview of a specimen of Cichlidogyrus with its typical morphological sclerotised structures (MCO, male copulatory organ in the upper part of the parasite image, attachment organ in the bottom part) and measurements used in the descriptions of the new species. Abbreviations: A, anchor (a, total length; b, blade length; c, shaft length; d, guard length; e, point length); DB, dorsal bar (h, auricle length; w, maximum straight width; x, total length; y, distance between auricles); VB, ventral bar (x, length of one ventral bar branch; w, maximum width); H, hook length; Pe, penis curved length; He, heel straight length; Ap, accessory piece straight length.
In the text
thumbnail Figure 3

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus longipenis. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar; VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ (on the left as observed in most of our specimens, on the right the phenotype similar to the one reported by Paperna & Thurston, 1969): Ap, accessory piece; Pe, penis. Scale bar: 20 μm.
In the text
thumbnail Figure 4

Micrographs of the male copulatory organ of Cichlidogyrus longipenis, from a parasite individual of the present study (left) and from the holotype by Paperna & Thurston, 1969 (right), fixed in two different mediums. Scale bar: 20 μm.
In the text
thumbnail Figure 5

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus bifurcatus. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar, VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ: AP, accessory piece; Pe, penis; He, heel. Scale bar: 20 μm.
In the text
thumbnail Figure 6

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus pseudodossoui n. sp. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar; VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ: AP, accessory piece; Pe, penis; He, heel; Vg, vagina. Scale bar: 20 μm.
In the text
thumbnail Figure 7

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus nyanza n. sp. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar; VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ: AP, accessory piece; Pe, penis. Scale bar: 20 μm.
In the text
thumbnail Figure 8

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus furu n. sp. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar; VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ: AP, accessory piece; Pe, penis; He, heel. Scale bar: 20 μm.
In the text
thumbnail Figure 9

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus cf. furu n. sp. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar; VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ: AP, accessory piece; Pe, penis; He, heel. Scale bar: 20 μm.
In the text
thumbnail Figure 10

Micrographs of the male copulatory organ of Cichlidogyrus furu n. sp. (left) and of C. cf. furu n. sp. (right), fixed in Hoyer’s medium. Scale bar: 20 μm.
In the text
thumbnail Figure 11

Sclerotised parts (haptor and male copulatory organ) of Cichlidogyrus vetusmolendarius n. sp. I–VII, hook pairs; DA, dorsal anchors; DB, dorsal transverse bar; VA, ventral anchors; VB, ventral transverse bar. MCO, male copulatory organ: AP, accessory piece; Pe, penis; He, heel. Scale bar: 20 μm.
In the text

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