Open Access
Research Article
Issue
Parasite
Volume 29, 2022
Article Number 37
Number of page(s) 12
DOI https://doi.org/10.1051/parasite/2022035
Published online 18 July 2022

© D-N-D Bahanak et al., published by EDP Sciences, 2022

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

Introduction

Monogenea have a direct life cycle. They are diversified and often host specific [12] and these characters make them an important asset to tackle the question of evolution of species or speciation [48]. As is the case for free-living organisms, speciation in parasites may occur “on-site” (sympatric/synxenic) or on vicarious sites (allopatric/alloxenic) [10]. While the second type of speciation is common for free-living organisms following migration or population isolation, it is less easy for Monogenea; in fact, being strict host specialists, they are the least probable switchers. However, once host switching succeeds, they have a high probability for speciation [7, 19, 48]. Quadriacanthus (Monogenea, Ancyrocephalinae) was proposed by Paperna (1961) for Q. clariadis Paperna, 1961 from the gills of Clarias gariepinus (Burchell) sampled in Israel [32]. To date 38 species are recorded in this genus from Asia and Africa [13, 45]. Although their majority (34 among the 38 known species) have been recorded from Clariid-hosts, the remaining four species have been recorded from non-clariid hosts: Quadriacanthus bagrae Paperna, 1979 from Bagrus docmak (Forsskål) and Bagrus bajad (Forsskål), both Bagridae [34]; Quadriacanthus euzeti Nack, Pariselle & Bilong Bilong, 2016 from Papyrocranus afer (Günther), Notopteridae [30], Quadriacanthus anaspidoglanii Akoumba, Tombi & Pariselle, 2017 from Notoglanidium macrostoma (Pellegrin), Claroteidae [2], and a fourth one, doubtful (see [17, 34]) Quadriacanthus tilapiae Paperna, 1973 from Oreochromis esculentus (Graham), Cichlidae [33]. The presence of these Quadriacanthus spp. on gill filaments of non-clariid hosts raises the question of their origin. The recent study by Francová et al. [13] on Quadriacanthus parasites of catfishes in eastern Africa suggests that the record of Q. bagrae on a bagriid host is the result of a lateral transfer from a clariid-host and that Clariidae are ancestral hosts of Quadriacanthus. In Cameroon, the presence of Q. euzeti and Q. anaspidoglanii on non-clariid fishes was also considered to originate from lateral transfers between Clariidae or Bagridae to Notopteridae for the first [30] and from Clariidae to Claroteidae for the second [2]. Because clariids, bagrids and notopterids or claroteids live in sympatry in Lake Ossa [30] and/or in the Memou’ou River [2], it was impossible, without genetic data, to determine which group was the original host family of laterally transferred Quadriacanthus species. Therefore, the main topic of our work concerns the use of sequence data to test the origin of these species. Taking the example of Q. euzeti in Lake Ossa, we hypothesize that if this species comes from a clariid host, it will be phylogenetically close to Q. levequei Birgi, 1988 (which is morphologically close to Q. euzeti) hosted by Clarias jaensis Boulenger in this lake [42, 43]. If Q. euzeti originates from a bagriid host, it will be phylogenetically close to Q. bagrae described on B. docmak, the sole Bagridae presently recorded in this lake. In the present study, we analyze three morphologically related Quadriacanthus species parasites of clariid and non-clariid fishes, namely Q. levequei, Q. euzeti, and Q. anaspidoglanii and add a new one, also morphologically similar. These four Quadriacanthus species are genetically compared to Q. bagrae and other Quadriacanthus species available in GenBank.

Material and methods

Specimens of the following four species: Clarias maclareni Trewavas [44] (n = 20) endemic to Lake Barombi Mbo (4°38′ N, 9°22′ E); C. jaensis (n = 15) from the Nyong River, Mbalmayo market (3°30′48.54″ N, 11°30′04.83″ E) and Sokamalem, Abong-Mbang (03°58′21.4″ N, 13°14′53.3″ E); A. macrostoma (n = 34) from the Nyong River, Mengong (2°58′31.64″ N, 11°27′06.87″ E), and P. afer (n = 10) from Lake Ossa (4°39′ N, 9°24′ E) (Fig. 1), were caught between January 2016 to February 2017 using gill nets, cast-nets, fish-traps or hook lines, and/or purchased from fishermen. They were immediately placed in a cool box containing ice, then transported to the laboratory where they were frozen at −21 °C. In the laboratory, after thawing of the carcasses, the gill arches of fish specimens were removed by dorsal and ventral sections, then placed in a Petri-dish containing tap water. The parasites were dislodged from the gill filaments with a dissecting needle. Monogeneans were fixed individually between slide and cover slip in a drop of GAP (glycerin ammonium-picrate mixture) [22]. After 24 h, preparations were sealed using Glyceel [4]. The identification was based on the morphology and the size of sclerotized parts of the haptor and the copulatory organs. The measurements, carried out according to Gussev [14] modified by N’Douba et al. [27] (Fig. 2), and drawings of the sclerotized parts of the haptor and copulatory complex, were made with the aid of a Leica DM 2500 microscope, LAS software (3.8), ImageJ 1. 53 K software and Corel DrawX4® software, version 14.0.0.701. Measurements, in micrometers (μm) are presented as follows: mean (minimum–maximum). Prevalence (P) and mean intensity (MI) were calculated according to Bush et al. [8]. Type material and vouchers were deposited in the helminth collection of the Royal Museum for Central Africa (MRAC) Tervuren (Belgium) under accession numbers MRAC 43425-43429. A principal components analysis (PCA) was performed using Statistica 6, with “standardized” measurements according to Messu et al. [26]. To prevent the influence of temperature or of development stage, we divided each by the length of hook II, which is supposed to keep larval size [36]. Twenty-four characters (among a total number of twenty-nine measured on each specimen, see Table 1) were retained for the PCA. Ten (10) specimens of each species included in this work were used in the PCA. For genetic purposes, fish were dissected in the field; gill arches were excised as mentioned above and stored in alcohol (95%) according to Justine et al. [18], then examined under stereomicroscope. Parasites found were mounted individually between slide and cover-slip in a drop of water and identified according to Birgi [6], Nack et al. [30] and Akoumba et al. [2]. After identification, each parasite was placed individually in an Eppendorf® tube containing 95% alcohol. PCR was performed on these specimens according to Marchiori et al. [23], directly without DNA extraction. Standard PCR was performed using primers specific to the D1-D2 domain of the large subunit region (LSU) of the 28S ribosomal gene: C1 (forward; 5′ – ACCCGCTGAATTTAAGCAT – 3′) and D2 (reverse; 5′ – TGGTCCGTGTTTCAAGAC – 3′) [15]. The amplification consisted of three steps and began with 2 min at 93 °C for initial denaturation, followed by 30 cycles: 30 s at 93 °C, 30 s at 56 °C for annealing, 1 min 30 s at 72 °C for extension, with a final 5 min extension step at 72 °C. The final concentration of different reagents was as follows: GoTaq Flexibuffer (Promega) 1×, MgCl2 2.5 mM, PCR nucleotide mix 0.2 nM of each DNTP, forward and reverse primers 1 μM of each, GoTaq (Promega) DNA polymerase 2 U, template DNA 0.2 μg (between 1.6 and 3 μL depending on the DNA extract concentration), nuclease-free water up to 20 μL. Sequencing was performed at the Genseq platform of ISE-M (Institute of Evolutionary Sciences of Montpellier) using the same primers as in initial PCR amplification. Purification was performed with an Agencourt® AMPure® PCR purification kit, following the manufacturer’s recommendations. Sequences were aligned using the Muscle program and improved manually using molecular evolutionary genetics analysis (MEGA) software [41] version 6.0. The alignments were trimmed manually using the same software. Additional 28S sequences of seven Quadriacanthus species namely Quadriacanthus kobiensis Ha, 1968 from Clarias batrachus (Linnaeus), Q. bagrae from B. docmak, Q. mandibulatus Francová & Řehulková, 2017 from Heterobranchus bidorsalis Geoffroy Saint Hilaire, Q. fornicates Francová & Řehulková, 2017, Q. zuheiri Francová & Řehulková, 2017, Q. pravus Francová & Řehulková, 2017 and Q. clariadis from C. gariepinus were retrieved for the nucleotide database GenBank (see Table 2 for accession numbers). Three species parasitizing Siluriform fish, namely Synodontella zambezensis Douëllou & Chishawa, 1995, Schilbetrema sp. and Thaparocleidus mutabilis (Gussev & Strelkov, 1960) and Onchobdella aframae Paperna, 1968 parasitizing a Cichlidae were used as the outgroup; they were obtained from GenBank. Prior to analysis, an evolutionary model was selected by MEGA 6.0 using the Bayesian information criterion (BIC). The model with the lowest BIC score was considered to better describe the pattern. Neighbor-Joining (NJ), Maximum Parsimony (MP), and Maximum Likelihood (ML) analyses were performed using MEGA version 6.0, assessing nodal support non-parametric bootstrap with 1000 replicates.

thumbnail Figure 1

Sampling locations: (1) Lake Barombi Mbo; (2) Lake Ossa; (3, 4 & 5) Nyong River, (3) Mbalmayo market, (4) Mengong, (5) Abong Mbang. A = Africa, B = Cameroon, C = Studied area.

thumbnail Figure 2

Morphometrics of Quadriacanthus spp. proposed by Gussev (1962) and modified by N’Douba et al. (1999). (A) Anchor: (a) length, (ab) base width, (e) point length; (Ap) Accessory piece length; (MCO) Male copulatory organ length; (C) Cuneus: (j) length, (i) width; (DB) Dorsal bar: (ct) center length, (h) median process length, (w) width, (x) length; (VB) Ventral bar: (w) width, (x) length; (H) Hook length; (Vg) Vaginal length; scale 20 µm.

Table 1

Measurements of the four Quadriacanthus species.

Table 2

List of the monogenean species used in this study, including their host, geographic location, accession numbers in GenBank, and the reference of their publication.

Results

The investigation of gill filaments of one osteoglossiform (Notopteridae) and three siluriform species, resulted in the record of four monogenean species. All recorded monogeneans were dactylogyrids, with anatomy corresponding to the diagnosis of Quadriacanthus given by Paperna [33], amended by Kritsky and Kulo [20] and used by Nack et al. [30] and Bahanak et al. [3]: Q. euzeti from P. afer (Prevalence = 100%, Mean Intensity = 2.5), Q. anaspidoglanii from A. macrostoma (P = 98%, MI = 3.5), Q. levequei from C. jaensis (P = 40%, MI = 1.1) and Q. barombiensis n. sp. from C. maclareni (P = 80%, MI = 4.1). Below, we present the redescription of Q. levequei due to the differences observed with the original description, and the description of Q. barombiensis n. sp. New sequences were generated from each identified species in the present study.

Quadriacanthus levequei Birgi, 1988

Type-host: Clarias pachynema Boulenger, 1909.

New host: Clarias jaensis Boulenger, 1903.

Site: gill filaments.

Type locality: Mefou near Yaoundé.

New locality: Nyong River, Mbalmayo fish market, Cameroon (3°30′48.54″ N, 11°30′04.83″ E), Sokamalem, Abong-Mbang, Cameroon (03°58′21.4″ N, 13°14′53.3″ E).

Material: 10 adult worms whole-mounted in GAP.

Voucher specimen: MRAC 43428–43429.

Redescription (Fig. 3, Table 1): Adult worms 624 (609–778) long, 113 (81–167) large at the level of ovary. Pharynx circular 39 (34–45). Dorsal bar with rectangular center with two lateral expansions, one stick-shaped median process posteriorly directed with two filaments at its end. Dorsal anchors without shaft nor handle, but with regular curved blade ending with a short point. Dorsal cunei elongated. Ventral bar V-shaped made up of two medially articulated branches. Ventral anchors with shaft and handle slightly differentiated, curved blade ending with long point. Ventral cunei triangular, smaller than dorsal ones. Seven pairs of hooks, pair IV with short handle, larger than pairs I, II, III, V, VI and VII, the latter pairs about subequal. Tubular male copulatory organ (MCO) enlarged at its basal zone and tapered at distal extremity. Accessory piece straight, slightly curved distally and ending in two small, rounded hooks, one surmounting the other. Tubular vagina showing two reduced lateral expansions at its median zone.

thumbnail Figure 3

Quadriacanthus levequei Birgi, 1988; (VA) Ventral anchor, (DA) Dorsal anchor, (AP) Accessory piece, (MCO) Male copulatory organ, (DC) Dorsal cuneus, (VC) Ventral cuneus, (DB) Dorsal bar, (VB) Ventral bar, Hooks (I–VII), (Vg) Vagina; scale 20 μm.

Remarks

The morphology of dorsal bar with rectangular center and a median expansion stick-shaped showing two filaments at its end, the one of dorsal anchor, and the size of MCO and its accessory piece (compared to the measurements taken from the original drawings, see Table 1) of the specimens recorded in the current study on C. jaensis are similar to those of Q. levequei reported on C. pachynema by Birgi [6]. The differences observed between our measurements from the newly studied specimens, those taken from original drawings and those given in the original description (i.e. the size of MCO, accessory piece [AP], dorsal bar length [DBx], dorsal bar median process length [DBh], dorsal bar center length [DBct], hooks pair four length [IV], Table 1) are more likely due to the different methods used to measure and draw these sclerotized parts.

Quadriacanthus barombiensis n. sp. Bahanak, Nack & Pariselle (Fig. 4)

urn:lsid:zoobank.org:act:0CD26701-675B-481D-85C9-BBC4EA5C92A5

thumbnail Figure 4

Quadriacanthus barombiensis n. sp. Bahanak, Nack & Pariselle; (VA) Ventral anchor, (DA) Dorsal anchor, (AP) Accessory piece, (MCO) Male copulatory organ, (DC) Dorsal cuneus, (VC) Ventral cuneus, (DB) Dorsal bar, (VB) Ventral bar, Hooks (I–VII), (Vg) Vagina; scale 20 μm.

Type-host: Clarias maclareni Trewavas, 1962.

Site: gill filaments.

Type locality: Lake Barombi Mbo, Cameroon (4°38′ N, 9°22′ E).

Material: 30 adult worms whole-mounted in GAP.

Type specimens: holotype: MRAC 43425 and paratypes: MRAC 43426–43427.

Etymology: Epithet barombiensis refers to the type locality.

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 [17].

Description

Adult worms 579 (410–730) long, 148 (102–208) large at level of ovary. Pharynx circular 30 (27–33). Dorsal bar with rectangular center, two lateral branches, stick-shaped median process with small circular median hole, and ending with two filaments. Dorsal anchor without handle nor guard, with regular curved thin blade and short point. Ventral bar V-shaped made up of two lateral medially articulated expansions. Ventral anchor with a blade curved in an arc and ending in a long point. Ventral and dorsal cunei triangular, dorsal cuneus being larger than ventral one (see Table 1). Seven pairs of hooks, pair IV with short and pear-shaped handle, larger than pairs I, II, III, V, VI and VII, the latter pairs about subequal. Tubular MCO large at basal zone and tapered at distal extremity, accessory piece slightly S-shaped ending in one small point. Vagina not observed.

Remarks

By its general morphology of haptoral structures and MCO: the stick shape of dorsal bar median process (1), tubular shape of MCO enlarged at basal zone and tapered at distal end (2), and s-shape of accessory piece (3), Q. barombiensis n. sp. resembles Q. levequei, Q. anaspidoglanii and Q. euzeti; but it can easily be distinguished from its congeners by: the morphology of the distal extremity of the accessory piece with one small hook versus two small hooks in Q. levequei (1), the dorsal bar postero-median process with two filaments versus none in Q. euzeti and Q. anaspidoglanii (2); the vagina not sclerotized versus sclerotized in Q. levequei, Q. euzeti and Q. anaspidoglanii (3), and (4) the mean size of sclerotized parts: i.e. MCO (28 vs. 38 in Q. levequei, 34.2 in Q. anaspidoglanii, and 37.8 in Q. euzeti), accessory piece (23 vs. 33, 28.7 and 29.1), dorsal cunei (j = 12 vs. 17, 14 and 18.6), ventral bar (x = 49 vs. 54, 40.9 and 55.7).

Principal component analysis (PCA)

PCA performed on the standardized measurements of sclerotized parts of haptor and MCO of the four newly studied species, namely Q. euzeti, Q. levequei, Q. anaspidoglanii and Q. barombiensis n. sp., shows four well-defined clusters (63.90% of variance on axes 1 and 2). Specimens of Q. barombiensis n. sp. and Q. euzeti formed two isolated and clearly separated groups; however, a small overlapping zone is observed between specimens of Q. anaspidoglanii and Q. levequei (Fig. 5A). Both species are separated by axis 1 and 3 (Fig. 5B). The most represented variables and their coordinates are: ventral anchor length (VAa = −0.96), dorsal anchor base width (DAab = −0.96), dorsal anchor length (DAa = −0.95), dorsal bar length (DBx = −0.94), dorsal cunei length (DCj = −0.92), ventral cunei length (VCj = −0.91) on axis 1; hook pair five and six length (V = −0.8, VI = −0.71) on axis 2 (Fig. 5C) and ventral anchor point length (VAe = 0.84), dorsal bar median process length (DBh = 0.72) on axis 3 (Fig. 5D).

thumbnail Figure 5

Principal component analysis scatterplot of 10 Quadriacanthus specimens of each of the following species: Quadriacanthus euzeti from Papyrocranus afer, Quadriacanthus barombiensis n. sp. from Clarias maclareni, Quadriacanthus anaspidoglanii from Anaspidoglanis macrostoma and Quadriacanthus levequei from Clarias jaensis. A: axes 1 and 2, B: axes 1 and 3. C and D: scatterplot of variable along axis 1 and 2 and axis 1 and 3, respectively. Dorsal anchor: (DAa) length, (DAab) base width, (DAe) point length. Ventral anchor: (VAa) length, (VAab) base width, (VAe) point length. (Ap) Accessory piece length, (MCO) Male copulatory organ length. Cuneus: (Cj) length, (Ci) width. (DB) Dorsal bar: (DBct) center length, (DBh) median process length, (DBw) width, (DBx) length. Ventral bar: (VBw) width, (VBx) length. (I–VII) Hook length.

Phylogenetic analysis

After trimming, the alignment of 616 positions (base pairs) was obtained, among these positions 335 variable sites were identified, 184 of which were parsimony informative. TN93 + G was selected as the best fit for our data. The analysis based on three different methods (NJ, MP and ML) produced a congruent tree topology (Fig. 6). All the Quadriacanthus spp. appeared clustered in one monophyletic group. Quadriacanthus kobiensis (Asian species) is well separated from African Quadriacanthus spp. and situated at the basal position of the tree. Considering African Quadriacanthus spp., two well-defined clusters were observed with high support. The first cluster (I) was formed by Q. bagrae, Q. clariadis, Q. fornicatus, Q. mandibulatus, Q. pravus and Q. zuheiri with high support. Within this cluster, Q. bagrae was sister species to Q. clariadis with high support. The second cluster (II) was formed by Q. levequei, Q. euzeti, Q. barombiensis and Q. anaspidoglanii with high support. Within this second cluster, Q. euzeti is separated from the other three Quadriacanthus spp. among which Q. anaspidoglanii was sister species to Q. barombiensis n. sp. and Q. levequei, both latter species being separated by 1% of Gamma-corrected genetic distance (Table 3, Fig. 6).

thumbnail Figure 6

Consensus tree based on Neighbor-Joining, Maximum Parsimony and Maximum Likelihood for 28S rDNA (616 bp). Numbers indicated above the branches correspond to bootstrap values NJ/MP/ML, respectively obtained after 1000 iterations.

Table 3

Matrix of Gamma-corrected pairwise distances (in %) between 28S rDNA sequences of 616 bp length of the 15 dactylogyridean species.

Discussion

Quadriacanthus barombiensis n. sp. is specific to C. maclareni, i.e. oioxenous [10], as is the case for the majority of known Quadriacanthus species [2, 3, 6, 2729, 30, 45]. Quadriacanthus levequei was previously described from the gills of C. pachynema and considered oioxenous [6]; its new record on one congeneric host (C. jaensis) changes its host specificity status from oioxenous to stenoxenous [12], even better mesostenoxenous [9]. This enlargement of the host spectrum of Q. levequei in the Nyong River Basin may have been promoted by relative phylogenetic proximity [21, 38] of C. jaensis and C. pachynema and/or local ecological conditions in the environment [30, 35]. According to Teugels [43], C. maclareni is morphologically close to C. jaensis and both species belong to sub-genus Clarias (Platycephaloides), but contrary to C. jaensis which hosts four dactylogyridean species, namely Q. dageti Birgi, 1988, Q. teugelsi, Q. nyongensis Birgi, 1988 and Birgiellus calaris Bilong Bilong, Nack and Euzet, 2007 [5], C. maclareni hosts only one species: Q. barombiensis n. sp. We assume that when the ancestor of C. maclareni colonized Lake Barombi Mbo from the Memé River system, which played a major role in fish colonization of this lake [31, 44], it could have hosted (1) several monogenean species, which have been lost due to environmental changes or following bottleneck events [37], or (2) only the ancestor of Q. barombiensis n. sp. Clarias maclareni being endemic in this Cameroonian volcanic line crater lake which shelters a Cichlid species flock [44], without parasite lateral transfer and/or intra-host speciation (synxenic [10]) favored by host population fragmentation, no increase of monogenean species richness has been possible [37, 46]. The close relationship between host species: C. maclareni and C. jaensis (see Teugels op. cit.), and their respective parasite species: Q. barombiensis n. sp. and Q. levequei (see Table 3 and Fig. 6), is a good illustration of a co-vicariance followed by the co-speciation of both fish and their Monogeneans [7]. Quadriacanthus euzeti, Q. anaspidoglanii, Q. levequei, and Q. barombiensis n. sp. (Cameroonian species, Guinean ichthyofaunan province) nested in cluster II, while Q. bagrae, Q. clariadis, Q. fornicatus, Q. pravus, Q. zuheiri and Q. mandibulatus (East African species, nilo-soudanian ichthyofaunan province) nested in cluster I. Nack et al. [30] did not succeed in determining whether the lateral transfer of Q. euzeti on P. afer (Notopteridae) originated from a Clariidae or from a Bagridae host species. The current study shows that this host switch originated from a Clariidae, presumably C. jaensis, and early took place before the speciation of other Cameroonian Quadriacanthus (Q. anaspidoglanii, Q. levequei and Q. barombiensis n. sp.). This type of phenomenon (transfer from a distant host family) has been recorded by Messu Mandeng et al. [26] in Cameroon, where Cichlidogyrus Paperna, 1960 usually found on cichlid hosts transferred to a cyprinodontiform host. In addition, the basal position of Q. kobiensis, parasite of Clarias batrachus (Linnaeus) from Asia (where African clariids originate [1]), suggests that members of Clariidae are ancestral hosts of Quadriacanthus spp. [13] and that African Quadriacanthus species have an Asian origin too (which was suggested by Pariselle et al. [37] based on the presence of additional sclerites (cunei) associated with the anchors in Asian Siluriform monogeneans and Quadriacanthus species). Quadriacanthus euzeti, Q. anaspidoglanii and Q. bagrae from non-clariid hosts are distinguished from their close congeners (Q. levequei for the two first species and Q. clariadis for Q. bagrae) hosted by clariid species, by the morphology and size of sclerotized parts of the haptor, while the copulatory organs look similar [2, 13, 20, 30, 34]: e.g. the dorsal and ventral anchor blade length, the thickness of ventral bar and the length of dorsal cunei are always reduced in Q. anaspidoglanii, while they are bigger in Q. euzeti; Francová et al. [13] highlight that Q. bagrae differs from Q. clariadis by the length of the ventral bar and the size of dorsal anchor blade, longer in Q. clariadis. This observation supports the adaptive nature of haptoral hard parts which are subject to selective pressure [16] such as gill morphology, encountered by these different Quadriacanthus spp. parasitizing distant hosts [26, 40].

Acknowledgments

The authors thank: Maarten Vanhove for his help during the phylogenetic analysis of molecular data, Michiel Jorissen for his help in depositing type-specimens at the museum; the editor and the two anonymous referees for their valuable comments.

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Cite this article as: Bahanak D-N-D, Mbondo JA, Bassock Bayiha ED, Pariselle A, Nack J, Bilong Bilong CF & Agnèse J-F. 2022. Description of a new species from Clarias maclareni and phylogenetical analysis of Quadriacanthus (Monogenea, Dactylogyridae) species transfers between clariid and non-clariid fish hosts in Cameroon. Parasite 29, 37.

All Tables

Table 1

Measurements of the four Quadriacanthus species.

Table 2

List of the monogenean species used in this study, including their host, geographic location, accession numbers in GenBank, and the reference of their publication.

Table 3

Matrix of Gamma-corrected pairwise distances (in %) between 28S rDNA sequences of 616 bp length of the 15 dactylogyridean species.

All Figures

thumbnail Figure 1

Sampling locations: (1) Lake Barombi Mbo; (2) Lake Ossa; (3, 4 & 5) Nyong River, (3) Mbalmayo market, (4) Mengong, (5) Abong Mbang. A = Africa, B = Cameroon, C = Studied area.

In the text
thumbnail Figure 2

Morphometrics of Quadriacanthus spp. proposed by Gussev (1962) and modified by N’Douba et al. (1999). (A) Anchor: (a) length, (ab) base width, (e) point length; (Ap) Accessory piece length; (MCO) Male copulatory organ length; (C) Cuneus: (j) length, (i) width; (DB) Dorsal bar: (ct) center length, (h) median process length, (w) width, (x) length; (VB) Ventral bar: (w) width, (x) length; (H) Hook length; (Vg) Vaginal length; scale 20 µm.

In the text
thumbnail Figure 3

Quadriacanthus levequei Birgi, 1988; (VA) Ventral anchor, (DA) Dorsal anchor, (AP) Accessory piece, (MCO) Male copulatory organ, (DC) Dorsal cuneus, (VC) Ventral cuneus, (DB) Dorsal bar, (VB) Ventral bar, Hooks (I–VII), (Vg) Vagina; scale 20 μm.

In the text
thumbnail Figure 4

Quadriacanthus barombiensis n. sp. Bahanak, Nack & Pariselle; (VA) Ventral anchor, (DA) Dorsal anchor, (AP) Accessory piece, (MCO) Male copulatory organ, (DC) Dorsal cuneus, (VC) Ventral cuneus, (DB) Dorsal bar, (VB) Ventral bar, Hooks (I–VII), (Vg) Vagina; scale 20 μm.

In the text
thumbnail Figure 5

Principal component analysis scatterplot of 10 Quadriacanthus specimens of each of the following species: Quadriacanthus euzeti from Papyrocranus afer, Quadriacanthus barombiensis n. sp. from Clarias maclareni, Quadriacanthus anaspidoglanii from Anaspidoglanis macrostoma and Quadriacanthus levequei from Clarias jaensis. A: axes 1 and 2, B: axes 1 and 3. C and D: scatterplot of variable along axis 1 and 2 and axis 1 and 3, respectively. Dorsal anchor: (DAa) length, (DAab) base width, (DAe) point length. Ventral anchor: (VAa) length, (VAab) base width, (VAe) point length. (Ap) Accessory piece length, (MCO) Male copulatory organ length. Cuneus: (Cj) length, (Ci) width. (DB) Dorsal bar: (DBct) center length, (DBh) median process length, (DBw) width, (DBx) length. Ventral bar: (VBw) width, (VBx) length. (I–VII) Hook length.

In the text
thumbnail Figure 6

Consensus tree based on Neighbor-Joining, Maximum Parsimony and Maximum Likelihood for 28S rDNA (616 bp). Numbers indicated above the branches correspond to bootstrap values NJ/MP/ML, respectively obtained after 1000 iterations.

In the text

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