Three new Dactylogyrus species (Monogenea: Dactylogyridae) and redescription of one other, gill parasites of five Labeo spp. (Cypriniformes: Cyprinidae) from the Sanaga basin (Cameroon, Central Africa)

Sévérin-Oscar Fankoua Etienne Didier Bassock Bayiha Arnold Roger Bitja Nyom Imane Rahmouni Alexandre Michel Njan Nlôga Charles Félix Bilong Bilong About the authors

ABSTRACT

Three new and one already known species of Dactylogyrus Diesing, 1850 are described from five species of Labeo (Cyprinidae) sampled in the middle section of the Sanaga hydrosystem (Centre Region-Cameroon): Dactylogyrus sanagaensis sp. nov. from Labeo sanagaensis Tshibwabwa, 1997, L. nunensis Pellegrin, 1929, L. camerunensis Trewavas, 1974 and L. annectens Boulenger, 1903; Dactylogyrus nachtigalensis sp. nov. and D. yassensis Musilová, Řehulková & Gelnar, 2009 from Labeo batesii Boulenger, 1911; and Dactylogyrus djimensis sp. nov. from Labeo camerunensis. Dactylogyrus sanagaensis sp. nov. is close to D. longiphalloides, D. longiphallus, D. leonis, D. marocanus, and D. dembae, however it can be easily distinguished from these species by the size of MCO. Dactylogyrus nachtigalensis sp. nov. is similar to D. dembae and D. sanagaensis sp. nov. but this new species can be mainly differentiated by the length of penis. Dactylogyrus djimensis sp. nov. mostly similar to D. omega can be differentiated from it by the penis diameter. Dactylogyrus yassensis collected from Cameroon doesn’t significantly differ morphometrically from the original description, thus extends the distribution of this species to Sanaga basin. Monogenean species collected from Labeo spp. in the middle section of the Sanaga hydrosystem were classified into two morphological groups: the ‘pseudanchoratus-like group’ and the ‘cyclocirrus-like group’ newly defined herein. Phylogenetic relationships are suggested among Dactylogyrus species.

KEYS WORDS:
Dactylogyrus nachtigalensis sp. nov.; Dactylogyrus sanagaensis sp. nov.; Dactylogyrus djimensis sp. nov.; Dactylogyrus yassensis; taxonomy.

INTRODUCTION

While both Cyprinidae and Cichlidae are more represented in the African freshwater ichthyofauna (Lévêque et al. 2008Lévêque C, Oberdorff T, Paugy D, Stiassny MLJ, Tedesco PA (2008) Global diversity of fish (Pisces) in freshwater. Hydrobiologia 595: 545-567. https://doi. 10.1007/s10750-007-9034-0
https://doi. 10.1007/s10750-007-9034-0...
), cyprinids belonging to the genus Labeo Cuvier, 1816 are widely distributed throughout Africa and South-East Asia (De Weirdt et al. 2007De Weirdt D, Getahun A, Tshibwabwa S, Teugels GG (2007) Cyprinidae. In: Stiassny MLJ, Teugels GG, Hopkins CD (Eds) Poissons d’eaux et saumâtres de basse Guinée, ouest de l’Afrique centrale. IRD, MnHn, MRAC, Paris, vol. 1, 466-571.). About 88 species of Labeo are described in Africa, which can be divided into two distinct groups based on the presence of papillate or plicate lips. Members of the latter group are only represented in Lower Guinea by six valid species and an undescribed one (Tshibwabwa 1997Tshibwabwa SM (1997) Systématique des espèces africaines du genre Labeo (Teleostei, Cyprinidae) dans les régions ichtyogéographiques de Basse-Guinée et du Congo. II. PhD Thesis, Faculté Universitaire Notre-Dame de la Paix de Namur, Namur, Belgique, 227pp. Available online at: https://researchportal.unamur.be/en/studentTheses/syst%C3%A9matique-des-esp%C3%A8ces-africaines-du-genre-labeo-teleostei-cypr
https://researchportal.unamur.be/en/stud...
). They are all present in Cameroon (Bitja Nyom et al. 2020Bitja Nyom AR, Njom SD, Kitio HI, Bilong Bilong CF (2020) Diversité de l’ichtyofaune de la rivière Djérem: impact du barrage de Mbakaou et enjeux pour la conservation des poissons dans le Parc National du Mbam et Djérem (Cameroun). International Journal of Biological and Chemical Science 14: 1520-1535. https://doi.org/10.4314/ijbcs.v14i5.3
https://doi.org/10.4314/ijbcs.v14i5.3...
) that is a crossroads of many hydrographic basins (Niger, Congo, Cross and Atlantic) (Olivry 1986Olivry JC (1986) Fleuves et rivières du Cameroun. MESRES-ORSTOM, Paris, 781pp.): Labeo sanagaensis Tshibwabwa, 1997, L. batesii Boulenger, 1911, L. nunensis Pellegrin, 1929, L. camerunensis Trewavas, 1974, L. annectens Boulenger, 1903, L. lukulae Boulenger, 1902, and Labeo sp. All of them are found in the Sanaga hydrosystem. Despite the diversity of Labeo spp. in this basin, no data on their parasitic biodiversity is available.

Monogeneans are hosts specific and may provide information on their hosts biogeography and/or phylogeny (Guégan et al. 1988Guégan JF, Lambert A, Euzet L (1988) Etude des Monogènes des Cyprinidae du genre Labeo en Afrique de l’Ouest. I. Genre Dactylogyrus Diesing, 1850. Revue d’Hydrobiologie Tropicale 21(2): 135-151., 1989Guégan JF, Lambert A, Euzet L (1989) Etude des Monogènes des Cyprinidae du genre Labeo en Afrique de l’ouest. II. Genre Dogielius Bykhowski, 1936. Revue d’Hydrobiologie Tropicale 22(1): 35-48., Boeger et al. 2003Boeger WA, Kritsky DC, Pie MR (2003) “Context of diversification of the viviparous Gyrodactylidae (Platyhelminthes, Monogenoidea).” Zoologica Scripta 32: 437-448. https://doi. 10.1046/j.1463-6409.2003.00130.x
https://doi. 10.1046/j.1463-6409.2003.00...
, Pérez-Ponce & Choudhury 2005Pérez-Ponce de Leon G, Choudhury A (2005) “Biogeography of helminth parasites of freshwater fishes in Mexico: the search for patterns and processes”. Journal of Biogeography 32: 645-659. https://doi:10.1111/j.1365-2699.2005.01218.x
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, Šimková et al. 2007Šimková A, Pečinková M, Řehulková E, Vyskočilová M, Ondračkova M (2007) Dactylogyrus species parasitizing European Barbus species: morphometric and molecular variability. Parasitology 134: 1751-1765. https://doi. 10.1017/S0031182007003265
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, 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: 1-15. https://doi.org/10.4061/2011/471480
https://doi.org/10.4061/2011/471480...
). To date, more than 900 nominal species of Dactylogyrus Diesing, 1850 have been described in the world (Gibson et al. 1996Gibson DI, Timofeeva TA, Gerasev PI (1996) A catalogue of the nominal species of the monogenean genus Dactylogyrus Diesing, 1850 and their host genera. Systematic Parasitology 35: 3-48.) mainly on cyprinids. A total of 100 species have been listed on African cyprinids belonging to six genera: Enteromius Cope, 1867, Labeobarbus Rüppell, 1836, Labeo, Luciobarbus Heckel, 1843, Carasobarbus Karaman, 1971, and recently on Pterocapoeta Günther, 1902 (Raphahlelo et al. 2020Raphahlelo EM, Přikrylová I, Malta MM (2020) Dactylogyrus spp. (Monogenea, Dactylogyridae) from the gills of Enteromius spp. (Cypriniformes, Cyprinidae) from the Limpopo Province, South Africa with description of three new species. Acta parasitological 65: 396-412. https://doi.org/10.2478/s11686-020-00175-5
https://doi.org/10.2478/s11686-020-00175...
). According to Paperna (1979Paperna I (1979) Monogenea of inland water fish in Africa. Annales des Musée Royal de l’Afrique Centrale, Science Zoologique 226: 1-131.), Dactylogyrus spp. in Africa could be divided into three distinctive groups (pseudanchoratus-like group, afrobarbae-like group and varicorhini-like group) based in one hand on the morphology of sclerotized parts of the haptor, and on the other hand on the structure of copulatory organs: pseudanchoratus-like group characterized by anchors with long inner root and very short or even vestigial outer root, a tubiform cirrus (penis) slightly curved or coiled if longer (Paperna 1979Paperna I (1979) Monogenea of inland water fish in Africa. Annales des Musée Royal de l’Afrique Centrale, Science Zoologique 226: 1-131.); afrobarbae-like group characterized by anchors with long inner root and short or vestigial outer root, tubiform cirrus (penis), long and coiled once or twice, with distal portion embraced by the accessory piece; varicorhini-like group characterized by two bars one large and wide with extreme median constriction, cirrus (penis) long coiled tube (Paperna 1979Paperna I (1979) Monogenea of inland water fish in Africa. Annales des Musée Royal de l’Afrique Centrale, Science Zoologique 226: 1-131.). El-Gharbi et al. (1994El-Gharbi S, Birgi E, Lambert A (1994) Monogènes Dactylogyridae parasites de Cyprinidae du genre Barbus d’Afrique du Nord. Systematic Parasitology 27: 45-70.), then Rahmouni et al. (2017Rahmouni I, Řehulková E, Pariselle A, Berrada Rkhami O, Šimková A (2017) Four new species of Dactylogyrus Diesing, 1850 (Monogenea: Ancyrocephalidae) parasitizing the gills of northern Moroccan Luciobarbus Heckel (Cyprinidae): morphological and molecular characterisation. Systematic Parasitology 94: 575-591. https://doi.org/10.1007/s11230-017-9726-4
https://doi.org/10.1007/s11230-017-9726-...
) identified four types of haptors in the North African region: varicorhini-like group, pseudanchoratus-like group, carpathicus-like group characterized by the presence of a cross-shaped ventral bar, and the guirensis-like group specific to the Guir basin and mainly characterized by a single cross-shaped bar with curved ends, anchors with very long guard and tip. These last two groups were only found in this part of the continent where afrobarbae-like group seems to be absent. In Africa, only few data concern Monogenea parasitizing Labeo spp. (Paperna 1969Paperna I (1969) Monogenetic trematodes of fish of the Volta basin and south Ghana. Bulletin de l’Institut Fondamental d’Afrique Noire 31: 840-880., 1973Paperna I (1973) New species of Monogenea (Vermes) from African freshwater fish. A preliminary report. Revue de Zoologie et de Botanique Africaine 87: 505-518., 1979Paperna I (1979) Monogenea of inland water fish in Africa. Annales des Musée Royal de l’Afrique Centrale, Science Zoologique 226: 1-131., Guégan and Lambert 1991Guégan JF, Lambert A, Euzet L (1988) Etude des Monogènes des Cyprinidae du genre Labeo en Afrique de l’Ouest. I. Genre Dactylogyrus Diesing, 1850. Revue d’Hydrobiologie Tropicale 21(2): 135-151., Gibson et al. 1996Gibson DI, Timofeeva TA, Gerasev PI (1996) A catalogue of the nominal species of the monogenean genus Dactylogyrus Diesing, 1850 and their host genera. Systematic Parasitology 35: 3-48., Musilová et al. 2009Musilová N, Řehulková E, Gelnar M (2009) Dactylogyrids (Platyhelminthes: Monogenea) from the gills of the African carp, Labeo coubie Rüppell (Cyprinidae), from Senegal with description of three new species of Dactylogyrus and the redescription of Dactylogyrus cyclocirrus Paperna, 1973. Zootaxa 2241: 47-68., Pravdová et al. 2018Pravdová M, Ondračková1 M, Přikrylová I, Blažek R, Mahmoud Z, Gelnar M (2018) Dactylogyrids (Platyhelminthes: Monogenea) from Sudanese Labeo spp., with a description of Dogielius sennarensis sp. nov. and a redescription of Dogielius flosculus Guégan, Lambert & Euzet, 1989. Helminthologia 55: 306-321. https://doi:10.2478/helm-2018-0033
https://doi:10.2478/helm-2018-0033...
). In Cameroon, no data on monogeneans from Labeo was found; Birgi and Euzet (1983Birgi E, Euzet L (1983) Monogènes parasites des poissons des eaux douces du Cameroun. Présence des genres Cichlidogyrus et Dactylogyrus chez Aphyosemion (Cyprinodontidae). Bulletin de la Société Zoologique de France 108: 101-106.) described for the first time a dactylogyrid (Dactylogyrus batesii Birgi & Euzet, 1983) from a Cyprinodontidae of the genus Aphyosemion Myers, 1924. Afterwards fourteen monogenean species were described from species belonging to Barbus Cuvier & Cloquet, 1816 (syn. Enteromius Cope, 1867) in the Nyong basin (Birgi 1987Birgi E (1987) Monogènes parasites de poissons d’eau douce au Tchad et du Sud-Cameroun. Taxinomie et essai de biogéographie comparée. PhD thesis, Université de Montpellier II, France, 230pp. Available online at: https://www.theses.fr/032039581
https://www.theses.fr/032039581...
, Birgi and Lambert 1987Birgi E, Lambert A (1987) Les Dactylogyrus (Plathelminthes, Monogenea) des Cyprinidae du genre Barbus du Sud Cameroun. Revue d’Hydrobiologie Tropicale 20 (1): 37-48.).

The aim of this work was to bring better knowledge on the biodiversity of Monogenean parasites of Labeo spp. in the middle section of the Sanaga hydrosystem.

MATERIAL AND METHODS

Fish specimens (30 Labeo batesii, 21 L. sanagaensis, 19 L. nunensis, 15 L. camerunensis, 3 L. annectens) were sampled from January 2018 to March 2019 in the middle section of the Sanaga basin (Fig. 1) using gill nets. Immediately after fishing, they were kept in a portable deep freezer (Engel) then transported to the laboratory for further examination. After thawing, the gill arches were detached and placed in a Petri dish with tap water. Monogeneans were detached from the gill filaments under a stereomicroscope (M8 Wild Heerbrugg) using an entomological needle, then mounted between slide and cover slip in a drop of ammonium picrate-glycerine (Malmberg 1957Malmberg G (1957) On the occurrence of Gyrodactylus on Swedish fishes. Skrifterutgivna av Sodra Sveriges Fiskeriforeningen, 19-76.) according to Bassock Bayiha et al. (2016Bassock Bayiha ED, Nack J, Pariselle A, Bilong Bilong CF (2016) Two new species of gill parasites assigned to Protoancylodiscoides (Monogenea, Ancyrocephalidae) from Chrysichthys spp. (Siluriformes, Claroteidae) in River Sanaga (Cameroon). Zootaxa 4170: 178-186. https://doi.org/10.11646/zootaxa.4170.1.11
https://doi.org/10.11646/zootaxa.4170.1....
). After 24 hours, slides were sealed with Glyceel (Bates 1997Bates JW (1997) The slide-sealing compound ‘Glyceel’. Journal of Nematology 29: 565-566.). Morphological study of the sclerotized parts of the haptor and the copulatory organs (i.e., male copulatory organ and vagina) was made with a Leica DM 2500 microscope and the LAS 3.8 software. Measurements, with some modifications, are those defined by Gussev (1962Gussev AV (1962) Order Dactylogyridea. In: Bychovskaya-Pavlovskaya IE, Gussev AV, Dubinina MN, Izymova NA, Smirnova TS, Sokolovskaya IL, Shtein GA, Shul’man SS, Epsthein VM (Eds) Key to the parasites of freshwater fish of the USSR. Israel Program for Scientific Translations, Jerusalem, 204-342.) (Fig. 2). They are given in micrometers and expressed as follows: mean (range, number of measurements). Drawings were made with the camera lucida of a Leitz Diaplan microscope and refined through Coral Draw X4 Software (v. 14.0.0.70, Corel Inc.). Numbering the haptoral pieces followed Llewellyn (1963Llewellyn J (1963) Larvae and larval development of Monogenea. In: Dawes B (Eds) Advances in Parasitology. Academic Press, London, vol. 1, 287-326.) and the recommendation adopted at ICOPA IV (Euzet and Prost 1981Euzet L, Prost M (1981) Report of the meeting on Monogenea: problems of systematics, biology and ecology. Review of Advanced in parasitology. P.W.N. Polish Scientific Publishers, Warsaw, 1003-1004.). Mean intensity and prevalence are defined after Bush et al. (1997Bush AO, Latterty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83: 575-583. https://doi. 10.2307/3284227
https://doi. 10.2307/3284227...
). Principal Component Analysis (PCA) of morphometric data was performed on 22 variables from 53 specimens using Statistica software version 6 (StatSoft Inc. 2012StatSoft Inc (2012) Electronic Statistics Textbook. StatSoft, Tulsa, v. 12.0. Available online at http://www.statsoft.com
http://www.statsoft.com...
). Note that authors of new species are different from those of this paper according to Article 50.1 and Recommendation 50A of the International Code of Zoological Nomenclature (ICZN 1999ICZN (1999) International Code of Zoological Nomenclature. The International Trust for Zoological Nomenclature, London, http://www.nhm.ac.uk/hosted-sites/iczn/code
http://www.nhm.ac.uk/hosted-sites/iczn/c...
). Type specimens were deposited in the Royal Museum for Central Africa (RMCA), Tervuren, Belgium.

Figure 1
Map of the middle section of the Sanaga hydrosystem indicating sampling localities.

Figure 2
Measurements taken on sclerotized parts according to Gussev (1962Gussev AV (1962) Order Dactylogyridea. In: Bychovskaya-Pavlovskaya IE, Gussev AV, Dubinina MN, Izymova NA, Smirnova TS, Sokolovskaya IL, Shtein GA, Shul’man SS, Epsthein VM (Eds) Key to the parasites of freshwater fish of the USSR. Israel Program for Scientific Translations, Jerusalem, 204-342.). Anchor: (a) total length, (b) length to notch, (c) outer root length, (d) inner root length, (e) point length; (DB) Dorsal bar and (VB) ventral bar: (x) length, (w) width; (H) hook I to VII: length (“larval hook” + shank = proximal + distal subunit); Male copulatory organ (MCO): (TL) total length, (Pe) penis, (L) length, (APb) accessory piece base length; (Vg) vagina: (L) length, (l) width. Scale bar: 20 μm.

TAXONOMY

Dactylogyrus sanagaensis Fankoua, Bassock Bayiha & Rahmouni, sp. nov.

Fig. 3

http://zoobank.org/73C94FE9-77F5-4999-95CB-6A3F1F8B75C5

Type host. Labeo sanagaensis Tshibwabwa, 1974.

Other hosts. Labeo nunensis Pellegrin, 1929; Labeo camerunensis Trewavas, 1974; Labeo annectens Boulenger, 1903.

Infection site. Gill lamellae.

Type locality. Nachtigal (04°20’50.1”N; 011°38’00.3”E).

Other localities. Ndokoa (04°23’56.64”N; 011°44’14.52”E), National Park of Mpem and Djim (05°6’37.23”N; 11°33’28.91”E).

Prevalence. 69.2% in Labeo sanagaensis, 60% in L. nunensis, 67.7% in L. camerunensis, 33.3% in L. annectens.

Mean intensity. 7.9 in L. sanagaensis, 15.5 in L. nunensis, 8.5 in L. camerunensis, 01 in L. annectens.

Material studied. 18 whole-mounted specimens in GAP.

Type specimens. Holotype RMCA_VERMES_43352, Paratype RMCA_VERMES_43353, Paratype RMCA_VERMES_43354, Paratype RMCA_VERMES_43355, Paratype RMCA_VERMES_43356, Paratype RMCA_VERMES_43357.

Etymology. Epithet sanagaensis refers to the River Sanaga in which specimens of the type host were sampled.

Figure 3
Drawing of sclerotized parts of Dactylogyrus sanagaensis sp. nov.: (DA) dorsal anchor, (DB) Dorsal bar, (VB) ventral bar, (Pe) penis, (AP) accessory piece, (Vg) vagina, (N) needle. Scale bar: 20 μm.

Description. The anatomy is that of the Dactylogyrus. Body length 335.8 (271.9-483.8; n = 18); width 68.3 (48.5-86.4; n = 18) at level of ovary. Cephalic glands present. Two pairs of eye-spots of variable size, anterior to pharynx. Haptor not well separated from rest of the body. Dorsal anchor (DA) with arched point, guard distinctively longer than shaft, and arched at the distal extremity. Ventral bar (VB) reduced, crescent moon-shaped. Dorsal bar (DB) straight and enlarged at the middle and at the two extremities. All the 14 hooks (07 pairs) with similar morphology but different sizes. One pair of needles (N) located near hooks pair V. Male copulatory organ (MCO) complex, J-shaped, tubular penis starting by a basal bulb (one ovoid lobe). Accessory piece (AP) is T-shaped with two branch of equal size, one with a sharp extremity, the other with a rounded extremity; a thinner part attached to this extremity folded back near the sharp extremity. Vagina (Vg) is a short thick tube with a flame shaped structure at its distal extremity; the distal third of vagina is wrapped by a large ring with two short filaments on either side.

The measurements of haptoral and copulatory sclerites are similar in both hosts and given in Table 1.

Table 1
Measurements in micrometers of the sclerotized parts of three new species of Dactylogyrus and three others species already described.

Remarks. Dactylogyrus sanagaensis sp. nov. resembles D. leonisMusilová, Řehulková & Gelnar, 2009Musilová N, Řehulková E, Gelnar M (2009) Dactylogyrids (Platyhelminthes: Monogenea) from the gills of the African carp, Labeo coubie Rüppell (Cyprinidae), from Senegal with description of three new species of Dactylogyrus and the redescription of Dactylogyrus cyclocirrus Paperna, 1973. Zootaxa 2241: 47-68. from Labeo coubie Rüppell, 1832, D. longiphallus Paperna, 1973 from L. victorianus Boulenger, 1901, D. longiphalloides Guégan & Lambert, 1991 from Labeo allauadi, Pellegrin, 1933, and D. marocanus El Gharbi, Birgi & Lambert, 1994 from Carasobarbus fritschii Günther, 1901 and D. dembae Musilová, Řehulková & Gelnar, 2009 from L. coubie by the similar shaped haptoral sclerites, the conspicuous subterminal notch on the outer root of the dorsal anchor, the same ‘pseudanchoratus’ type of the male copulatory organ (J-shaped), accessory piece T-shaped, tubular vagina with a distal flame shaped structure, and a large ring with two short distal filaments. The main difference is the size of MCO: AP = 29-41 µm vs 28-32 µm; 31-40 µm; 45-52 µm; 38-57 µm and 26-30 µm respectively for D. leonis, D. longiphallus, D. longiphalloides, D. marocanus and D. dembae; Pe = 27-34 µm vs 28-34 µm; 38-45 µm; 40-45 µm; 41-61 µm and 27-34 µm respectively for D. leonis, D. longiphallus, D. longiphalloides, D. marocanus and D. dembae.

Dactylogyrus nachtigalensis Fankoua, Bassock Bayiha & Rahmouni, sp. nov.

Fig. 4

http://zoobank.org/01715191-F0D4-44A7-9F41-8E1532573603

Type host. Labeo batesii Boulenger, 1911.

Infection site. Gill lamellae.

Type locality. Nachtigal (04°20’50.1”N; 011°38’00.3”E).

Other localities. Ndokoa (04°23’56.64”N; 011°44’14.52”E), National Park of Mpem and Djim (5° 6’37.23”N; 11°33’28.91”E), Assamba (04°24’33”N; 011°49’47.34”E).

Prevalence. 90%.

Mean intensity. 5.1.

Material studied. 12 whole mounted specimens in GAP.

Type specimens. Holotype RMCA_VERMES_43364, Paratype RMCA_VERMES_43365, Paratype RMCA_VERMES_43366, Paratype RMCA_VERMES_43367, RMCA_VERMES_4338 and RMCA_VERMES_43369.

Etymology. Epithet nachtigalensis refers to the type locality (Nachtigal).

Figure 4
Drawing of sclerotized parts of Dactylogyrus nachtigalensis sp. nov.: (DA) dorsal anchor, (DB) Dorsal bar, (VB) ventral bar, (Pe) penis, (AP) accessory piece, (Vg) vagina, (N) needle. Scale bar: 20 μm.

Description. The anatomy is that of the Dactylogyrus. Body length 339.9 (194.4-402.9; n = 12); width 70.7 (42.5-86.8; n = 12) at the level of ovary. Haptor not really separated from the rest of the body by a constriction; cephalic glands present, two pairs of eye-spots of variable sizes, anterior to pharynx. Dorsal anchor with arched point, guard distinctively longer than shaft, arched narrow handle. Dorsal bar (DB) slightly curved at its median part. Ventral bar (VB) crescent moon-shaped, much smaller than dorsal bar. Presence of seven pairs of hooks with same morphology and size except pair VI smaller than the others; all hooks kept their larval form (oncomiracidia). One pair of needles (N) located near hooks of pair V. Male copulatory organ (MCO): tubular J-shaped penis begins with a basal bulb, runs alongside the accessory piece. Accessory piece straight bar, wrapped around the basal bulb, ends in two branches like in D. sanagaensis sp. nov., one branch straight and sharp ended, the other one longer, thinner at its distal part, folded back at first third, reaches the sharp end then folded back again. Base of accessory piece (AP b) shorter than in D. sanagaensis sp. nov. Vagina short with large aperture, distal extremity with sclerotised plate.

The measurements of haptoral and reproductive sclerites are given in Table 1.

Remarks. Dactylogyrus nachtigalensis sp. nov. is close to D. sanagaensis sp. nov. by the morphology of its haptor and MCO, but differs from it by (i) the length of the penis: 52.1-65.6 µm vs 42.7-47.1 µm, (ii) the morphology of the dorsal bar, straight in both species, but slightly curved in the median part in D. nachtigalensis sp. nov., (iii) the total length of male copulatory organ: 11.7-14.8 µm vs 17.8-30.4 µm in D. sanagaensis sp. nov., the morphology and size of the vagina, not flame shaped and 5.6-9.1 µm vs flame shaped and 7.4-17.2 µm in D. sanagaensis sp. nov. Dactylogyrus nachtigalensis is also close to D. dembae (syn: D. cf. labeous) from Labeo coubie by the morphology of the haptor and male copulatory organ. The main differences are the length of penis 42.7-47.1 µm and of the MCO 11.7-14.8 µm vs 27-34 µm and 26-30µm in D. dembae. Dactylogyrus nachtigalensis sp. nov. also presents the typically morphology of ‘pseudanchoratus-like group’.

Dactylogyrus djimensis Fankoua, Bassock Bayiha & Rahmouni, sp. nov.

Fig. 5

http://zoobank.org/D703D538-7418-4FE5-843F-95D37AF0DA94

Type host. Labeo camerunensis Trewavas, 1974.

Infection site. Gill lamellae.

Type locality. Djim river: 04°20’50, 1”N; 011°38’00, 3”E; alt.441 m.

Prevalence. 50 %.

Mean intensity. 3.5.

Material studied. 16 whole mounted specimens in GAP.

Type specimens. Holotype RMCA_VERMES_43358, Paratype RMCA_VERMES_43359, Paratype RMCA_VERMES_43360, Paratype RMCA_VERMES_43361, Paratype RMCA_VERMES_43362, Paratype RMCA_VERMES_43363.

Etymology. Epithet djimensis refers to the River Djim in which specimens of the type host were sampled.

Figure 5
Drawing of sclerotized parts of Dactylogyrus djimensis sp. nov.: (DA) dorsal anchor, (DB) Dorsal bar, (VB) ventral bar, (Pe) penis, (AP) accessory piece, (Vg) vagina, (N) needle. Scale bar: 20 μm.

Description. Body length 612 (455-822, n = 16) and 141 (14-245, n = 16) width at the level of ovary. Cephalic glands present, two pairs of eye-spots of variable sizes, anterior to pharynx. Haptor well separated from the rest of the body by a narrow constriction. Dorsal anchors strong with arched point, guard longer than shaft. Dorsal bar (DB) straight with spherical and fenestrated extremities. Ventral bar (VB) vestigial shovel-shaped. Presence of seven pairs of hooks morphologically similar with larval form, approximately same length except hooks pairs I and V longer than others. One pair of needles (N) located near hooks pair V. Male copulatory organ (MCO) with: tubular coiled penis starts from a bulb with large base, lacks flange, winds around the accessory piece at its middle and ends in a rounded part; accessory piece slightly sclerotized, forms an asymmetrical triangular frame with a shaft. No sclerotized vagina observed.

New measurements of haptoral and reproductive sclerites are given in Table 1.

Remarks. By the morphology of the haptoral sclerites and the MCO, this species is close to D. yassensisMusilová, Řehulková & Gelnar, 2009Musilová N, Řehulková E, Gelnar M (2009) Dactylogyrids (Platyhelminthes: Monogenea) from the gills of the African carp, Labeo coubie Rüppell (Cyprinidae), from Senegal with description of three new species of Dactylogyrus and the redescription of Dactylogyrus cyclocirrus Paperna, 1973. Zootaxa 2241: 47-68. from L. coubie, D. cyclocirrus Paperna, 1973 from Labeo coubie, L. cylindricus Peters, 1852, L. victorianus and L. senegalensis Valenciennes, 1842, D. digitalis Paperna, 1969 from L. coubie, D. nathaliae Guégan & Lambert, 1988 from Labeo sp. from Mali, and D. omega Guégan & Lambert, 1991 from L. parvus and L. rouaneti. It differs from D. yassensis by the length of anchor inner root 9.6-12.9 µm and outer root 3.1-6.6 µm vs 12-14 µm and 5-7 µm, dorsal bar 21.1-26.4 µm vs 26-27µm, penis 74.8-90.4 µm vs 74-79 µm; from D. cyclocirrus by the length of anchor inner root 9.6-12.9 µm vs 24-28 µm, dorsal bar 21.1-26.4 µm vs 23-27 µm, penis 74.8-90.4 µm vs 62-69 µm; from D. digitalis by the length of dorsal bar 21.1-26.4 µm vs 28-34 µm, and its coiled penis 74.8-90.4 µm vs simple penis 70 µm; from D. nathaliae by the size of anchor inner length 32.7-36.3 µm vs 26-30 µm, its coiled penis 74.8-90.4 µm vs curved penis 37-45 µm; from D. omega by the length of anchor inner root 9.6-12.9 µm and outer root 3.1-6.6 µm vs 10-14 µm and 3-6 µm, dorsal bar 21.1-26.4 µm vs 24-28 µm, though hooks length and diameter of penis 10.7-16.7 µm vs 2-3.

Dactylogyrus yassensis Musilová, Řehulková & Gelnar, 2009

Fig. 6

Type host and locality. Labeo coubie, Gambia River near the Campement du Lion, Niokolo-Koba National Park, Senegal.

Other records. Labeo senegalensis, Niger River (Bamako), Baoulé River (Missira), Mali; Guiers Lake, Senegal, (Guégan et al. 1988Guégan JF, Lambert A, Euzet L (1988) Etude des Monogènes des Cyprinidae du genre Labeo en Afrique de l’Ouest. I. Genre Dactylogyrus Diesing, 1850. Revue d’Hydrobiologie Tropicale 21(2): 135-151.); Labeo coubie, Gambia River near the hotel Simenti, Niokolo-Koba National Park, Senegal; Labeo horie Heckel, 1847, While Nile, Kosti, Sudan; Blue Nile, Sennar.

Present record. Labeo batesii, 1911 in Sanaga at Nachtigal (04°20’50.1”N; 011°38’00.3”E), in Sanaga at Ndokoa (04°23’56.64”N; 011°44’14.52”E), National Park of Mpem and Djim (5° 6’37.23”N; 11°33’28.91”E) and Assamba (04°24’33”N; 011°49’47.34”E).

Infection site. Gill lamellae.

Prevalence. 60%

Mean intensity. 5.2

Material studied. Whole mounted specimens in GAP.

Figure 6
Drawing of sclerotized parts of Dactylogyrus yassensis. (DA) dorsal anchor, (DB) Dorsal bar, (VB) ventral bar, (Pe) penis, (AP) accessory piece, (Vg) vagina, (N) needle. Scale bar: 20 μm.

Redescription. Body length 594.3 (491.9-758.7; n = 7); width 141 (100.7-206.4; n = 7) at the level of ovary. Cephalic glands present, two pairs of eyes present anterior to the pharynx. Single pair of anchors (dorsal); long inner root truncate; short outer root blunt; curved shaft slightly swollen at level of filament hitch; point not reaching level of tip of inner root. Dorsal bar bonelike, with short truncate posteromedial process; ventral bar reduced, vestigial. Presence of 7 pairs of hooks, similar with larval form, approximately same length except hooks pairs I and V. One pair of needles located near hooks of pair V. No sclerotized vagina observed. Copulatory organ is a coiled wide tube, winds around the accessory piece. Accessory piece slightly sclerotized, articulated to base.

New measurements of haptoral and reproductive sclerites are given in Table 1.

Remarks. The morphology and measurements of the specimens parasitizing Labeo batesii in the Sanaga basin (Cameroon) correspond to the original description of Dactylogyrus yassensis from L. coubie in five countries: Niger, Mali, Ghana, Gambia and Senegal (Musilová et al. 2009Musilová N, Řehulková E, Gelnar M (2009) Dactylogyrids (Platyhelminthes: Monogenea) from the gills of the African carp, Labeo coubie Rüppell (Cyprinidae), from Senegal with description of three new species of Dactylogyrus and the redescription of Dactylogyrus cyclocirrus Paperna, 1973. Zootaxa 2241: 47-68.; Pravdová et al. 2018Pravdová M, Ondračková1 M, Přikrylová I, Blažek R, Mahmoud Z, Gelnar M (2018) Dactylogyrids (Platyhelminthes: Monogenea) from Sudanese Labeo spp., with a description of Dogielius sennarensis sp. nov. and a redescription of Dogielius flosculus Guégan, Lambert & Euzet, 1989. Helminthologia 55: 306-321. https://doi:10.2478/helm-2018-0033
https://doi:10.2478/helm-2018-0033...
). The only difference that could be detected is that of the penis length 82.3-95 µm vs 74-79 µm from the original description by Musilová et al. (2009) in West Africa. Dactylogyrus yassensis can be confused with D. omega but differs mainly from it by larger anchor, dorsal bar smaller and without fenestrated extremities, penis length longer, and the other sclerotized structures slightly smaller.

Morphometric study by PCA

The principal component analysis (PCA) performed on the measurements of sclerotized parts of the haptor and the MCO showed that Monogeneans collected in the present work belong to four well distinct groups (Fig. 7). With regard to the haptor data and the MCO, axe 2 isolated two subsets made up of two groups each. Axe 1 separated D. nachtigalensis sp.nov. from “D. sanagaensis sp.nov. + D. longiphaloides” on the one side, and D. yassensis from “D. djimensis sp.nov. + D. omega” on the other side.

Figure 7
Result of the principal component analysis performed on measurements (µm) of sclerotized parts of monogeneans.

DISCUSSION

Prior to this study, no record of Dactylogyrus was made from Labeo species in Cameroon because they were not investigated in this country. With the three new Monogeneans described, the number of Dactylogyrus species parasitizing the gills of Labeo spp. in Africa reaches 30. In the current work, D. nachtigalensis sp. nov. and D. djimensis sp. nov. infect only a single host species; L. batesii and L. camerunensis respectively; they are momentarily strictly host specific or oixenous (Euzet and Combes 1980Euzet L, Combes C (1980) Les problèmes de l’espèce chez les animaux parasites. Bulletin de la Société Zoologique de France 40: 239-285.). Dactylogyrus yassensis found parasitizing the gills of L. batesii, is also known from L. coubie, L. senegalensis and L. horie (Musilová et al. 2009Musilová N, Řehulková E, Gelnar M (2009) Dactylogyrids (Platyhelminthes: Monogenea) from the gills of the African carp, Labeo coubie Rüppell (Cyprinidae), from Senegal with description of three new species of Dactylogyrus and the redescription of Dactylogyrus cyclocirrus Paperna, 1973. Zootaxa 2241: 47-68., Pravdová et al. 2018Pravdová M, Ondračková1 M, Přikrylová I, Blažek R, Mahmoud Z, Gelnar M (2018) Dactylogyrids (Platyhelminthes: Monogenea) from Sudanese Labeo spp., with a description of Dogielius sennarensis sp. nov. and a redescription of Dogielius flosculus Guégan, Lambert & Euzet, 1989. Helminthologia 55: 306-321. https://doi:10.2478/helm-2018-0033
https://doi:10.2478/helm-2018-0033...
). Therefore, in the Sub-Saharan area, this monogenean is stenoxenous (Euzet and Combes 1980Euzet L, Combes C (1980) Les problèmes de l’espèce chez les animaux parasites. Bulletin de la Société Zoologique de France 40: 239-285.) or precisely mesostenoxenous (Caira et al. 2003Caira JN, Jensen K, Holsinger KE (2003) On a new index of host specificity. In: Combes C, Jourdane J (Eds) Taxonomy, Ecology and Evolution of Metazoan Parasites. Combes, C. Jourdane, J, PUP, Perpignan, vol. 1, 161-201.). Dactylogyrus sanagaensis sp. nov. is described from four host species, namely L. sanagaensis, L. nunensis, L. annectens and L. camerunensis; therefore, it is also mesostenoxenous (Caira et al. 2003Caira JN, Jensen K, Holsinger KE (2003) On a new index of host specificity. In: Combes C, Jourdane J (Eds) Taxonomy, Ecology and Evolution of Metazoan Parasites. Combes, C. Jourdane, J, PUP, Perpignan, vol. 1, 161-201.). It is worthy to notice that the five Labeo species studied are sympatric (De Weirdt et al. 2007De Weirdt D, Getahun A, Tshibwabwa S, Teugels GG (2007) Cyprinidae. In: Stiassny MLJ, Teugels GG, Hopkins CD (Eds) Poissons d’eaux et saumâtres de basse Guinée, ouest de l’Afrique centrale. IRD, MnHn, MRAC, Paris, vol. 1, 466-571., Bitja et al. 2020Bitja Nyom AR, Njom SD, Kitio HI, Bilong Bilong CF (2020) Diversité de l’ichtyofaune de la rivière Djérem: impact du barrage de Mbakaou et enjeux pour la conservation des poissons dans le Parc National du Mbam et Djérem (Cameroun). International Journal of Biological and Chemical Science 14: 1520-1535. https://doi.org/10.4314/ijbcs.v14i5.3
https://doi.org/10.4314/ijbcs.v14i5.3...
). Their parasitic richness is low, i.e. one for L. annectens, L. nunensis and L. sanagaensis, two for L. batesii and L. camerunensis, while in West Africa monogenean richness reaches 12 species in L. coubie (Scholz et al. 2018Scholz T, Vanhove MPM, Smit N, Jayasundera Z, Gelnar M (2018) A Guide to the Parasites of African Freshwater Fishes. Royal Belgian Institute of Natural Science, Belgium, 424pp.). This low number of Dactylogyrus spp. parasitizing Labeo spp. in the current work could be due at least to the facts that (1) this study was limited in the middle section of the Sanaga hydrosystem and yet it is known that the infra-community can vary along a watercourse (Valtonen et al. 1997Valtonen ET, Holmes JC, Koskivaara M (1997) Eutrophication, pollution and fragmentation: effects on parasites communities in roach (Rutilus rutilus) and perch (Perca fluviatilis) in four lakes in central Finland. Canadian Journal of Fisheries and Aquatic Sciences 54: 572-585.); (2) there are still many Labeo in Cameroon (Lévêque et al. 1990Lévêque C, Paugy D, Teugels GG (1990) Faune des poissons d’eaux douces et saumâtres de l’Afrique de l’Ouest. ORSTOM-MRAC, Paris, 384pp., De Weirdt et al. 2007De Weirdt D, Getahun A, Tshibwabwa S, Teugels GG (2007) Cyprinidae. In: Stiassny MLJ, Teugels GG, Hopkins CD (Eds) Poissons d’eaux et saumâtres de basse Guinée, ouest de l’Afrique centrale. IRD, MnHn, MRAC, Paris, vol. 1, 466-571.) for which ectohelminths remain unstudied.

The presence of D. sanagaensis in four Labeo, namely L. sanagaensis, L. nunensis, L. annectens and L. camerunensis, suggests a relationship between these fish species in the one hand, and may be due to the ecological conditions in the other hand (Euzet and Combes 1980Euzet L, Combes C (1980) Les problèmes de l’espèce chez les animaux parasites. Bulletin de la Société Zoologique de France 40: 239-285., Rhode 1993Rhode K (1993) Ecology of marine parasite. An introduction to marine parasitology. Cab International, Wallingford, Oxon, 2nd ed., 298pp., Mbondo et al. 2017Mbondo AJ, Nack J, Pariselle A, Bilong Bilong CF (2017) The diversity of Monogenean gill parasites of two Synodontis species (Siluriformes, Mochokidae) with description of two new species assigned to Synodontella. Vie et Milieu, Life and Environment 67: 75-80.). The presence of D. yassensis in L. batesii in the current work is an enlargement of its host spectra, as this parasite was previously described from L. coubie, L. senegalensis and L. horie (Musilová et al. 2009Musilová N, Řehulková E, Gelnar M (2009) Dactylogyrids (Platyhelminthes: Monogenea) from the gills of the African carp, Labeo coubie Rüppell (Cyprinidae), from Senegal with description of three new species of Dactylogyrus and the redescription of Dactylogyrus cyclocirrus Paperna, 1973. Zootaxa 2241: 47-68., Pravdová et al. 2018Pravdová M, Ondračková1 M, Přikrylová I, Blažek R, Mahmoud Z, Gelnar M (2018) Dactylogyrids (Platyhelminthes: Monogenea) from Sudanese Labeo spp., with a description of Dogielius sennarensis sp. nov. and a redescription of Dogielius flosculus Guégan, Lambert & Euzet, 1989. Helminthologia 55: 306-321. https://doi:10.2478/helm-2018-0033
https://doi:10.2478/helm-2018-0033...
) in West Africa.

Based on the morphology of the haptor and MCO sclerotized parts, D. sanagaensis sp. nov. and D. nachtigalensis sp. nov. are ranged in the ‘pseudanchoratus like-group’ (Paperna 1979Paperna I (1979) Monogenea of inland water fish in Africa. Annales des Musée Royal de l’Afrique Centrale, Science Zoologique 226: 1-131.), while D. djimensis, D. omega, and D. yassensis in addition to D. cyclocirrus and D. nathaliae may form a new type named “cyclocirrus” (Fig. 8). This new group is characterized by a straight dorsal bar, ventral bar vestigial, shovel-shaped and perpendi cular to the dorsal bar, tubular coiled penis, accessory piece an elongated ring lying on either side of the penis. In the Sanaga river basin, D. sanagaensis and D. nachtigalensis are not hosted by the same fish. The morphological similarities of their sclerotized parts suggest an alloxenic speciation phenomenon (Euzet and Combes 1980Euzet L, Combes C (1980) Les problèmes de l’espèce chez les animaux parasites. Bulletin de la Société Zoologique de France 40: 239-285., Combes and Théron 2000Combes C, Théron A (2000) Metazoan parasites and resource heterogeneity: constraints and benefits. International Journal for Parasitology 30: 299-304. https://doi. 10.1016/S0020-7519(00)00012-6
https://doi. 10.1016/S0020-7519(00)00012...
, Pouyaud et al. 2006Pouyaud L, Desmarias E, Deveney M, Pariselle A (2006) Phylogenetic relationships among monogenean gill parasites (Dactylogyridea, Ancyrocephalidae) infesting tilapiine hosts (Cichlidae): Systematic and evolutionary implications. Molecular Phylogenetics and Evolution 38: 241-249. https://doi:10.1016/j.ympev.2005.08.013
https://doi:10.1016/j.ympev.2005.08.013...
). For D. djimensis and D. yassensis, the alloxenic and or allopatric diversification could have taken place.

Figure 8
Dactylogyrus-groups based on the morphology of dorsal anchors and male copulatory organ.

At the level of our investigations, we cannot give a definite number of monogenean types of haptors associated to MCO found in Cameroon from Labeo spp. in particular, and from Cyprinids in general. It is however important to notice that the ‘pseudanchoratus-like group’, ‘afrobarbae-like group’ and ‘varicorhini-like group’ were already observed in this country (Birgi and Lambert 1987Birgi E, Lambert A (1987) Les Dactylogyrus (Plathelminthes, Monogenea) des Cyprinidae du genre Barbus du Sud Cameroun. Revue d’Hydrobiologie Tropicale 20 (1): 37-48.).

It is noticed that measurements of monogenean individuals studied in this work overlap those of some species already known (Fig. 7); case of: D. djimensis sp.nov. and D. omega; D. sanagaensis sp.nov. and D. longiphaloides (Guégan & Lambert 1991Guégan JF, Lambert A (1991) Dactylogyrids (Platyhelminthes: Monogenea) of Labeo (Teleostei: Cyprinidae) from West African coastal rivers. Journal of the Helminthological Society of Washington 58(1): 85-99.); D. yassensis redescribed and original D. yassens (Musilová, Řehulková & Gelnar, 2009Musilová N, Řehulková E, Gelnar M (2009) Dactylogyrids (Platyhelminthes: Monogenea) from the gills of the African carp, Labeo coubie Rüppell (Cyprinidae), from Senegal with description of three new species of Dactylogyrus and the redescription of Dactylogyrus cyclocirrus Paperna, 1973. Zootaxa 2241: 47-68.). Further genetic analyses are therefore needed to reveal the phylogenetical relationships between these parasite species.

ACKNOWLEDGMENTS

The authors wish to thank Energie de France through financial and logistic support of Nachtigal HydroPower Company and Institut de Recherche pour le Développement under contract COO5-DES-[17].

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ADDITIONAL NOTES

  • Zoobank register

    http://zoobank.org/D016DD4F-A78A-4FE8-B6C0-34575FAA9AF1
  • How to cite this article

    Fankoua S-O, Bassock Bayiha ED, Bitja Nyom AR, Rahmouni I, Njan Nlôga AM, Bilong Bilong CF (2022) Three new Dactylogyrus species (Monogenea: Dactylogyridae) and redescription of one other, gill parasites of five Labeo spp. (Cypriniformes: Cyprinidae) from the Sanaga basin (Cameroon, Central Africa). Zoologia (Curitiba) 39: e21009. https://doi.org/10.1590/S1984-4689.v39.e21009
  • Published by

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

Publication Dates

  • Publication in this collection
    07 Feb 2022
  • Date of issue
    2022

History

  • Received
    13 July 2021
  • Accepted
    17 Jan 2022
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