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Article

New Records and Descriptions of Three New Species of Quadriacanthus (Monopisthocotyla: Dactylogyridae) from Catfishes (Teleostei: Siluriformes, Clariidae) in the Upper Congo Basin

by
Gyrhaiss K. Kasembele
1,2,
Maarten P. M. Vanhove
2,3,4,5,*,
Archimède Mushagalusa Mulega
2,6,7,
Auguste Chocha Manda
1,
Michiel W. P. Jorissen
2,3,
Wilmien J. Luus-Powell
8,
Willem J. Smit
8,
Charles F. Bilong Bilong
9 and
Dieu-ne-dort Bahanak
10
1
Unité de Recherche en Biodiversité et Exploitation durable des Zones Humides (BEZHU), Faculté des Sciences Agronomiques, Université de Lubumbashi, Lubumbashi P.O. Box 1825, Democratic Republic of the Congo
2
Research Group Zoology: Biodiversity & Toxicology, Centre for Environmental Sciences, Hasselt University, BE-3590 Diepenbeek, Belgium
3
Department of Biology, Royal Museum for Central Africa, Leuvensesteenweg 13, BE-3080 Tervuren, Belgium
4
Laboratory of Biodiversity and Evolutionary Genomics, Department of Biology, KU Leuven, Ch. Deberiotstraat 32, BE-3000 Leuven, Belgium
5
Capacities for Biodiversity and Sustainable Development, Operational Directorate Natural Environment, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, BE-1000 Brussels, Belgium
6
Laboratory Biodiversity, Ecology and Genome, Research Center Plant and Microbial Biotechnology, Biodiversity and Environment, Mohammed V University in Rabat, Rabat 10100, Morocco
7
Département de Biologie, Centre de Recherche en Hydrobiologie, Uvira P.O. Box 73, Democratic Republic of the Congo
8
DSI-NRF SARChI Chair in Ecosystem Health, Department of Biodiversity, University of Limpopo, Sovenga 0727, South Africa
9
Laboratory of Parasitology and Ecology, Faculty of Sciences, University of Yaoundé 1, Yaoundé P.O. Box 337, Cameroon
10
Institute of Agricultural Research-Minko Multipurpose Research Station, Meyomessala P.O. Box 167, Cameroon
*
Author to whom correspondence should be addressed.
Animals 2025, 15(3), 395; https://doi.org/10.3390/ani15030395
Submission received: 6 January 2025 / Revised: 21 January 2025 / Accepted: 21 January 2025 / Published: 30 January 2025
(This article belongs to the Collection Diagnosis, Evaluation, and Management of Wildlife, Exotic and Zoo Animals Disease)
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Simple Summary

Monogenean flatworms are mainly parasitic in lower aquatic vertebrates including fish, anurans and chelonians. Quadriacanthus is one of the four genera infecting African clariids. To date, 45 members of the genus are described, but this is still embryonic compared to the expected parasite and host species richness in Africa. In this study, we examined the gills of five species of Clarias: Clarias ngamensis, C. stappersii, C. buthupogon, C. gariepinus and C. theodorae. Eight parasite species morphologically characterised as belonging to Quadriacanthus were identified, among them five known species and three that are newly described here. In view of the importance of the clariids in this study system, this part of aquatic biodiversity is still to be further studied to contribute to inventorying parasite species in Africa.

Abstract

In the Upper Congo Basin, there are few records of monopisthocotylan parasites from clariids. More surveys of clariid fishes can lead to the discovery of multiple monopisthocotylan species that are new to the region or new to science. We aimed to investigate the monopisthocotylan parasite fauna belonging to Quadriacanthus of five clariid fishes in the Upper Congo Basin by (i) inventorying the species composition and providing the description of new species when necessary, and (ii) analysing their infection parameters. Clarias ngamensis, C. stappersii, C. buthupogon, C. gariepinus and C. theodorae were purchased from fishermen in the Lufira, Lubumbashi and Kafubu rivers in the Upper Congo Basin. Monopisthocotylans were mounted on glass slides with ammonium picrate-glycerin for identification based on morphological analysis of genital and haptoral sclerotised parts. Eight species, namely Q. aegypticus, Q. allobychowskiella, Q. amakaliae, Q. domatanai, Q. halajiani, Q. kalomboi n. sp., Q. bassocki n. sp. and Q. shigoleyae n. sp. are reported. The most prevalent parasite species was Q. amakaliae on C. stappersii (prevalence 60%) with a mean infection intensity of 9.8 ± 7.7. We report C. stappersii and C. buthupogon as new hosts for species of Quadriacanthus as well as three new parasite species for science and new localities for the first five parasite species mentioned above. The new records and the description of Q. kalomboi n. sp., Q. bassocki n. sp. and Q. shigoleyae n. sp. increase the knowledge of the diversity of monopisthocotylans in this region.

1. Introduction

In the past decade, there has been a growing focus on the study of monopisthocotylan parasites in the Upper Congo Basin. Several studies have been conducted on monopisthocotylan parasites in Lake Tanganyika and the Bangweulu–Mweru and Upper Lualaba Ecoregions [1] (e.g., [2,3,4,5,6,7,8,9,10,11,12]). Many of these studies focused on cichlid fishes, while Prudhoe [13], Vanhove et al. [14], Mushagalusa Mulega et al. [8] and Kasembele et al. [6] reported monopisthocotylans of clariid fishes, the former three for Clarias gariepinus (Burchell, 1822) and the latter for C. ngamensis Castelnau, 1861. Considering the whole Congo Basin, a total of 13 clariid species are reported [15]; among them, seven species are present in the Upper Congo Basin (C. gariepinus; C. ngamensis; C. buthupogon Sauvage, 1879; C. dumerilii Steindachner, 1866; C. liocephalus Boulenger, 1898; C. stappersii Boulenger, 1915; C. theodorae Weber, 1897) [16,17]. The latter five fish species have never been studied for their monopisthocotylan fauna [18]. Monopisthocotyla Brabec, Salomak, Kolísko, Scholz & Kuchta, 2023 is one of two major clades within Monogenea, which is a diverse but paraphyletic [19] group of parasitic flatworms reported from freshwater, brackish and marine fishes, crustaceans, cephalopods, amphibians, and reptiles with one species from a mammal [18]. The high species richness of Monopisthocotyla and the relatively narrow host specificity of its members are used today as an important asset in understanding parasite adaptation, evolution and speciation via host switching [20,21]. There is also a great interest in the host–parasite interaction networks due to the importance of considering the community context to better understand the ecological and evolutionary implications of these interactions [22]. In addition, monopisthocotylans can be used for detecting pollution, indicating host biology, and as tools in phylogeny, biogeography and host systematics [23,24,25,26].
African clariids harbour monopisthocotylan gill parasites belonging to Birgiellus Bilong Bilong, Nack and Euzet, 2007, Gyrodactylus von Nordmann, 1832, Macrogyrodactylus Malmberg, 1957 and Quadriacanthus Paperna, 1961 [27,28,29,30,31]. The latter genus comprises 45 known species worldwide recorded from clariids (13 fish species), bagrids (three fish species), notopterids (one fish species), claroteids (one fish species), and cichlids (one fish species) [6,18,32,33]. Given the large number of identified and unidentified host species not yet examined for parasites, it can be anticipated that the recorded monopisthocotylan diversity is incomplete. Thus, it can be hypothesised that further parasitological surveys in the Upper Congo Basin may lead to the recording of many parasite species, including undescribed species, as some fish species remain to be surveyed for their monopisthocotylan parasites (see e.g., [34]). This study focuses on the monopisthocotylan parasite fauna belonging to Quadriacanthus of five clariid fishes: the Blunt-toothed African catfish C. ngamensis, the Blotched catfish C. stappersii, C. buthupogon, the North African catfish C. gariepinus and the Snake catfish C. theodorae (Teleostei: Siluriformes, Clariidae) occurring in the Upper Congo Basin. Objectives include (i) inventorying the diversity of Quadriacanthus species and, in case of the discovery of new species, providing their description and (ii) analysing infection parameters of these monopisthocotylan parasites.

2. Materials and Methods

2.1. Study Area

This study was carried out in the south of the former Katanga province in the Upper Congo Basin, especially (I) in the Upper Lualaba Ecoregion (sensu Thieme et al. [1]) in the Lufira River, which is a major tributary of the Lualaba River [35,36], and (II) in the Bangweulu–Mweru Ecoregion (sensu Thieme et al. [1]) in (i) the Lubumbashi River, which originates west of the city of Lubumbashi and flows into (ii) the Kafubu River, which is a tributary of the Luapula River (Figure 1).

2.2. Fish Sampling

The sampling was opportunistic, without targeting the number of fishes to be dissected, in advance. Fish were bought alive from fishermen along the shores of Lufira (September 2015, November 2021), Lubumbashi and Kafubu rivers from November 2020 to July 2021 and then transported alive in aerated tanks containing river water to the laboratory of Biodiversité et Exploitation durable des Zones Humides (BEZHU) of the Université de Lubumbashi. Since gills of live fish cannot be exhaustively inspected for monogeneans [18], the fish were killed by severing the spinal cord just posterior to the cranium and identified following the keys proposed by Teugels [37] immediately prior to examination [38].

2.3. Parasite Sampling

Fish were dissected and right gill arches removed by dorso-ventral section. These were placed in a Petri dish containing water for examination using a stereomicroscope Optika 4.0.0 (OPTIKA Srl, Ponteranica, Italy). Parasites were dislodged from the gill filaments using entomological needles and fixed between slide and cover slip into a drop of ammonium picrate-glycerin, according to Nack et al. [39]. Twenty-four hours later, coverslips were sealed using nail varnish.

2.4. Monopisthocotylan Community Composition and Infection Parameters

Parasite identification was based on the morphology and the size of sclerotised parts of the genital and the haptor [20,39]. The measurements were carried out according to Gussev [40] and modifications by N’Douba et al. [41] (Figure 2) with the aid of a Leica DM 2500 microscope (Leica Microsystems CMS GmbH, Wetzlar, Germany), LAS software (3.8), and drawings of the sclerotised parts of the genital structures and haptor were made with the aid of Corel Draw Graphics Suite X8 software (Corel Corporation, www.corel.com/). Measurements in micrometers (µm) are presented as follows: mean (minimum–maximum). To comply with the regulations set out in article 8.5 of the amended 2012 version of the International Code of Zoological Nomenclature (ICZN) [42], details of the new species have been submitted to ZooBank. The Life Science Identifier (LSID) of the article is urn:lsid:zoobank.org:pub:FAF64692-C810-438A-9CDE-C3C796E3AF88. For each new species, the LSID is reported in the taxonomic summary. Note that the authors of the new taxa are different from the authors of this article; see Article 50.1 and Recommendation 50 A of the International Code of Zoological Nomenclature [43]. Parasite diversity is summarized by the species richness; regarding infection parameters, prevalence (P) and mean intensity (MI) are provided following definitions given by Margolis et al. [44] and Bush et al. [45] and categorised following Valtonen et al. [46].

3. Results

A total of 85 fish specimens of the five clariid fish species (C. ngamensis, n = 14; C. stappersii, n = 32; C. buthupogon, n = 9; C. gariepinus, n = 11; C. theodorae, n = 19) were dissected in the Upper Congo Basin (Table 1).
The investigation of gill filaments resulted in the record of eight monopisthocotylan species (Table 2). The morphology of the monogeneans found corresponds to the diagnosis of Quadriacanthus following Paperna [27] and amendments by Kritsky and Kulo [47]. Among these eight monopisthocotylan species recorded, five are known (Q. aegypticus El-Naggar & Serag, 1986, Q. allobychowskiella Paperna, 1979, Q. amakaliae Kasembele, Bahanak & Vanhove, 2024 (Figure 3a,b), Q. domatanai Kasembele, Bahanak & Vanhove, 2024 (Figure 3c,d), Q. halajiani Kasembele, Bahanak & Vanhove, 2024 (Figure 3e,f)) [6,30,48] and three (Q. kalomboi n. sp., Q. bassocki n. sp. and Q. shigoleyae n. sp.) are newly described (see Table 2; Figure 4, Figure 5, Figure 6 and Figure 7). Descriptions of new species are given below, and the infection parameters of all the retrieved species are provided in Table 2. No monopisthocotylan parasite was found on the gills of C. stappersii from Lubumbashi River nor from the gills of C. theodorae from both Lubumbashi and Kafubu rivers.
  • Quadriacanthus kalomboi n. sp.
ZooBank registration: The LSID for Quadriacanthus kalomboi Kasembele, Bahanak & Vanhove n. sp. is urn:lsid:zoobank.org:act:87B042BC-5206-4BCA-A207-227EF1226227.
  • Host: Clarias stappersii
  • Locality: Democratic Republic of the Congo, Kafubu River 11°43′50.00″ S; 27°27′42.60″ E, G.K. Kasembele leg.
  • Collection date: 4 June 2021
  • Site of infection: gills
  • Material: The holotype HU n°1005 is deposited in the collection of the Research Group Zoology: Biodiversity & Toxicology of Hasselt University (Diepenbeek, Belgium).
  • Prevalence: P = 8.3%; mean intensity: MI = 1
  • Etymology: This species is named in honour of Kalombo Kabalika Clément, MSc, from the Unité de Recherche en Biodiversité et Exploitation durable des Zones Humides, Faculté des Sciences Agronomiques, Université de Lubumbashi, DR Congo, for his valuable and kind assistance during our field campaigns.
  • Description
Dorsal anchor without shaft nor guard, with broad base, shaft sharply curved, ending with a short point. Dorsal bar with rectangular centre, a medium median process posteriorly directed and two lateral expansions. Dorsal cuneus triangular. Ventral anchor without shaft nor guard with regularly curved blade. Ventral bar V-shaped with two lateral branches. Y-shaped ventral cuneus. Seven pairs of hooks: pair IV larger than the rest which are almost equal in length (Figure 4 and Figure 7a,b). Tubular male copulatory organ (MCO) in the form of straight tube, flared, wide at the base and narrow at the distal extremity. Accessory piece (AP) ending like a hook with three small outgrowths: two posteriorly and one anteriorly, giving an appearance of a flame. No sclerotised vagina observed. Measurements of sclerotised pieces taken from one flattened specimen are shown in Table 3.
Animals 15 00395 g004
Figure 4. Sclerotised parts of the genitals and haptor of Quadriacanthus kalomboi n. sp. with the male copulatory organ (MCO), accessory piece (AP), ventral bar (VB), ventral anchor (VA), ventral cuneus (Vcn), dorsal bar (DB), dorsal anchor (DA), dorsal cuneus (Dcn), (I–VII) hooks.
Figure 4. Sclerotised parts of the genitals and haptor of Quadriacanthus kalomboi n. sp. with the male copulatory organ (MCO), accessory piece (AP), ventral bar (VB), ventral anchor (VA), ventral cuneus (Vcn), dorsal bar (DB), dorsal anchor (DA), dorsal cuneus (Dcn), (I–VII) hooks.
Animals 15 00395 g004
  • Differential diagnosis
This species is comparable to Q. lubandaensis Kasembele, Bahanak & Vanhove, 2024 and Q. fornicatus Francová & Řehulková, 2017, described from C. ngamensis in the Bangweulu–Mweru Ecoregion (DRC), and C. gariepinus from Sudan [6,49], respectively, because of the morphology of the ventral bars (shape of the two elongated components) and anchors (moderate base, curved shaft, long point) and the MCO (straight tube, base simple). However, Q. kalomboi n. sp. can be differentiated from these two species by the morphology of its accessory piece in the shape of a flame with three small outgrowths versus in the form of a spike-like structure for Q. fornicatus and a simple hook-like ending in Q. lubandaensis.
  • Quadriacanthus bassocki n. sp.
ZooBank registration: The LSID for Quadriacanthus bassocki Kasembele, Bahanak & Vanhove n. sp. is urn:lsid:zoobank.org:act:5C1B53FD-FE53-4F70-A354-76EC47FDF0E7.
  • Host: Clarias gariepinus
  • Locality: Democratic Republic of the Congo, Kafubu River 11°43′50.00″ S; 27°27′42.60″ E, G.K. Kasembele leg.
  • Collection date: 4 June 2021
  • Site of infection: gills
  • Other hosts: C. stappersii; C. buthupogon
  • Other locality: DR Congo, Lubumbashi River 11°39′19.20″ S; 27°27′37.40″ E
  • Material: The holotype HU n°1006 and 36 paratypes HU n°1007–1042 are deposited in the collection of the Research Group Zoology: Biodiversity & Toxicology of Hasselt University (Diepenbeek, Belgium).
  • Prevalence: P = 50% (Kafubu River); mean intensity: MI = 1
  • Etymology: This species is named in honour of Dr. Etienne Bassock Bayiha of the Laboratory of Parasitology and Ecology, Faculty of Sciences, University of Yaoundé 1, Cameroon, for his contribution in lab work.
  • Description
Dorsal bar with rectangular centre, a long median process posteriorly directed and two lateral expansions. Dorsal anchor without shaft nor guard with broad base, shaft sharply curved, ending with a short point. Dorsal cuneus triangular. Ventral bar V-shaped with two lateral branches. Ventral anchor without shaft nor guard, with base smaller than the base of the dorsal anchor, and curved blade. Ventral cuneus smaller than dorsal one. Seven pairs of hooks: pair IV longer than the rest, which are almost equal in length (Figure 5 and Figure 7c,d). A tube-shape MCO flared, wide and thick-walled at its base, gradually narrowing towards the distal extremity. The accessory piece, simple and articulated to the MCO, ending in a well-developed long point. Tubular vagina partly sclerotised. Measurements of sclerotised pieces taken from ten flattened specimens are shown in Table 3.
Animals 15 00395 g005
Figure 5. Sclerotised parts of the genitals and haptor of Quadriacanthus bassocki n. sp. with the male copulatory organ (MCO), accessory piece (AP), vagina (Vg), ventral bar (VB), ventral anchor (VA), ventral cuneus (Vcn), dorsal bar (DB), dorsal anchor (DA), dorsal cuneus (Dcn), (I–VII) hooks.
Figure 5. Sclerotised parts of the genitals and haptor of Quadriacanthus bassocki n. sp. with the male copulatory organ (MCO), accessory piece (AP), vagina (Vg), ventral bar (VB), ventral anchor (VA), ventral cuneus (Vcn), dorsal bar (DB), dorsal anchor (DA), dorsal cuneus (Dcn), (I–VII) hooks.
Animals 15 00395 g005
  • Differential diagnosis
Quadriacanthus bassocki n. sp. is comparable to Q. amakaliae, Q. barombiensis Bahanak, Nack & Pariselle, 2022, Q. levequei Birgi, 1988 and Q. anaspidoglanii Akoumba, Pariselle & Tombi, 2017, described, respectively, from C. ngamensis (in DR Congo), C. maclareni Trewavas, 1962, C. pachynema Boulenger, 1903 and Notoglanidium macrostoma (Pellegrin, 1909), in Cameroon [20,50,51]. They are similar in the morphology of the dorsal bar with a rectangular centre, a funnel-shaped median process that is posteriorly directed, without filaments at its end like in Q. amakaliae and Q. anaspidoglanii; the tubular shape of the MCO, wide at its base and gradually shrinking towards the distal extremity; the shape of the distal part of the AP ending in a point like in Q. levequei, Q. anaspidoglanii and Q. barombiensis. However, Q. bassocki n. sp. can be differentiated from Q. barombiensis and Q. levequei by the absence of filaments on the median process, which is present in the latter two parasite species; the distal extremity of the AP ending in a simple point for Q. bassocki n. sp. versus the distal extremity of the AP surrounded by two filaments for Q. amakaliae and two small hooks for Q. levequei.
  • Quadriacanthus shigoleyae n. sp.
ZooBank registration: The LSID for Quadriacanthus shigoleyae Kasembele, Bahanak & Vanhove n. sp. is urn:lsid:zoobank.org:act:99AD47E2-D042-4125-A297-029295CD1CE2.
  • Host: Clarias ngamensis
  • Locality: Democratic Republic of the Congo, Lufira River 11°4′31.60″ S; 26°55′2.40″ E, G.K. Kasembele leg.
  • Collection date: 30 September 2015
  • Site of infection: gills
  • Material: The holotype HU n°1043 and 48 paratypes HU n°1044–1091 are deposited in the collection of the Research Group Zoology: Biodiversity & Toxicology of Hasselt University (Diepenbeek, Belgium).
  • Prevalence: P = 33.3%; mean intensity: MI = 17 ± 20.7 parasites
  • Etymology: This species is named in honour of Miriam Isoyi Shigoley, MSc, for her kind contribution in the lab work, during the first author’s predoctoral visit at the Centre for LIST Environmental Sciences of Hasselt University (Belgium).
  • Description
Dorsal anchor without shaft nor guard with broad base, shaft sharply bent, short point. Dorsal bar with rectangular centre, a broad and long median process posteriorly directed and two lateral expansions. Dorsal cuneus triangular. Ventral anchor without shaft nor guard with narrow base and curved blade. Ventral bar V-shaped with two lateral branches. Ventral cuneus triangular. Seven pairs of hooks: pair IV larger than pairs III, I, V, VI and VII, the four latter pairs almost equal in length (Figure 6 and Figure 7e,f). MCO tube-shaped, flared at the base and distal end like a femur (thighbone). Accessory piece, articulated around the MCO, composed of narrow base, thick median part, an animal tail-like distal part and ending in a point. No sclerotised vagina observed. Measurements of sclerotised pieces taken from seven flattened specimens are shown in Table 3.
Animals 15 00395 g006
Figure 6. Sclerotised parts of the genital and haptor of Quadriacanthus shigoleyae n. sp. with the male copulatory organ (MCO), accessory piece (AP), ventral bar (VB), ventral anchor (VA), ventral cuneus (Vcn), dorsal bar (DB), dorsal anchor (DA), dorsal cuneus (Dcn), (I–VII) hooks.
Figure 6. Sclerotised parts of the genital and haptor of Quadriacanthus shigoleyae n. sp. with the male copulatory organ (MCO), accessory piece (AP), ventral bar (VB), ventral anchor (VA), ventral cuneus (Vcn), dorsal bar (DB), dorsal anchor (DA), dorsal cuneus (Dcn), (I–VII) hooks.
Animals 15 00395 g006
  • Differential diagnosis
Quadriacanthus shigoleyae n. sp. resembles Q. curvicirrus Kasembele, Bahanak & Vanhove, 2024 described from C. ngamensis (in DR Congo) [6]. They are similar in the morphology of the ventral (shape of the two elongated branches) and dorsal (with rectangular centre, broad and long median process posteriorly directed and two lateral expansions) bars, and the dorsal anchors (broad base, shaft sharply bent, short point) and cunei (triangular). They can be distinguished by the characteristic genital shape of each species, femoral tube-shaped MCO, with a thickened AP ending in a tail-shaped extremity with a pointed ending for Q. shigoleyae n. sp. versus a tube-shaped MCO curved at its distal end with a simple base and a massive accessory piece with outgrowths posteriorly and anteriorly directed for Q. curvicirrus.
Animals 15 00395 g007
Figure 7. Photomicrographs of the sclerotised structures of the genitals and haptor of (a,b) Quadriacanthus kalomboi n. sp. ex Clarias stappersii from Kafubu River, (c,d) Quadriacanthus bassocki n. sp. ex Clarias buthupogon from Lubumbashi River, and (e,f) Quadriacanthus shigoleyae n. sp. ex Clarias ngamensis from Lufira River. Scale bar 20µm.
Figure 7. Photomicrographs of the sclerotised structures of the genitals and haptor of (a,b) Quadriacanthus kalomboi n. sp. ex Clarias stappersii from Kafubu River, (c,d) Quadriacanthus bassocki n. sp. ex Clarias buthupogon from Lubumbashi River, and (e,f) Quadriacanthus shigoleyae n. sp. ex Clarias ngamensis from Lufira River. Scale bar 20µm.
Animals 15 00395 g007

4. Discussion

The new records of Q. aegypticus, Q. allobychowskiella, Q. amakaliae, Q. domatanai, Q. halajiani and the descriptions of Q. kalomboi n. sp., Q. bassocki n. sp. and Q. shigoleyae n. sp. increase the knowledge of the diversity of monopisthocotylans in the Upper Congo Basin. Consequently, the number of known species of Quadriacanthus is extended to 48. From Africa, Řehulková et al. [18] reported 34 valid species; Bouah et al. [52] described two species; Bahanak et al. [20] described one species; Mushagalusa Mulega et al. [9] described one species; Kasembele et al. [6] described five species; and from Asia, Tripathi et al. [53] redescribed and synonymised two species of Quadriacanthus in their checklist. This study is the first record of monogenean flatworms on C. stappersii and C. buthupogon. Given the sample size for all fish species (including C. gariepinus, C. ngamensis and C. theodorae), it cannot be ascertained that the number of parasite species recorded is exhaustive.
The discovery of several new species and new host records in this study further emphasises how understudied this group is.
Regarding host range, Q. amakaliae, which is originally described from C. ngamensis in Lake Lubanda (DR Congo) [6] and now recorded on C. stappersii and C. buthupogon, should currently be considered a parasite with a mesostenoxenous specificity (more than one host, but restricted to one genus), infesting two or more congeneric host species [54,55,56]. The record of Quadriacanthus aegypticus, Q. allobychowskiella, Q. domatanai and Q. halajiani in this study is considered as a new locality record given that these parasite species were already reported on C. ngamensis by Kasembele et al. [6]. Another noteworthy observation is the description of Q. bassocki n. sp. from C. gariepinus which is known to harbour 11 species of Quadriacanthus from different basins/ecoregions or geographic areas [18,32,33,53], bringing the number of species within the genus infesting it to 12. This study demonstrates again that more sampling efforts can lead to the discovery of more parasite species and the recording of more host–parasite combinations even on relatively better-studied host species. Combes [57] states that sampling fewer than 30 hosts does not reveal the presence of species with low prevalence and abundance.
Indeed, differences in infection parameters could be attributed to factors such as season, biogeographical distribution, sample size or other environmental conditions. Communities of monogeneans have been shown to vary seasonally and across different habitat types, and the composition of parasite species may differ between regions and basins [58,59]. Nevertheless, the record of species being random, other similar studies successfully investigated less than 30 host specimens, and they still recorded or described many parasite species including rare ones, e.g., Q. aegypticus (P = 6.7%, MI: 1 ± 1) and Q. amakaliae (P = 6.7%, MI: 1 ± 0) recorded by [5] on C. ngamensis in Lake Lubanda (n, number of fish specimens= 15) and the Luapula River (n = 15); Q. thysi N’Douba, Lambert & Euzet 1999 (P = 8.3%, MI = 0.08) infecting Heterobranchus longifilis Valenciennes, 1840 (n = 12) in Cameroon [60]; Gyrodactylus nyingiae (P = 33.3%, MI: 1 ± 0) on Pterocapoeta maroccana Günther, 1902 (n = 3) in Morocco [61]; and Quadriacanthus spp. (13.3% < P < 40%, 1 < MI < 5.3) from C. gariepinus (n = 15) in South Africa [33]. The results of this study are furthermore consistent with the hypothesis that the potential host diversity in the tropics and the relatively narrow specificity of Quadriacanthus spp. could lead to the discovery of several, also new, parasite species [50,51,62].
Considering infection parameters in the current study area, Q. amakaliae is the most prevalent species with P = 60% for C. stappersii reported from the Lufira River, P = 50% for C. buthupogon from the Kafubu River, which is followed by Q. bassocki n. sp. (P = 50%) on both C. buthupogon and C. gariepinus from the Kafubu River. Parasite taxa are classified as common (P > 50%), intermediate (10–50%), or rare (<10% prevalence) by Valtonen et al. [46]. The prevalence of the other Quadriacanthus species is 10 < P < 50% (rendering them intermediate taxa in this study system) except for Q. kalomboi n. sp. and Q. bassocki n. sp. both from C. stappersii from Kafubu River (rare taxa here, P < 10%). Quadriacanthus amakaliae was ranked as common taxon in the Lufira River system and intermediate taxon in the Kafubu River system here and had previously been recorded as rare taxon from C. ngamensis in the Upper Congo Basin [6]. Infection parameters change depending on host and environmental factors [63,64]. In terms of mean intensities, parasite species can be classified as being of high intensity (MI > 100), medium (50 ≤ MI ≤ 100), low (10 ≤ MI < 50) or very low intensity (MI < 10) [46]. Results of this study show two groups, the first comprising Q. shigoleyae n. sp. (MI = 17 ± 20.7) on C. ngamensis from Lufira River, Q. bassocki on C. buthupogon from Kafubu River (11 ± 0) and Lubumbashi River (8 ± 11.9), and Q. amakaliae (9.8 ± 7.7) on C. stappersii from Lufira River, showing low mean intensity in these systems. This is different from the second group comprising the rest of the species, here exhibiting very low mean intensity levels. Values found for the second group are similar to those found by Kasembele et al. [6] especially for Q. aegypticus and Q. allobychowskiella on C. ngamensis from the Upper Congo Basin. Once more, infection levels vary with environmental conditions (physico-chemical parameters of water, e.g., the state of pollution of the water, potential eutrophication), or the host densities. Particularly influential can be the difference between conditions in nature versus in aquaculture, where fish are close and in permanent contact, and an oncomiracidium can quickly find a host after a short free swimming period [24,64,65,66,67,68].

5. Conclusions

We reported eight gill monopisthocotylan species belonging to Quadriacanthus from the clariid fishes C. ngamensis, C. stappersii, C. buthupogon and C. gariepinus in the Upper Congo Basin. For Q. amakaliae, we report a new host record, and for Q. aegypticus, Q. allobychowskiella, Q. domatanai and Q. halajiani, we report new locality records. Quadriacanthus kalomboi n. sp., Quadriacanthus bassocki n. sp. and Quadriacanthus shigoleyae n. sp. are described as new species. For future sampling, higher numbers of host specimens and more regions in the Upper Congo Basin are intended to be covered to record more information on monopisthocotylan diversity [5,6].

Author Contributions

G.K.K. carried out the study (sampled fishes, collected parasites, performed morphological identification of parasites, analysed data and wrote the paper). M.P.M.V., C.F.B.B., D.-n.-d.B. helped with the morphological identification of parasites species. M.P.M.V., A.M.M., A.C.M., M.W.P.J., W.J.L.-P., W.J.S., C.F.B.B., D.-n.-d.B. helped with the writing of the paper, analysis of the data, interpretation and discussion of results and provided scientific background in the field of monopisthocotylan research. All authors have read and agreed to the published version of the manuscript.

Funding

The network underlying this study arose thanks to funding from VLIR-UOS, namely the Short Training Initiative “Building an African network for sustainable management of aquatic biological resources supported by genetics and parasitology” (NKOI2016PR008) and the South Initiative “Renforcement des capacités locales pour une meilleure évaluation biologique des impacts miniers au Katanga (RD Congo) sur les poissons et leurs milieux aquatiques” (ZRDC2014MP084), and from the framework agreements of the Belgian Development Cooperation with the Royal Museum for Central Africa (Mbisa Congo project 2013–2018) and the Royal Belgian Institute of Natural Sciences (Capacities for Biodiversity and Sustainable Development program). This research was also supported by VLIR-UOS (IUC-UNILU, CD2021IUC04A104 and Global Minds). Maarten P.M. Vanhove was financed by the Special Research Fund of Hasselt University (BOF20TT06). Wilmien J. Luus-Powell and Willem J. Smit were supported by the South African Research Chairs Initiative of the Department of Science and Innovation and National Research Foundation of South Africa (Grant No. 101054). The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Institutional Review Board Statement

In the absence of relevant animal welfare regulations in the DRC, we used the guidelines and authorization in accordance with the Unité de Recherche en Biodiversité et Exploitation durable des Zones Humides (BEZHU) of the Université de Lubumbashi. Fishes were bought from fishermen (Autorisation d’échantillonnage N/Réf/fac/Agro/646/2015; Autorisation d’échantillonnage N/Réf/fac/Agro/714/2019).

Informed Consent Statement

Not applicable.

Data Availability Statement

Parasites were deposited in the collection of the Research Group Zoology: Biodiversity & Toxicology, at Hasselt University (Diepenbeek, Belgium) under accession numbers HU n°1005–HU n°1094 (type material) and XXII.3.45–XXIII.1.40 (reference material).

Acknowledgments

The Université de Lubumbashi is thanked through the Faculty of Agronomic Sciences (for facilitating and authorising sampling) and the local team of the Laboratory BEZHU (Unité de Recherche en Biodiversité et Exploitation durable des Zones Humides), Anicet Doma Tana, Clément Kalombo Kabalika for their help in fish sampling. The University of Yaoundé 1 (Cameroon) is also thanked through the Faculty of Sciences, Laboratory of Parasitology and Ecology (Etienne Bassock and Jonathan Mbondo) for hosting and helping Gyrhaiss K. Kasembele in the lab for parasite identification and drawing during his research visit. The authors gratefully acknowledge Antoine Pariselle, Filip A.M. Volckaert, Ouafae Berrada-Rkhami, Abdelaziz Benhoussa, Tine Huyse, Isaure de Buron-Connors, Valentin N’Douba, Arnold R. Bitja Nyom, Jos Snoeks, Emmanuel J. Vreven, Virginie Bito, and Luc Janssens de Bisthoven, senior scientists in the aforementioned projects.

Conflicts of Interest

The authors declare no conflicts of interest.

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Animals 15 00395 g001
Figure 1. Map of sampling sites in the Upper Congo Basin: Lufira River 11°4′31.60″ S; 26°55′2.40″ E; Lubumbashi River 11°39′19.20″ S; 27°27′37.40″ E; Kafubu River 11°43′50.00″ S; 27°27′42.60″ E.
Figure 1. Map of sampling sites in the Upper Congo Basin: Lufira River 11°4′31.60″ S; 26°55′2.40″ E; Lubumbashi River 11°39′19.20″ S; 27°27′37.40″ E; Kafubu River 11°43′50.00″ S; 27°27′42.60″ E.
Animals 15 00395 g001
Animals 15 00395 g002
Figure 2. Morphometrics of Quadriacanthus spp. used in this study are based on Gussev [40] with modifications by N’Douba et al. [41]. MCO: male copulatory organ length; AP: accessory piece length; MCC: male copulatory complex (MCO and AP combined); I–VII: hook length; DB: dorsal bar: (x) length, (w) width, (h) median process length, (ct) centre length; DA: dorsal anchor: (a) length, (ab) base diameter or width, (e) point length; DCn: dorsal cuneus (j) length; VB: ventral bar: (x) length, (w) width; VA: ventral anchor: (a) length, (ab) base diameter or width, (e) point length; VCn: ventral cuneus (i) length; Vg: vagina length [6].
Figure 2. Morphometrics of Quadriacanthus spp. used in this study are based on Gussev [40] with modifications by N’Douba et al. [41]. MCO: male copulatory organ length; AP: accessory piece length; MCC: male copulatory complex (MCO and AP combined); I–VII: hook length; DB: dorsal bar: (x) length, (w) width, (h) median process length, (ct) centre length; DA: dorsal anchor: (a) length, (ab) base diameter or width, (e) point length; DCn: dorsal cuneus (j) length; VB: ventral bar: (x) length, (w) width; VA: ventral anchor: (a) length, (ab) base diameter or width, (e) point length; VCn: ventral cuneus (i) length; Vg: vagina length [6].
Animals 15 00395 g002
Animals 15 00395 g003
Figure 3. Photomicrographs of the sclerotised structures of the genitals and haptor of (a,b) Quadriacanthus amakaliae ex Clarias stappersii from Kafubu River, (c,d) Quadriacanthus domatanai ex Clarias ngamensis From Lubumbashi River, and (e,f) Quadriacanthus halajiani ex Clarias ngamensis from Kafubu River. Scale bar: 20 µm.
Figure 3. Photomicrographs of the sclerotised structures of the genitals and haptor of (a,b) Quadriacanthus amakaliae ex Clarias stappersii from Kafubu River, (c,d) Quadriacanthus domatanai ex Clarias ngamensis From Lubumbashi River, and (e,f) Quadriacanthus halajiani ex Clarias ngamensis from Kafubu River. Scale bar: 20 µm.
Animals 15 00395 g003
Table 1. The number of specimens per fish species per sampling site.
Table 1. The number of specimens per fish species per sampling site.
Fish SpeciesSampling Site
Lufira RiverLubumbashi RiverKafubu River
Clarias ngamensis635
C. stappersii101012
C. buthupogon-72
C. gariepinus-74
C. theodorae-118
Table 2. The monopisthocotylan parasite species recovered from Clarias ngamensis, Clarias stappersii, Clarias buthupogon and Clarias gariepinus from the Upper Congo Basin. The different localities are represented by the following abbreviations: Luf: Lufira River; Lub: Lubumbashi River; Kaf: Kafubu River.
Table 2. The monopisthocotylan parasite species recovered from Clarias ngamensis, Clarias stappersii, Clarias buthupogon and Clarias gariepinus from the Upper Congo Basin. The different localities are represented by the following abbreviations: Luf: Lufira River; Lub: Lubumbashi River; Kaf: Kafubu River.
Host SpeciesParasite SpeciesLocalityNo. of Examined HostsNo. of Infested HostsMean Intensity
C. ngamensisQuadriacanthus shigoleyae n. sp.Luf6217
Q. aegypticusLub311
Kaf511
Q. allobychowskiellaLub311
Kaf521.5
Q. domatanaiLub312
Kaf511
Q. halajianiKaf511
C. stappersiiQ. amakaliaeLuf1069.8
Kaf1262.8
Q. kalomboi n. sp.Kaf1211
Q. bassocki n. sp.Kaf1212
C. buthupogonQ. amakaliaeLub723
Kaf211
Q. bassocki n. sp.Lub728
Kaf2111
C. gariepinusQ. bassocki n. sp.Lub716
Q. bassocki n. sp.Kaf421
Table 3. Obtained measurements (in micrometers) of Quadriacanthus species. Legend: MCO: male copulatory organ length; AP: accessory piece length; I–VII: hook length; DB: dorsal bar: (x) length, (w) width, (h) median process length, (ct) centre length; DA: dorsal anchor: (a) length, (ab) base diameter or width, (e) point length; DCn: dorsal cuneus length; VB: ventral bar: (x) length, (w) width; VA: ventral anchor: (a) length, (ab) base diameter, (e) point length; VCn: ventral cuneus length. Number of flattened specimens on which measurements of sclerotised pieces were taken: (n).
Table 3. Obtained measurements (in micrometers) of Quadriacanthus species. Legend: MCO: male copulatory organ length; AP: accessory piece length; I–VII: hook length; DB: dorsal bar: (x) length, (w) width, (h) median process length, (ct) centre length; DA: dorsal anchor: (a) length, (ab) base diameter or width, (e) point length; DCn: dorsal cuneus length; VB: ventral bar: (x) length, (w) width; VA: ventral anchor: (a) length, (ab) base diameter, (e) point length; VCn: ventral cuneus length. Number of flattened specimens on which measurements of sclerotised pieces were taken: (n).
Quadriacanthus kalomboi n. sp.
(n = 1)		Q. bassocki n. sp.
(n = 10)		Q. shigoleyae n. sp.
(n = 7)
MCO24.1624.8 (16–29.8)45.3 (38.6–50.7)
AP24.1424.1 (18.9–27.6)48.3 (43.5–51.3)
I15.4412 (10.7–12.8)15.4 (14.5–16.3)
II11.411.3 (7.7–12.1)12.1 (10.8–13.4)
III14.4212.7 (11.5–13.5)13.9 (12.4–15.1)
IV30.5620.4 (19.6–21.3)24.2 (21.8–26.9)
V13.412.8 (12–13.5)13.7 (13.3–14.1)
VI13.4412.9 (12.3–13.8)13 (12.2–13.3)
VII12.912.7 (11.8–13)12.9 (12.4–13.1)
DBx32.2625.7 (22.7–27.6)41.8 (39.9–43.4)
DBw14.988.3 (7.5–9.7)13.6 (11.3–15.2)
DBh13.0625.1 (23.2–27.2)44.3 (41.5–47.6)
DBct24.1218.4 (16.8–21.2)34.8 (30.7–38.5)
DAa40.0332.2 (23.5–35.4)36.3 (34.8–38)
DAab13.0810.3 (9.9–10.8)16.6 (16–17.1)
DAe4.844.9 (3.8–13.6)4.6 (3.7–5.3)
DCn13.6311.7 (10.8–13.6)17.2 (15.9–18.3)
VBx46.6538.7 (35.5–41.3)58.1 (40.4–63.1)
VBw10.334.4 (4.1–6.3)11.4 (10.3–12.4)
VAa26.7523.9 (23.3–24.8)31.8 (30.9–32.5)
VAab6.786.8 (6.2–7.3)12 (10.2–13)
VAe12.7716.2 (15.5–17.2)27.9 (27.2–28.8)
VCn6.765.6 (5.3–6)12 (10.8–14)
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Kasembele, G.K.; Vanhove, M.P.M.; Mushagalusa Mulega, A.; Chocha Manda, A.; Jorissen, M.W.P.; Luus-Powell, W.J.; Smit, W.J.; Bilong Bilong, C.F.; Bahanak, D.-n.-d. New Records and Descriptions of Three New Species of Quadriacanthus (Monopisthocotyla: Dactylogyridae) from Catfishes (Teleostei: Siluriformes, Clariidae) in the Upper Congo Basin. Animals 2025, 15, 395. https://doi.org/10.3390/ani15030395

AMA Style

Kasembele GK, Vanhove MPM, Mushagalusa Mulega A, Chocha Manda A, Jorissen MWP, Luus-Powell WJ, Smit WJ, Bilong Bilong CF, Bahanak D-n-d. New Records and Descriptions of Three New Species of Quadriacanthus (Monopisthocotyla: Dactylogyridae) from Catfishes (Teleostei: Siluriformes, Clariidae) in the Upper Congo Basin. Animals. 2025; 15(3):395. https://doi.org/10.3390/ani15030395

Chicago/Turabian Style

Kasembele, Gyrhaiss K., Maarten P. M. Vanhove, Archimède Mushagalusa Mulega, Auguste Chocha Manda, Michiel W. P. Jorissen, Wilmien J. Luus-Powell, Willem J. Smit, Charles F. Bilong Bilong, and Dieu-ne-dort Bahanak. 2025. "New Records and Descriptions of Three New Species of Quadriacanthus (Monopisthocotyla: Dactylogyridae) from Catfishes (Teleostei: Siluriformes, Clariidae) in the Upper Congo Basin" Animals 15, no. 3: 395. https://doi.org/10.3390/ani15030395

APA Style

Kasembele, G. K., Vanhove, M. P. M., Mushagalusa Mulega, A., Chocha Manda, A., Jorissen, M. W. P., Luus-Powell, W. J., Smit, W. J., Bilong Bilong, C. F., & Bahanak, D.-n.-d. (2025). New Records and Descriptions of Three New Species of Quadriacanthus (Monopisthocotyla: Dactylogyridae) from Catfishes (Teleostei: Siluriformes, Clariidae) in the Upper Congo Basin. Animals, 15(3), 395. https://doi.org/10.3390/ani15030395

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