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Monogeneans from Catfishes in Lake Tanganyika. I: Two new species of Bagrobdella (Dactylogyridae) from Auchenoglanis occidentalis (Siluriformes: Claroteidae)

ABSTRACT

In the framework of the study of Siluriform fish monogeneans of Lake Tanganyika, we described two new species of Bagrobdella Paperna, 1969 from Auchenoglanis occidentalis (Valenciennes, 1840). Bagrobdella vanhovei sp. nov. is characterized by the morphology of its MCO which is unique among its congeners, presenting a non-terminal opening, whereas the other species have a terminal opening, and Bagrobdella vansteenbergei sp. nov. characterized by the size of its hooks, which are almost all of the same size, and its male copulating organ with a unique shape: a sub-terminal opening and no membrane surrounding. The Multivariate analysis done on morphometrical characters shows that the new and already described species are well individualized, except for Bagrobdella parauchenoglanii Akoumba, Pariselle, Tombi & Bilong Bilong, 2017 and Bagrobdella fraudulenta Euzet & Le Brun, 1990 (but these two species are easily distinguishable by their morphology), and that B. vanhovei sp. nov. has a great intra-specific morphometrical variation.

KEY WORDS:
Bagrobdella vanhovei sp. nov.; Bagrobdella vansteenbergei sp. nov.; Congo Basin; East Africa; intraspecific variation; over dispersion.

INTRODUCTION

Lake Tanganyika is the oldest of the East African Great Lakes (Cohen et al. 1993Cohen AS, Bills R, Cocquyt CZ, Caljon AG (1993) The impact of sediment pollution on biodiversity in Lake Tanganyika. Conservation Biology 7(3): 667-677. https://doi.org/10.1046/j.1523-1739.1993.07030667.x
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). Its 3.200 km2 of surface area is unevenly distributed among four countries, including the Democratic Republic of the Congo in the West (14.800 km2 or 45%), Tanzania in the East (13.500 km2 or 41%), Burundi in the North (2600 km2 or 8%) and Zambia in the South (200 km2 or 6%) (Cohen et al. 1993Cohen AS, Bills R, Cocquyt CZ, Caljon AG (1993) The impact of sediment pollution on biodiversity in Lake Tanganyika. Conservation Biology 7(3): 667-677. https://doi.org/10.1046/j.1523-1739.1993.07030667.x
https://doi.org/10.1046/j.1523-1739.1993...
, Fermon 2007Fermon Y (2007) Étude de l’état des lieux de la partie nord du lac Tanganyika dans le cadre du Programme Pêche d’Action Contre la Faim en République Démocratique du Congo. Action Against Hunger, USA, report, 88 pp.) (Fig. 1).

Figure 1
Sampling sites localities.

It stands out from the rest of the world’s lakes by its richly diverse ichthyofauna, which makes it an important hotspot for the world’s freshwater lacustrine biodiversity (Coulter et al. 1986Coulter GW, Allanson BR, Bruton MN, Greenwood PH, Hart RC, Jackson PBN, Ribbink AJ (1986) Unique qualities and special problems of the African Great Lakes. Environmental Biology of Fishes 17(3): 161-183. https://doi.org/10.1007/BF00002094
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) and a ‘natural laboratory’ for evolutionary biologists (Martens 1997Martens K (1997) Speciation in ancient lakes. Trends in Ecology and Evolution 12(5): 177-182. https://doi.org/10.1016/S0169-5347(97)01039-2
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, Langenberg et al. 2003Langenberg VT, Nyamushahu S, Roijackers R, Koelmans AA (2003) External nutrient sources for Lake Tanganyika. Journal of Great Lakes Research 29(Suppl. 2): 169-180. https://doi.org/10.1016/S0380-1330(03)70546-2
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, Albrecht & Wilke 2008Albrecht C, Wilke T (2008) Ancient Lake Ohrid: Biodiversity and evolution. Hydrobiologia 615(1): 103-140. https://doi.org/10.1007/s10750-008-9558-y
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, Cristescu et al. 2010Cristescu ME, Adamowicz SJ, Vaillant JJ, Haffner DG (2010) Ancient lakes revisited: From the ecology to the genetics of speciation. Molecular Ecology 19(22): 4837-4851. https://doi.org/10.1111/j.1365-294X.2010.04832.x
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).

The cichlid fish of Lake Tanganyika have received particular attention, they are phenotypically, ecologically and genetically highly diverse (Nishida 1991Nishida M (1991) Lake Tanganyika as an evolutionary reservoir of old lineages of East African cichlid fishes: Inferences from allozyme data. Experientia 47(9): 974-979. https://doi.org/10.1007/BF01929896
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, Salzburger et al. 2002Salzburger W, Meyer A, Baric S, Verheyen E, Sturmbauer C (2002) Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunas. Systematic Biology 51(1): 113-135. https://doi.org/10.1080/106351502753475907
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, 2005Salzburger W, Mack T, Verheyen E, Meyer A (2005) Out of Tanganyika: Genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. BMC Evolutionary Biology 5(1983): 1-15. https://doi.org/10.1186/1471-2148-5-17
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). With 239 endemic species out of the 241 described (an endemism rate of 99%) (Ronco et al. 2020Ronco F, Büscher HH, Indermaur A, Salzburger W (2020) The taxonomic diversity of the cichlid fish fauna of ancient Lake Tanganyika, East Africa. Journal of Great Lakes Research 46(5): 1067-1078. https://doi.org/10.1016/j.jglr.2019.05.009
https://doi.org/10.1016/j.jglr.2019.05.0...
, 2021Ronco F, Matschiner M, Böhne A, Boila A, Büscher HH, El Taher A, Indermaur A, Malinsky M, Ricci V, Kahmen A, Jentoft S, Salzburger W (2021) Drivers and dynamics of a massive adaptive radiation in cichlid fishes. Nature 589(7840): 76-81. https://doi.org/10.1038/s41586-020-2930-4
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), Lake Tanganyika show the highest degree of endemism compared to other great lakes in Africa and the Americas (Salzburger et al. 2014Salzburger W, Bocxlaer BV, Cohen AS (2014) Ecology and evolution of the African great lakes and their faunas. Annual Review of Ecology, Evolution, and Systematics 45: 519-545. https://doi.org/10.1146/annurev-ecolsys-120213-091804
https://doi.org/10.1146/annurev-ecolsys-...
). In addition to calling its importance to the study of biodiversity, the Cichlids of Lake Tanganyika have also attracted the attention of parasitologists, primarily in host biogeography, systematics and parasite evolution (e.g., Bates 1997Bates JW (1997) The Slide-Sealing Compound “Glyceel”. Journal of Nematology 29(4): 565-566., Grégoir et al. 2015Grégoir AF, Hablützel PI, Vanhove MPM, Pariselle A, Bamps J, Volckaert FAM, Raeymaekers JAM (2015) A link between host dispersal and parasite diversity in two sympatric cichlids of Lake Tanganyika. Freshwater Biology 60(2): 323-335. https://doi.org/10.1111/fwb.12492
https://doi.org/10.1111/fwb.12492...
, Pariselle et al. 2011Pariselle A, Boeger WA, Snoeks J, Bilong Bilong CF, Morand S, Vanhove MPM (2011) The monogenean parasite fauna of cichlids: a potential tool for host biogeography. International Journal of Evolutionary Biology 2011: 471480. https://doi.org/10.4061/2011/471480
https://doi.org/10.4061/2011/471480...
, 2015Pariselle A, Van Steenberge M, Snoeks J, Volckaert FAM, Huyse T, Vanhove MPM (2015) Ancyrocephalidae (Monogenea) of lake tanganyika: Does the Cichlidogyrus parasite fauna of Interochromis loocki (Teleostei, Cichlidae) reflect its host’s phylogenetic affinities? Contributions to Zoology 84(1): 25-38. https://doi.org/10.1163/18759866-08401003
https://doi.org/10.1163/18759866-0840100...
, Raeymaekers et al. 2013Raeymaekers JAM, Hablützel PI, Grégoir AF, Bamps J, Roose AK, Vanhove MPM, Van Steenberge M, Pariselle A, Huyse T, Snoeks J (2013) Contrasting parasite communities among allopatric colour morphs of the Lake Tanganyika cichlid Tropheus. BMC Evolutionary Biology 13: 41. https://doi.org/10.1186/1471-2148-13-41
https://doi.org/10.1186/1471-2148-13-41...
, Van Steenberge et al. 2015Van Steenberge M, Pariselle A, Huyse T, Volckaert FAM, Snoeks J, Vanhove MPM (2015) Morphology, molecules, and monogenean parasites: An example of an integrative approach to cichlid biodiversity. Plos One 10(4): e0124474. https://doi.org/10.1371/journal.pone.0124474
https://doi.org/10.1371/journal.pone.012...
, Vanhove et al. 2013Vanhove MPM, Van Steenberge M, Dessein S, Volckaert FAM, Snoeks J, Huyse T, Pariselle A (2013) Biogeographical implications of Zambezian Cichlidogyrus species (Platyhelminthes: Monogenea: Ancyrocephalidae) parasitizing Congolian cichlids. Zootaxa 3608(5): 398-400. https://doi.org/10.11646/zootaxa.3608.5.8
https://doi.org/10.11646/zootaxa.3608.5....
, 2015Vanhove MPM, Pariselle A, Van Steenberge M, Raeymaekers JAM, Hablützel PI, Gillardin C, Hellemans B, Breman FC, Koblmüller S, Sturmbauer C, Snoeks J, Volckaert FAM, Huyse T (2015) Hidden biodiversity in an ancient lake: Phylogenetic congruence between Lake Tanganyika tropheine cichlids and their monogenean flatworm parasites. Scientific Reports 5: 13669. https://doi.org/10.1038/srep13669
https://doi.org/10.1038/srep13669...
, 2016Vanhove MPM, Hablützel PI, Pariselle A, Šimková A, Huyse T, Raeymaekers JAM (2016) Cichlids: A host of opportunities for evolutionary parasitology. Trends in Parasitology 32(10): 820-832. https://doi.org/10.1016/j.pt.2016.07.002
https://doi.org/10.1016/j.pt.2016.07.002...
).

The non-cichlids of Lake Tanganyika, less diversified than the Cichlidae, have attracted very little attention of scientists. However, they are represented by 75 species belonging to 11 families, and have a rate of endemicity of 59%. Species of some of these families, such as Clupeidae and Latidae, have already been the subject of some ecological (Coulter et al. 1986Coulter GW, Allanson BR, Bruton MN, Greenwood PH, Hart RC, Jackson PBN, Ribbink AJ (1986) Unique qualities and special problems of the African Great Lakes. Environmental Biology of Fishes 17(3): 161-183. https://doi.org/10.1007/BF00002094
https://doi.org/10.1007/BF00002094...
), parasitological (Kmentová et al. 2018Kmentová N, Van Steenberge M, Raeymaekers JAM, Koblmüller S, Hablützel PI, Muterezi Bukinga F, Mulimbwa N’sibula T, Masilya MP, Nzigidahera B, Ntakimazi G, Gelnar M, Vanhove MPM (2018) Monogenean parasites of sardines in Lake Tanganyika: Diversity, origin and intraspecific variability. Contributions to Zoology 87(2): 105-132. https://doi.org/10.1163/18759866-08702004
https://doi.org/10.1163/18759866-0870200...
, 2020Kmentová N, Koblmüller S, Van Steenberge M, Raeymaekers JAM, Artois T, De Keyzer ELR, Milec L, Muterezi-Bukinga F, Mulimbwa N’sibula T, Masilya Mulungula P, Ntakimazi G, Volckaert FAM, Gelnar M, Vanhove MPM (2020) Weak population structure and recent demographic expansion of the monogenean parasite Kapentagyrus spp. infecting clupeid fishes of Lake Tanganyika, East Africa. International Journal for Parasitology 50(6-7): 471-486. https://doi.org/10.1016/j.ijpara.2020.02.002
https://doi.org/10.1016/j.ijpara.2020.02...
) and genomic (De Keyzer et al. 2019De Keyzer ELR, De Corte Z, Van Steenberge M, Raeymaekers JAM, Calboli FCF, Kmentová N, N’Sibula Mulimbwa T, Virgili M, Vangestel C, Masilya MP, Volckaert FAM, Vanhove MPM (2019) First genomic study on Lake Tanganyika sprat Stolothrissa tanganicae: A lack of population structure calls for integrated management of this important fisheries target species. BMC Evolutionary Biology 19(1): 1-15. https://doi.org/10.1186/s12862-018-1325-8
https://doi.org/10.1186/s12862-018-1325-...
) studies. Siluriformes represent five (Bagridae, Claroteidae, Clariidae, Mochokidae, and Malapteruridae) of these 11 families, making Lake Tanganyika the most diverse lake in Siluriformes than any other lake in the world (Fermon 2007Fermon Y (2007) Étude de l’état des lieux de la partie nord du lac Tanganyika dans le cadre du Programme Pêche d’Action Contre la Faim en République Démocratique du Congo. Action Against Hunger, USA, report, 88 pp., Peart et al. 2014Peart CR, Bills R, Wilkinson M, Day JJ (2014) Nocturnal claroteine catfishes reveal dual colonisation but a single radiation in Lake Tanganyika. Molecular Phylogenetics and Evolution 73(1): 119-128. https://doi.org/10.1016/j.ympev.2014.01.013
https://doi.org/10.1016/j.ympev.2014.01....
). However, nothing is known about the parasites of these hosts.

The history of the Lake Tanganyika parasitic fauna began with the description of Ancyrocephalus limnothrissae Paperna, 1973 from the gills of Limnothrissa miodon (Boulenger, 1906). This species was redescribed under the name Kapentagyrus limnothrissae by Kmentová et al. (2018Kmentová N, Van Steenberge M, Raeymaekers JAM, Koblmüller S, Hablützel PI, Muterezi Bukinga F, Mulimbwa N’sibula T, Masilya MP, Nzigidahera B, Ntakimazi G, Gelnar M, Vanhove MPM (2018) Monogenean parasites of sardines in Lake Tanganyika: Diversity, origin and intraspecific variability. Contributions to Zoology 87(2): 105-132. https://doi.org/10.1163/18759866-08702004
https://doi.org/10.1163/18759866-0870200...
). The second description of Lake Tanganyika’s monogenean species was Gyrodactylus sturmbaueri Vanhove et al., 2011, G. thysi Vanhove et al., 2011 and G. zimbae Vanhove et al., 2011 by Vanhove et al. (2011Vanhove MPM, Volckaert FAM, Pariselle A (2011) Ancyrocephalidae (Monogenea) of lake tanganyika: I: Four new species of Cichlidogyrus from Ophthalmotilapia ventralis (Teleostei: Cichlidae), the first record of this parasite family in the basin. Zoologia (Curitiba) 28(2): 253-263. https://doi.org/10.1590/S1984-46702011000200016
https://doi.org/10.1590/S1984-4670201100...
). Since then, the number of studies in Lake Tanganyika has increased, with particular attention given to Cichlidogyrus Paperna, 1960 monogenean of Cichlid fish, which currently has 39 published species (Rahmouni et al. 2017Rahmouni C, Vanhove MPM, Šimková A (2017) Underexplored diversity of gill monogeneans in cichlids from Lake Tanganyika: eight new species of Cichlidogyrus Paperna, 1960 (Monogenea : Dactylogyridae) from the northern basin of the lake, with remarks on the vagina and the heel of the male copulatory organ. Parasites & Vectors 10: 591. https://doi.org/10.1186/s13071-017-2460-6
https://doi.org/10.1186/s13071-017-2460-...
, 2018Rahmouni C, Vanhove MPM, Šimková A (2018) Seven new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) parasitizing the gills of Congolese cichlids from northern Lake Tanganyika. PeerJ 6: e5604. https://doi.org/10.7717/peerj.5604
https://doi.org/10.7717/peerj.5604...
, Rahmouni 2021Rahmouni C (2021) Species diversity and phylogenetic relationships among gill-specific monogenean parasites (Platy helminthes : Dactylogyridae) of cichlids (Cichlidae) from Lake Tanganyika. PhD Thesis, Masaryk University, Brno, Czech Republic.).

This is the first study that describes Bagrobdella species in Lake Tanganyika. To date, four species are described from Ghana, Uganda, Mali and Cameroon: Bagrobdella auchenoglanii Paperna, 1969, B. fraudulenta Euzet & Le Brun, 1990 and B. anthopenis Euzet & Le Brun, 1990 (Euzet and Le Brun 1990Euzet L, Le Brun N (1990) Monogènes du genre Bagrobdella Paperna, 1969 parasites branchiaux d’Auchenoglanis occidentalis Cuvier et Valenciennes, 1840) (Teleostei, Siluriformes, Bagridae). Journal of African Zoology 104: 37-48.) from Auchenoglanis occidentalis (Valenciennes, 1840), and B. parauchenoglanii Akoumba, Pariselle, Tombi & Bilong Bilong, 2017 from Parauchenoglanis monkei (Keilhack, 1910) (Akoumba et al. 2017Akoumba JF, Pariselle A, Tombi J, Bilong Bilong CF (2017) Description of two new ancyrocephalid (Quadriacanthus and Bagrobdella) monogenea from the gills of auchenoglanid catfishes (Pisces, Siluriformes, Claroteidae) in Cameroon. Vie et Milieu, Life and Environment 67(2): 59-64.).

MATERIAL AND METHODS

Sampling

The parasites described in this study were collected from 11 specimens of A. occidentalis. Fish were captured in the North-Western part of the lake, a few meters from the orthodox church in Uvira (North of this part) and at the Mouth of River Mutambala (South of this part) (Fig. 1). The hosts were euthanized by severing their chordal spines, and identified on site as A. occidentalis using the Fermon et al. (2012Fermon Y, Nshombo Muderhwa V, Muzumani Risasi D, Jonas B (2012) Lac Tanganyika Guide de la faune des poissons de la côte congolaise, d’Ubwari à la Ruzizi. Amira, 238 pp.) keys. The gills and a small section of the pectoral fins were stored in 96% ethanol.

Fish DNA isolation was carried out according to the protocol of Aljanabi and Martinez (1997Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high-quality genomic DNA for PCR-based techniques. Nucleic Acids Research 25: 4692-4693. https://doi.org/10.1093/nar/25.22.4692
https://doi.org/10.1093/nar/25.22.4692...
). Vouchers were kept in the collection of CRH-Uvira (DRC).

The gills were examined under a Wild Heerbrugg® M8 binocular. The monogeneans were recovered using an entomologist needle and some individuals were mounted in a drop of Hoyer’s medium (Anderson 1954Anderson LE (1954) Hoyer’s solution as a rapid permanent mounting medium for bryophytes. The Bryologist 57(3): 242-244. https://doi.org/10.2307/3240091
https://doi.org/10.2307/3240091...
) on a slide, then covered with a coverslip to flatten the specimens and highlight the sclerotized structures. The slides were left for 24 hours in horizontal position before sealing the coverslip with Glyceel (Bates 1997Bates JW (1997) The Slide-Sealing Compound “Glyceel”. Journal of Nematology 29(4): 565-566.). Other individuals were mounted using tap water and identified under a Leica® DM 2500 microscope equipped with a digital camera (Leica DMC 4500).

Morphometric analysis

Measurements were based on Euzet and Le Brun (1990Euzet L, Le Brun N (1990) Monogènes du genre Bagrobdella Paperna, 1969 parasites branchiaux d’Auchenoglanis occidentalis Cuvier et Valenciennes, 1840) (Teleostei, Siluriformes, Bagridae). Journal of African Zoology 104: 37-48.), and taken using LAS version 4.12.0 (Figs 2-7), and given in µm by the range in parentheses, and number of individuals. Drawings of the sclerotized parts of the Monogeneans were made with Corel Draw® 2019 software using pictures taken from the camera. All analyses were performed using R 4.1.2 software (R Core Team 2022R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
http://www.R-project.org...
).

Figures 2-7
Measurement scheme of the sclerotized structures of Bagrobdella spp.: (2) anchor, a: total length; b: blade length; c: shaft length; d: guard length; e: point length. (3) Dorsal bar, x: horizontal length; y: vertical length; w: width. (4) Ventral bar, x: horizontal length; cx: length of median projection; cy: width of median projection; BL: length of outgrowth; Bl: width of outgrowth. (5) Trapezoidal piece, L: length; l: width. (6) Male copulatory complex, Pe: length of penis, AL: length of bulb; Al: width of bulb. (7) Length of hook.

Data from 45 individuals of one new species, 10 individuals of the other, and 10 individuals of B. parauchenoglanii, were subjected to a Principal Component Analysis (PCA). This analysis was done using the FactoMineR (Husson et al. 2020Husson F, Josse J, Le S, Maze J (2020) FactoMiner: Multivariate exploratory data analysis and data mining. R package version 2.6.) and factoextra (Kassambara and Mundt 2020Kassambara A, Mundt F (2020) Factoextra: extract and visualize the results of multivariate data analyses. R package version 1.0.7.) packages in R. Bagrobdella auchenoglanii, B. fraudulenta and B. anthopenis, each one represented by the mean values of the analyzed parameters obtained in Euzet and Le Brun (1990Euzet L, Le Brun N (1990) Monogènes du genre Bagrobdella Paperna, 1969 parasites branchiaux d’Auchenoglanis occidentalis Cuvier et Valenciennes, 1840) (Teleostei, Siluriformes, Bagridae). Journal of African Zoology 104: 37-48.) were added to the analysis as supplementary individuals.

To comply with the regulations set out in article 8.5 of the amended 2012 version of the International Code of Zoological Nomenclature (ICZN), details of the new species were submitted to ZooBank. For each new species, the Life Science Identifier (LSID) is reported in the taxonomic summary.

Types were deposited in the Helminth collections of the Royal Museum for Central Africa (MRAC, Tervuren, Belgium), of the Muséum national d’Histoire naturelle (MnHn, Paris, France) and of the Iziko South African Museum, Cape Town, Republic of South Africa (SAMC)

RESULTS

The identification of host species was confirmed by the molecular analysis, and the sequences were deposited in Genbank (Identification number ON682514). Gills of eleven A. occidentalis specimens were examined for parasite infection. Seven out of eleven hosts were found be parasitized. The most parasitized fish host is the sole specimen caught at the Mouth of Mutambala River. This individual hosted a total of 286 Monogeneans, 269 Bagrobdella vanhovei sp. nov. and 17 B. vansteenbergei. sp. nov. The other ten individuals that were captured off the Orthodox Church of Uvira possessed only Bagrobdella vanhovei sp. nov. individuals. Among them, four had no monogeneans, three had one individual, and the other three hosts had, five, six and 35 individuals respectively.

The two new species of Bagrobdella which were found are described herein.

TAXONOMY

Bagrobdella vanhovei Mushagalusa Mulega & Pariselle, sp. nov.

Fig. 8

https://zoobank.org/A7869408-CD17-4AB3-BFDC-9362C5DA9F13

Type-host. Auchenoglanis occidentalis (Valenciennes, 1840).

Site of infection. Gills.

Type locality. Mouth of Mutambala River (29°04.4042’E, 04°16.4598’S) and off the Orthodox church of Uvira (29°08’32.6”E, 03°23’42.0”S) (DRC) (Fig. 1).

Studied material. 78 specimens mounted in Hoyer’s medium.

Number of hosts examined. 11.

Prevalence. 6/11 = 54%.

Mean intensity. 318/6 = 53.

Abundance. 318/11 = 28.9.

Figure 8
Bagrobdella vanhovei sp. nov. haptoral structure and MCO. Scale bar: 20 µm.

Deposited material. Holotype deposited at the Royal Museum for Central Africa, Tervuren, Belgium (RMCA_VERMES_43660), paratypes deposited at the MRAC (number RMCA_VERMES_43661), the MnHn, Paris, France (MNHN HEL1824) and the Iziko South African Museum, Cape Town, Republic of South Africa (SAMC) (SAMC-A094638).

Description. Length 681 (522-965; 72); greatest width 200 (140-273; 72); pharynx 71 (49-97; 61); Dorsal anchor: a = 82 (65-94; 78), b = 66 (53-76; 78), c = 9 (3-17; 78), d = 21 (13-30; 78), e = 19 (13-22; 78), no visible filaments. Dorsal bar x = 87 (62-112; 72), w = 15 (9-23; 71), median projection posteriorly oriented: Y = 59 (33-82; 61). Ventral anchor slightly drilled at the blade beginning: a = 65 (38-74; 78), b = 71 (60-79; 78), c = 11 (5-16; 78), d = 18 (13-24; 78), e = 6 (3-9, 77), no visible filaments. Ventral bar x = 112 (76-146; 75), w = 16 (9-27; 74) extends in the form of an outgrowth, BL = 11 (5-20; 60), Bl = 6 (3-13; 60), median projection posteriorly orientated, cross-shaped, Cx = 72 (58-91; 77), Cy = 20 (14-29, 76). At median projection posterior extremity is attached another sclerotized piece trapeze-shaped. Fourteen hooks arranged in seven symmetrical pairs of different sizes: I (medio-ventral) the largest and longest: 52 (34-64; 77), II (medio-ventral) the smallest hooks: 17 (13-20; 69), III and IV (latero-dorsal and almost identical in size): 39 (27-48; 74) V to VII (latero-ventral and almost identical in size) 25 (17-35; 72). A medium-ventral trapezoidal plate, slightly sclerotized, is located between hooks I, L: 37 (28-50; 15), l: 28 (22-35; 16). Male copulatory organ (MCO): 61 (51-67; 71) with a well-developed basal bulb: AL = 15 (10-22; 41), Al = 10 (3-20; 41), followed by a thick-walled tube of constant diameter, folded at 30° at the middle, distal half surrounded by a membrane; at the distal extremity of the tube (level of opening) a portion of the wall formed a triangular part tapering at its end, length a quarter of that of the tube. Lidded eggs 93 (83-110; 12) are ovoid, at the pole opposite to the operculum is a filament finished by a small disc, exactly as described by Euzet and Le Brun (1990Euzet L, Le Brun N (1990) Monogènes du genre Bagrobdella Paperna, 1969 parasites branchiaux d’Auchenoglanis occidentalis Cuvier et Valenciennes, 1840) (Teleostei, Siluriformes, Bagridae). Journal of African Zoology 104: 37-48.) in the diagnose of Bagrobdella.

Etymology. The species is named after Professor Dr. Maarten P.M. Vanhove (University of Hasselt, Belgium), who is a specialist in monogeneans of cichlids from Lake Tanganyika.

Note. The authors of the new taxa are different from the authors of this paper: Article 50.1 and Recommendation 50A of the International Code of Zoological Nomenclature.

Remarks. The new species was placed in Bagrobdella due to the presence of a haptor with dorsal, ventral anchor/bar complexes, 7 pairs of hooks with ancyrocephaline distribution, pairs 1, 3-7 with shanks comprised of 2 subunits, proximal subunit expended, pair 2 with shank of 1 subunit. Ventral bar straight, with long anterior projection associated with lightly sclerotized skirt, dorsal bar straight, with posterior shield-like projection, which are characteristics of the genus (Kritsky and Kulo 1999Kritsky DC, Kulo SD (1999) Revisions of Protoancylodiscoides and Bagrobdella, with redescriptions of P. chrysichthes and B. auchenoglanii (Monogenoidea: Dactylogyridae) from the gills of two bagrid catfishes (Siluriformes) in Togo, Africa. Comparative Parasitology 66(2): 138-145.). Bagrobdella vanhovei sp. nov. is similar to B. auchenoglanii, B. fraudulenta, B. parauchenoglanii and B. anthopenis by (1) having a trapezoidal-shaped (former visible in 15 of the 78 studied specimens) piece associated with the median projection of the ventral bar (Figs 9-14), (2) having seven pairs of hooks of different sizes. Its dorsal anchors have a long point, while its ventral anchors have a very short one, like in Bagrobdella auchenoglanii and B. fraudulenta (B. parauchenoglanii and B. anthopenis having points of the same size for both ventral and dorsal anchors). Bagrobdella vanhovei sp. nov is easily distinguished from all species already described by the morphology of its MCO which is unique, being not spirally coiled - when all other species have a coiled MCO, which was a genus character (Kritsky and Kulo 1999), and more, the MCO of B. vanhovei has a sub-terminal opening (at three quarter of the total length), when for all other species the opening is terminal (Figs 15-20).

Figures 9-14
Haptors of the six species belonging to Bagrobdella: (9) Bagrobdella vanhovei sp. nov.; (10) Bagrobdella vansteenbergei sp. nov.; (11) Bagrobdella auchenoglanii; (12) Bagrobdella fraudulenta; (13) Bagrobdella anthopenis; (14) Bagrobdella parauchenoglanii (Akoumba et al 2017Akoumba JF, Pariselle A, Tombi J, Bilong Bilong CF (2017) Description of two new ancyrocephalid (Quadriacanthus and Bagrobdella) monogenea from the gills of auchenoglanid catfishes (Pisces, Siluriformes, Claroteidae) in Cameroon. Vie et Milieu, Life and Environment 67(2): 59-64., Euzet and Le Brun 1990Euzet L, Le Brun N (1990) Monogènes du genre Bagrobdella Paperna, 1969 parasites branchiaux d’Auchenoglanis occidentalis Cuvier et Valenciennes, 1840) (Teleostei, Siluriformes, Bagridae). Journal of African Zoology 104: 37-48.). Scale bars: 20 µm.

Figures 15-20
MCO of the six species belonging to Bagrobdella: (15) Bagrobdella vanhovei sp. nov.; (16) Bagrobdella vansteenbergei sp. nov.; (17) Bagrobdella auchenoglanii; (18) Bagrobdella fraudulenta; (19) Bagrobdella anthopenis; (20) Bagrobdella parauchenoglanii (Akoumba et al. 2017Akoumba JF, Pariselle A, Tombi J, Bilong Bilong CF (2017) Description of two new ancyrocephalid (Quadriacanthus and Bagrobdella) monogenea from the gills of auchenoglanid catfishes (Pisces, Siluriformes, Claroteidae) in Cameroon. Vie et Milieu, Life and Environment 67(2): 59-64., Euzet and Le Brun 1990Euzet L, Le Brun N (1990) Monogènes du genre Bagrobdella Paperna, 1969 parasites branchiaux d’Auchenoglanis occidentalis Cuvier et Valenciennes, 1840) (Teleostei, Siluriformes, Bagridae). Journal of African Zoology 104: 37-48.). Scale bar: 20 µm.

Bagrobdella vanhovei sp. nov has two small hard parts that have never been reported before in the description of Bagrobdella species. These are: 1) a structure in the shape of a button between the bar and ventral anchors (Fig. 26), 2) a semi-circular structure toping the extremity of the ventral bar median projection (Fig. 25).

Figures 21-26
(21) Bagrobdella vanhovei sp. nov. microphotograph in toto; (22) Bagrobdella vansteenbergei sp. nov. microphotograph in toto; (23) Microphotograph of the trapezoidal plate in the haptor of Bagrobdella vanhovei; (24) Button like structure; (25) Semi-circular structure; (26) Egg (B. vanhovei sp. nov). Scale bars: 21 = 100 µm, 22 = 200 µm, 23, 24, 26 = 20 µm, 25 = 50 µm.

Bagrobdella vansteenbergei Mushagalusa Mulega & Pariselle, sp. nov.

Fig. 27

https://zoobank.org/47A4EA89-ED69-4878-BFD7-A3F8FC11CA6E

Type-host. Auchenoglanis occidentalis (Valenciennes, 1840).

Site of infection. gills.

Type locality. Mouth of Mutambala River (DRC) 29°04.4042’E, 04°16.4598’S.

Studied materiel. 15 specimens mounted in Hoyer’s medium.

Number of hosts examined. 11.

Prevalence. 1/11 = 9%.

Mean intensity. 17/1 = 17.

Abundance. 17/11 = 1.5.

Figure 27
Bagrobdella vansteenbergei sp. nov., haptoral structure and MCO. Scale bar: 20 µm.

Type-material. Holotype deposited at the Royal Museum for Central Africa, Tervuren, Belgium (RMCA_VERMES_43658), paratypes deposited at the MRAC (number RMCA_VERMES_43659), the MnHn, Paris, France (MNHN HEL1825) and the Iziko South African Museum, Cape Town, Republic of South Africa (SAMC) (SAMC-A094636 and SAMC-A094637).

Description. The anatomy is that of Bagrobdella. Total length 621 (543-749, 12), greatest width 182 (113-262; 13); pharynx 64 (42-79; 10). Dorsal anchor a = 71 (67-77; 13), b = 64 (59-70; 13), c = 1 (0-5; 13), d = 10 (7-13; 13), e = 23 (21-26; 13). Dorsal bar x = 88 (77-100; 10), w = 14 (10-18; 10), median projection posteriorly oriented: Y = 55 (51-70; 6). Ventral anchor slightly drilled at the blade proximal extremity: a = 63 (61-67; 13), b = 62 (60-64; 12), c = 6 (4-8; 12), d = 12 (9-17; 12), e = 26 (22-28; 13). Ventral bar: 92 (78-103; 10), w = 14 (11-18; 8), extends in the form of an outgrowth: BL = 7 (5-11; 7), Bl = 5 (5-6; 8). This bar has a median projection posteriorly cross-chapped cx = 77 (69-85; 12), cy = 25 (21-31; 12), absence of sclerotized trapeze-shaped. Hook pairs of similar size: I = 26 (23-31; 11), II = 17 (14-19; 10), III and IV = 22 (19-27; 10), and V up to VII = 19 (18-22; 12). MCO 66 (58-71; 11), asymmetrical bulb AL = 16 (11-20; 9), Al = 9 (5-12; 9), is a curved tube with thick wall and constant diameter; a part of the wall extend the penis extremity of about 25%.

Etymology. The species is named after Dr. Maarten Van Steenberge, a researcher at Royal Belgian Institute of Natural Sciences, who is a specialist in African freshwater fish.

Note: The authors of the new taxa are different from the authors of this paper: Article 50.1 and Recommendation 50A of the International Code of Zoological Nomenclature.

Remarks. The new species was placed in Bagrobdella due to the presence of haptor with dorsal, ventral anchor/bar complexes, 7 pairs of hooks, pairs 1, 3-7 with shanks comprised of 2 subunits, proximal subunit expended, pair 2 with shank of 1 subunit. Ventral bar straight, with long anterior projection, dorsal bar straight, with posterior shield-like projection, which are characteristics of the genus (Kritsky and Kulo 1999Kritsky DC, Kulo SD (1999) Revisions of Protoancylodiscoides and Bagrobdella, with redescriptions of P. chrysichthes and B. auchenoglanii (Monogenoidea: Dactylogyridae) from the gills of two bagrid catfishes (Siluriformes) in Togo, Africa. Comparative Parasitology 66(2): 138-145.). Bagrobdella vansteenbergei sp. nov. differs from all other species already described by the size of its hooks, which are all of almost the same length (pair I being only slightly longer than the others), whereas they are of different size in all the previously described species (including B. vanhovei sp. nov.) (Figs 9-14). Moreover, the trapezoidal piece was not observed in the 17 individuals (15 Hoyer’s mounted and 2 preserved in ethanol), and the ventral anchors are slightly holed. Its male copulating organ is unique and different from the MCO of B. auchenoglanii, B. fraudulenta, B. anthopenis and B. parauchenoglanii by a shape which is not spirally coiled. As B. vanhovei, the MCO of B. vansteenbergei has a sub-terminal opening at three quarter of the total length. As Bagrobdella vanhovei sp. nov, Bagrobdella vansteenbergei sp. nov, has two small hard parts that have never been reported before in the description of Bagrobdella species. These are: 1) a structure in the shape of a button between the bar and ventral anchors (Fig. 26), 2) a semi-circular structure toping the extremity of the ventral bar median projection (Fig. 25).

Multivariate analyses

Our dataset contained 68 individuals with 21 quantitative variables (Figs 2-7). Among the 68 individuals, three were considered as illustrative (B. auchenoglanii, B. fraudulenta and B. anthopenis). The first two dimensions of the PCA represent 71.8% of the total dataset inertia. Individuals are clustered into three groups which correspond to the three species included in the analysis (Bagrobdella vanhovei sp. nov., B. vansteenbergei sp. nov., and Bagrobdella pauchenoglanii). Only parameters contributing to more than 95 percent for group separation were displayed on the graph (Fig. 28). The dimension 1 opposes most individuals belonging to the group B. vanhovei sp. nov. (to the right of the graph, characterized by a positive coordinate on the axis) to individuals belonging to the groups B. vansteenbergi and B. parauchenoglanii (from Cameroon), to the left of the graph, characterized by a strongly negative coordinate on the axis).

The individuals belonging to the group B. vanhovei sp. nov. (characterized by a positive coordinate on the axis) are sharing:

1) high values for III_IV, DA_d, DB_w, I, VA_b, DA_a, VB_x, VA_a, VA_d and DA_b (variables are sorted from the strongest); 2) low values for VA_e and Pe (variables are sorted from the weakest).

The individuals belonging to B. parauchenoglanii (characterized by a negative coordinate on the axis) are sharing: 1) high values for the variables Pe, VA_c, DA_c and VB_w (variables are sorted from the strongest); 2) low values for the variables DA_b, DB_.x, VB_x, cx, VA_a, DA_a, VA_b, DA_e, III_IV and DA_d (variables are sorted from the weakest).

In the group of B. vansteenbergei sp. nov. (characterized by a negative coordinate on the axis) individuals share: 1) high values for the variables VA_e and DA_e (variables are sorted from the strongest); 2) low values for the variables V_à_VII, DA_c, VA_c, IDB_w, DA_d, DV_d, VB_w and III_IV (variables are sorted from the weakest).

The dimension 2 opposes individuals belonging to B. parauchenoglanii (to the top of the graph, characterized by a strongly positive coordinate on the axis) to individuals belonging to B. vansteenbergei sp. nov.

On the graph, B. auchenoglanii and B. anthopenis are isolated from the other species, while B. fraudulenta grouped with B. parauchenoglanii, even so these two latter species being easily distinguishable (at least by their penis morphology) (Figs 15-20).

DISCUSSION

The non-homogeneous distribution in populations of parasite observed in our fish samples is very common (Dold and Holland 2011Dold C, Holland CV (2011) Ascaris and ascariasis. Microbes and Infection 13(7): 632-637. https://doi.org/10.1016/j.micinf.2010.09.012
https://doi.org/10.1016/j.micinf.2010.09...
), for example it has been observed very recently in the Brachyplatystoma vaillantii Valenciennes, 1840 (Siluriformes, Pimelodidae) in the Amazon (Brito-Junior and Tavares-Dias 2021Brito-Junior IA, Tavares-dias M (2021) Diversity of ectoparasites and endoparasites infecting Brachyplatystoma vaillantii (Siluriformes: Pimelodidae), a large migratory catfish from the Amazon. Acta Amazonica 51(2): 122-128. https://doi.org/10.1590/1809-4392201901321
https://doi.org/10.1590/1809-43922019013...
). As mentioned by Tinsley et al. (2020Tinsley RC, Vineer HR, Grainger-Wood R, Morgan ER (2020) Heterogeneity in helminth infections: factors influencing aggregation in a simple host-parasite system. Parasitology 147: 65-77.) the factors responsible for the aggregated distribution of a monogenean species on fish are likely linked to the host factors alone, instead of the heterogeneity in host exposition to parasite infestation stages.

As there is sometimes a correlation between water quality and helminth infections - e.g., in the Cyprinid fish Zargar et al. (2012Zargar UR, Yousuf AR, Chishti MZ, Ahmed F, Bashir H, Ahmed F (2012) Effects of water quality and trophic status on helminth infections in the cyprinid fish, Schizothorax niger Heckel, 1838 from three lakes in the Kashmir Himalayas. Journal of Helminthology 86(1): 70-76. https://doi.org/10.1017/S0022149X11000071
https://doi.org/10.1017/S0022149X1100007...
), overdispersion of B. vanhovei sp. nov. and the absence of B. vansteenbergei sp. nov. in the other six host individuals captured off the Orthodox Church of Uvira could be due to different water qualities at the level of these two sampling sites. Thus, B. vansteenbergei sp. nov. could be adapted to the conditions found at the Mouth of Mutambala River, while B. vanhovei sp. nov. could be more resistant to variations of abiotic conditions.

Bagrobdella vanhovei sp. nov. and B. vansteenbergei sp. nov. are both new to science and endemic to Lake Tanganyika. However, the four species of Bagrobdella already known have been described in different localities: B. auchenoglanii in Ghana (with a redescription based on individuals sampled in Mali and Togo), B. anthopenis in Mali, B. fraudulenta in Uganda and Mali (see Euzet and Le Brun 1990Euzet L, Le Brun N (1990) Monogènes du genre Bagrobdella Paperna, 1969 parasites branchiaux d’Auchenoglanis occidentalis Cuvier et Valenciennes, 1840) (Teleostei, Siluriformes, Bagridae). Journal of African Zoology 104: 37-48.) and recently B. parauchenoglanii in Cameroon (Akoumba et al. 2017Akoumba JF, Pariselle A, Tombi J, Bilong Bilong CF (2017) Description of two new ancyrocephalid (Quadriacanthus and Bagrobdella) monogenea from the gills of auchenoglanid catfishes (Pisces, Siluriformes, Claroteidae) in Cameroon. Vie et Milieu, Life and Environment 67(2): 59-64.).

Except for individuals of A. occidentalis sampled by Euzet and Le Brun at Bamako (in Niger River), which harbor three species of Bagrobdella (B. auchenoglanii, B. fraudulenta and B. anthopenis), in other localities: Lake Albert, Uganda (Paperna 1971Paperna I (1971) Redescription of Bagrobdella auchenoglanii Paperna, 1969 (Monogenea, Dactylogyridae). Revue de Zoologie et de Botanique Africaine 83: 141-146.); Kara River, Togo (Kritsky and Kulo 1999Kritsky DC, Kulo SD (1999) Revisions of Protoancylodiscoides and Bagrobdella, with redescriptions of P. chrysichthes and B. auchenoglanii (Monogenoidea: Dactylogyridae) from the gills of two bagrid catfishes (Siluriformes) in Togo, Africa. Comparative Parasitology 66(2): 138-145.); Oti River (Euzet and Le Brun 1990Euzet L, Le Brun N (1990) Monogènes du genre Bagrobdella Paperna, 1969 parasites branchiaux d’Auchenoglanis occidentalis Cuvier et Valenciennes, 1840) (Teleostei, Siluriformes, Bagridae). Journal of African Zoology 104: 37-48.) and Volta Lake (Paperna 1969Paperna I (1969) Monogenetic Trematodes of the fish of the Volta basin and South Ghana. Bulletin de l‘lnstitut Francais d’Afrique Noire, Série A 31: 840-880.), Volta Basin; Sassandra in RCI (Euzet and Le Brun 1990Euzet L, Le Brun N (1990) Monogènes du genre Bagrobdella Paperna, 1969 parasites branchiaux d’Auchenoglanis occidentalis Cuvier et Valenciennes, 1840) (Teleostei, Siluriformes, Bagridae). Journal of African Zoology 104: 37-48.), and on P. monkei in Cameroon (Akoumba et al. 2017Akoumba JF, Pariselle A, Tombi J, Bilong Bilong CF (2017) Description of two new ancyrocephalid (Quadriacanthus and Bagrobdella) monogenea from the gills of auchenoglanid catfishes (Pisces, Siluriformes, Claroteidae) in Cameroon. Vie et Milieu, Life and Environment 67(2): 59-64.), it seems that only one species is present (B. fraudulenta in Uganda, B. parauchenoglanii in Cameroon, B. auchenoglanii in the other localities).

So, among the five Bagrobdella species described from A. occidentalis, three (B. auchenoglanii, B. fraudulenta and B. anthopenis) are found in the watershed of the Nilo-Sudanian province, when the two others new one (B. vanhovei and B. vansteenbergei) are from the Tanganyika province. As a consequence, either these monogenean species are specific of their ichtyofaunal provinces, or we are in the presence of two different host species (the systematic status of A. occidentalis remains under debate - see for example Geerinckx and Vreven (2013Geerinckx T, Vreven E (2013) A re-evaluation of the species-level diversity within the catfish genus Auchenoglanis (Siluriformes: Claroteidae). Journal of Natural History 47(47-48): 2979-3010. https://doi.org/10.1080/00222933.2013.802043
https://doi.org/10.1080/00222933.2013.80...
)).

Bagrobdella vanhovei sp. nov. shows a high variability in its morphometrical characters (Fig. 28), with small, medium and large measurements for similar hard parts and this causes individuals of this species to oppose on the two axes of the PCA. These differences, apart from a great variability of specimens from a single species, may likely be due to two reasons: 1) presence of different species, 2) the use of different medium to prepare the slides (see Fankoua et al. 2017Fankoua SO, Bitja Nyom AR, Bahanak Dnd, Bilong Bilong CF, Pariselle A (2017) Influence of preservative and mounting media on the size and shape of monogenean sclerites. Parasitology Research 116: 2277-2281. https://doi.org/10.1007/s00436-017-5534-7
https://doi.org/10.1007/s00436-017-5534-...
). Knowing that we did not see morphological differences between “large” and “small” specimens, and that both were found together on same slides (in the same medium), we are most probably in the presence of a species with a great variability in the size of its haptoral hard parts.

Figure 28
PCA-Biplot of species belonging to Bagrobdella.

Considering that the two new species have a non-spirally coiled MCO, the Bagrobdella diagnosis should be amended, in fact the more recent given by Kritsky and Kulo (1999Kritsky DC, Kulo SD (1999) Revisions of Protoancylodiscoides and Bagrobdella, with redescriptions of P. chrysichthes and B. auchenoglanii (Monogenoidea: Dactylogyridae) from the gills of two bagrid catfishes (Siluriformes) in Togo, Africa. Comparative Parasitology 66(2): 138-145.) indicate that “Copulatory complex a coiled tube with clockwise rings”.

The research on new species of Monogenea from Siluriformes is ongoing in the Lake Tanganyika.

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ADDITIONAL NOTES

  • Zoobank register

    https://zoobank.org/8C8A77CC-BFE7-46E9-B364-58AEC22B8A6A
  • How to cite this article

    Mushagalusa Mulega A, Muterezi Bukinga F, Akoumba JF, Masilya MP, Pariselle A (2022) Monogeneans from Catfishes in Lake Tanganyika. I: Two new species of Bagrobdella (Dactylogyridae) from Auchenoglanis occidentalis (Siluriformes: Claroteidae). Zoologia (Curitiba) 39: e22016. https://doi.org/10.1590/S1984-4689.v39.e22016
  • Published by

    Sociedade Brasileira de Zoologia at Scientific Electronic Library Online (https://www.scielo.br/zool)

Edited by

Editorial responsibility

Walter A.P. Boeger

Publication Dates

  • Publication in this collection
    28 Oct 2022
  • Date of issue
    2022

History

  • Received
    24 Mar 2022
  • Accepted
    14 July 2022
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