Abstract
Parasite biodiversity of fish of the southern part of the Mediterranean sea is still incompletely explored. We describe here Microcotyle visa n. sp. from the gill filaments of the bluespotted seabream Pagrus caeruleostictus (Valenciennes) (Sparidae) collected off the Algerian coast. The identity of fish hosts was confirmed by barcoding. Microcotyle visa n. sp. is herein described and illustrated. Analysis of the cox1 gene of the monogeneans revealed minor intraspecific variation (1.4%), an order of magnitude lower than the distance between this species and other Microcotyle species (10–15 %). Microcotyle visa n. sp. is distinguished from Microcotyle erythrini van Beneden & Hesse, 1863, a congener infesting sparids, on the basis of morphological (size of clamps, number of testes) and molecular (cox1) differences. This is the fourth member of the genus known to parasitise a sparid host. A species of Paramicrocotyle sp. included in the molecular analysis was nested within a robust Microcotyle + Paramicrocotyle clade; in the absence of demonstrated molecular and morphological differences, we consider that Paramicrocotyle Caballero & Bravo-Hollis, 1972 is a junior synonym of Microcotyle van Beneden & Hesse, 1863 and transfer two species of Paramicrocotyle as Microcotyle danielcarrioni (Martinez & Barrantes, 1977) n. comb. and Microcotyle moyanoi (Villalba & Fernandes, 1986) n. comb.
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Introduction
The Microcotylidae Taschenberg, 1879 is one of the largest families of polyopisthocotylean monogeneans. It has received much attention by taxonomists (Dillon & Hargis, 1965; Mamaev, 1986; Tripathi, 1956; Unnithan, 1971). Still, the specific composition and status of some genera remain unclear (Mamaev, 1986). Tripathi (1956), in an early effort, arranged the species of the genus Microcotyle van Beneden & Hesse, 1863 into four subgenera: Microcotyle Tripathi, 1956, Bispina Tripathi, 1956, Vaginaespina Tripathi, 1956 and Aspina Tripathi, 1956, based on the characters of the cirrus and vagina (Tripathi, 1956). Dillon & Hargis (1965), in light of the insufficiency of the older literature and of Tripathiʼs systematic work as he omitted certain species unquestionably belonging to Microcotyle, found only little merit to his arrangement (Dillon & Hargis, 1965). Unnithan (1971) as well, considered Tripathiʼs subdivision of Microcotyle to be “too arbitrary” to be adopted without considerable modification (Unnithan, 1971), and erected several subfamilies. Mamaev (1977) considered that, regardless of some positive results of Unnithan’s work, his attempt “to eliminate ambiguities as far as possible” (Unnithan, 1971) “failed and caused only additional confusion” (Mamaev, 1977); he rejected all Unnithan’s subfamilies, and recognised only five of his 13 new genera, with a need of critical review of specific composition of four of them (Mamaev, 1977). Mamaev (1986) revised again the family and proposed eight subfamilies, 39 genera and 150 species (Mamaev, 1986).
During the 21st century, new genera (Omanicotyle Yoon, Al-Jufaili, Freeman, Bron, Paladini & Shinn, 2013, Paranaella Kohn, Baptista-Farias & Cohen, 2000) (see Kohn et al., 2000; Yoon et al., 2013) and species [Microcotyle algeriensis Ayadi, Gey, Justine & Tazerouti, 2017, M. argenticus Hadi & Bilqees, 2011, M. rubrum Hadi & Bilqees, M. jonii Hadi, Bilqees & Khatoon, 2011, M. omanae Machkewskyi, Dmitrieva, Al-Jufaili & Al-Mazrooei, 2013 and Polylabris bengalensis Sailaja & Madhavi, 2011] have been added to this family (Hadi & Bilqees 2010, 2011; Hadi et al., 2011; Sailaja & Madhavi, 2011; Machkewskyi et al., 2013; Ayadi et al., 2017).
Within the Microcotylidae, Microcotyle is the largest genus and has been considered one of the most difficult genera of Monogenea (see Sproston, 1946). Several attempts have been made to subdivide this genus (Unnithan, 1971 [1967]; Mamaev, 1977, 1986). Currently, WoRMS list about 60 valid species (WoRMS, 2018). As for other monogeneans, it is likely that studies integrating both morphology and molecules are necessary to elucidate phylogenetic relationships and limits between species.
Recent studies have shown that the biodiversity of monogeneans of marine fish in the southern part of the Mediterranean is far from being completely known (Chaabane et al., 2015, 2016a, b, 2017; Chaari et al., 2016; Kheddam et al., 2016; Boudaya & Neifar, 2016; Ayadi et al., 2017). In the course of a parasitological study of monogeneans of sparid fishes off the Algerian coast, we collected representatives of an undescribed species of Microcotyle on the gills of Pagrus caeruleostictus. The species is described here.
Materials and methods
Fishes
During 2016 and 2017, 73 Pagrus caeruleostictus were collected at Zemmouri El Bahri (36°48′4.58″N, 3°34′7.01″E) off the Algerian coast. Fish specimens were transferred to the laboratory shortly after capture and identified using keys (Fischer et al., 1987). Gills were removed from each fish and observed under microscope for the presence of monogeneans.
Morphological methods
Monogeneans were removed alive from gills using fine dissection needles, then fixed in 70% ethanol, stained with acetic carmine, dehydrated in graded ethanol series (70, 96 and 100%), cleared in clove oil, and mounted in Canada balsam. Some specimens were mounted in Berleseʼs fluid to study the morphology of clamps and the genital atrium. Drawings were made with the help of an Olympus BH-2 microscope equipped with a drawing tube. Drawings were scanned and redrawn on a computer with Adobe Illustrator. Measurements are in micrometres, and indicated as the range followed by the mean ± standard deviation (for n > 30) and the number of measurements in parentheses; measurements of the holotype are also indicated.
Molecular methods
To ensure that hosts and monogenean were labelled with respect of host-parasites relationships we followed Justine et al. (2013) and Ayadi et al. (2017). Specimens of Microcotyle sp. were extracted from the same host fish, and a tissue sample from the gills of the fish was taken. The extracted monogeneans were cut in three parts using a scalpel blade. Their anterior parts (which include the genital atrium) and posterior parts (which include the haptor) were mounted (both parts on a single slide) for drawing and deposition in a museum; their median parts were fixed in absolute ethanol then subjected to molecular analyses. Three specimens were analysed.
Molecular barcoding of fish
Total genomic DNA was isolated using QIAamp DNA Mini Kit (Qiagen, Courtaboeuf, France) as per the manufacturer’s instructions. The 5′ region of the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene was amplified with the primers FishF1 (5′-TCA ACC AAC CAC AAA GAC ATT GGC AC-3′) and FishR1 (5′-TAG ACT TCT GGG TGG CCA AAG AAT CA-3′) (Ward et al., 2005). PCR reactions were performed in a total volume of 20 μl, containing 1 ng of DNA, 1× CoralLoad PCR buffer, 3 mM MgCl2, 66 μM of each dNTP, 0.15 μM of each primer and 0.5 units of Taq DNA polymerase (Qiagen). The amplification protocol was 4 min at 94°C, followed by 40 cycles at 94°C for 30 s, 48°C for 40 s, and 72°C for 50 s, with a final extension step at 72°C for 7 min. PCR products were purified (Ampure XP Kit, Beckman Coulter, Brea, USA) and sequenced in both directions on a 3730xl DNA Analyzer 96-capillary sequencer (Applied Biosystems, Foster City, USA). We used CodonCode Aligner version 3.7.1 software (CodonCode Corporation, Dedham, MA, USA) to edit the sequence, which was 652 bp in length, compared it to the GenBank database content with BLAST, and deposited it in GenBank under the accession number MK275650. Species identification was confirmed with the BOLD identification engine (Ratnasingham & Hebert, 2007).
cox1 sequences of monogeneans
Total genomic DNA was isolated using QIAmp DNA Micro Kit (Qiagen). The specific primers JB3 (=COIASmit1) (forward 5′-TTT TTT GGG CAT CCT GAG GTT TAT-3′) and JB4.5 (=COI-ASmit2) (reverse 5′-TAA AGA AAG AAC ATA ATG AAA ATG-3′) were used to amplify a fragment of 424 bp of the cox1 gene (Bowles et al., 1995; Littlewood et al., 1997). PCR reaction was performed in 20 μl, containing 1 ng of DNA, 1× CoralLoad PCR buffer, 3 mM MgCl2, 0.25 mM dNTP, 0.15 μM of each primer, and 0.5 units of Taq DNA polymerase (Qiagen). Thermocycles consisted of an initial denaturation step at 94°C for 2 min, followed by 37 cycles of denaturation at 94°C for 30 s, annealing at 48°C for 40 s, and extension at 72°C for 50 s. The final extension was conducted at 72°C for 5 min. Sequences were edited with CodonCode Aligner software version 3.7.1 (CodonCode Corporation, Dedham, MA, USA), compared to the GenBank database content with BLAST, and deposited in GenBank under the accession numbers MK27652-MK27654.
Trees and distances
All available sequences for Microcotyle spp. available on GenBank, and one sequence of Paramicrocotyle sp., were included in the phylogenetic analyses (Table 1). Sequences of Bivagina pagrosomi (Murray, 1931) and Polylabris halichoeres Wang & Zhang, 1998 were used as the outgroup. The trees were inferred using the neighbour-joining (NJ) and maximum likelihood (ML) methods using MEGA7 (Kumar et al., 2016). For the latter, the best model, estimated by MEGA7, was the Hasegawa-Kishino-Yano model (Hasegawa et al., 1985) with discrete Gamma distribution (HKY + G). Genetic distances [p-distance and Kimura 2-parameter distance (Kimura, 1980)] were estimated with MEGA7. All codon positions were used.
Results
Molecular identification of fish
The provisional identification of fish species using morphological characteristics was challenged by DNA barcoding approach. BLAST analysis of the cox1 sequences of fish specimens examined in the present study with sequences in the GenBank and BOLD databases showed sequence similarity values of 99% for Pagrus caeruleostictus, thus confirming the identification of the hosts.
Molecular characterisation of monogeneans
The cox1 sequences of Microcotyle visa n. sp. were aligned with 10 other microcotylid sequences. The neighbour-joining and maximum likelihood methods led to similar tree topologies and thus only the NJ tree is shown (Fig. 1). All species included in Microcotyle and Paramicrocotyle formed a monophyletic clade separated from the outgroups (84% bootstrap in NJ, 75% in ML) and the species of Paramicrocotyle was nested within the Microcotyle + Paramicrocotyle clade. The three sequences for the new species grouped as a robust clade (100% bootstrap support in NJ, 98% in ML) within the Microcotyle + Paramicrocotyle clade. Another clade with high support included the two species of Microcotyle from scorpaeniform fishes, Microcotyle algeriensis ex Scorpaena notata Rafinesque and Microcotyle sp. ex Helicolenus dactylopterus (Delaroche) (100% bootstrap support in NJ). The support for other branches was generally low.
Neighbour-Joining tree (p-distance method) based on an analysis of cox1 sequence data for Microcotyle spp. Bootstraps percentages (1,000 replicates) are indicated next to the branches (only values > 70% are shown). There were a total of 294 positions in the final dataset. The Maximum Likelihood tree had similar topology and is not presented
Distances were computed using p-distance and Kimura 2-parameter distance. The differences were minor so only p-distances are commented here. Two sequences for M. visa n. sp. were identical differed by 1.4% from the third. Distances between these sequences of M. visa n. sp. and the other species ranged between 14.3–15.0% (Microcotyle erythrini) and 10.2–13.9% (remaining species) (Table 2). These distances, and the tree, clearly indicate that the new species is distinct from all species of Microcotyle and Paramicrocotyle for which sequence data are available, and especially that it is distinct from M. erythrini. Intraspecific distances within M. visa n. sp. were an order of magnitude inferior to the interspecific distances (1.4% vs 10.2–15.0%).
Family Microcotylidae Taschenberg, 1879
Genus Microcotyle van Beneden & Hesse, 1863
Microcotyle visa n. sp.
Type-host: Pagrus caeruleostictus (Valenciennes) (Perciformes: Sparidae), blue-spotted seabream.
Type-locality: Off Zemmouri el Bahri (36°48′4.58″N, 3°34′7.01″E), Algerian coast of the Western Mediterranean.
Site on host: Gills.
Type-specimens: Holotype (MNHN HEL850) and 50 paratypes (MNHN HEL851-HEL900), including three with molecular information, are deposited in the collections of the Muséum National d’Histoire Naturelle, Paris (MNHN). Paratypes with molecular information: anterior and posterior parts of specimens mounted together on slide, median part used for molecular analysis: specimen MO01, slide MNHN HEL851; specimen MO02, slide MNHN HEL852; specimen MO03, slide MNHN HEL853.
Representative DNA sequences: cox1 gene: GenBank MK27652 (paratype MO01, MNHN HEL851); MK27653 (paratype MO02, MNHN HEL852); GenBank MK27654 (paratype MO03, MNHN HEL853).
ZooBank registration: To comply with the regulations set out in article 8.5 of the amended 2012 version of the International Code of Zoological Nomenclature (ICZN, 2012), details of the new species have been submitted to ZooBank. The Life Science Identifier (LSID) for Microcotyle visa n. sp. is urn:lsid:zoobank.org:act: EA3F6DB0-1DBB-4C9C-9A01-50BB4EE666AA.
Etymology: The species name, visa, refers to the joy of the first author when she obtained her visa from the French administration after a long period of uncertainty. Invariable, treated as a noun in apposition.
Description (Figs. 2, 3)
[Based on 31 specimens] Body elongate, anterior end narrow, length of body proper 1,300–4,000 (1,998) (n = 31) (holotype: 2,200), total length 1,910–4,620 (2,737 ± 668) (n = 31) (holotype: 3,000); width at level of ovary 270–1,000 (500 ± 182) (n = 31) (holotype: 600). Haptor subsymmetrical or symmetrical, 250–1,250 (739) (n = 31) (holotype: 800) long, armed with 59–126 (100) (n = 20) (holotype: 94) clamps. Clamps of microcotylid type, arranged in 2 equal or sub-equal rows; length of clamps 25–60 (35) (n = 31), width 12–35 (21) (n = 31).
Microcotyle visa n. sp. ex Pagrus caeruleostictus. A, Holotype, whole body; B, Holotype, spines of genital atrium; C, Egg; D–F, Clamp (D, lower part, E, upper part, F, both parts superposed)
Microcotyle visa n. sp. ex Pagrus caeruleostictus, paratypes with associated molecular information. A, B, Paratype MNHN HEL852 (GenBank: MK27653); C, D, Paratype MNHN HEL851 (GenBank: MK27652)
Pair of oval septal organs septate, elongate-oval, 30–85 × 20–60 (47 × 32) (n = 31) (holotype: 45 × 35). Pharynx subspherical, 20–55 × 20–45 (30 × 27) (n = 31) (holotype: 30 × 30). Intestine bifurcates at level of genital atrium. Caeca with numerous lateral and medial diverticula, apparently fuse just anterior to haptor, left branch extends into haptor.
Testes 14–29 (23) (n = 29) (holotype: 29) in number, post-ovarian, occurring in 2 rows generally, intercaecal, in posterior half of body proper. Vas deferens conspicuous, runs in midline to genital atrium. Genital atrium at 120–600 (220) (n = 31) (holotype: 205) from anterior extremity of body, length 50–130 (74) (n = 31), width 45–95 (63) (n = 31). Genital atrium comprises anterior atrium proper and two posterior “pockets”. Atrium proper roughly shaped as inverted heart, bearing numerous [142–224 (189) (n = 12)] conical spines of similar sizes; spines apparently more dense in centre than in lateral parts. Variation in focus shows that the lumen of the atrium proper has two lateral expansions. Posterior pockets lined with spines similar to that of atrium proper, 18–39 (28) (n = 12). Total number of spines 172–262 (218) (n = 12). Genital pore middorsal.
Vaginal pore visible in most specimens, mediodorsal, posterior to genital atrium; distance from vagina to anterior extremity 320–780 (553) (n = 30). Canal from vagina to posterior part of female organs not seen. Ovary complex, begins at level of anteriormost testes, continues anteriorly in midline, reflexes at level of confluence of vitelline ducts, reflexes again toward anterior extremity, forms large anterior curve and reflexes a last time posteriorly and ends as oviduct. Oötype spindle-shaped, with posterior Mehlisʼ gland. Seminal receptacle well visible, lateral. Canal from vagina not seen. Genitointestinal canal visible in some specimens. Precise junctions between oviduct, oötype, vitelline duct and genitointestinal canal not elucidated.
Vitellarium extends in most part of body from genital atrium to haptor. Vitelline ducts pair, united anteriorly and posteriorly; anterior junction visible only in some specimens; posterior junction conspicuous as an Y in most specimens, at level of ovary and ventral to it.
Egg fusiform, 157–260 × 60–100 (195 × 71) (n = 12), with 2 filaments, often coiled, 157–260 (195) (n = 12) long.
Discussion
Differential diagnosis for Microcotyle visa n. sp.
In the following paragraphs, we compare the new species with Microcotyle spp. previously recorded from the Mediterranean (Table 3), then with Microcotyle spp. from sparid hosts (Table 3); to lighten the text, references in tables are not repeated here.
Comparison with species from the Mediterranean
Microcotyle visa n. sp. has in common with M. algeriensis the same shape of the genital atrium with two posterolateral “pockets” but differs in possessing a greater number of clamps which are also smaller, smaller genital atrium, greater number of testes and greater number of atrial spines (Table 3). Although the two species were described from the same type-locality, the hosts are different (Pagrus caeruleostictus vs Scorpaena notata, Scorpaenidae).
Microcotyle visa n. sp. has in common with Microcotyle sp. of Ayadi et al. (2017) the general organisation of the genital atrium but differs in having a greater number of clamps and a greater number of atrial spines and testes (Table 3). The hosts are also different (Helicolenus dactylopterus (Sebastidae) for Microcotyle sp.).
Apart from the above, the new species can be differentiated from the other species described in the Mediterranean by the presence of two lateral expansions in the genital atrium (vs not mentioned in other species).
Microcotyle visa n. sp. differs from M. lichiae Ariola, 1899 by the arrangement of spines in the atrium (5 concentric rows in M. lichiae; unfortunately, never redescribed since the original description). The host is also different (Lichia amia, Carangidae) (Table 3).
Microcotyle visa n. sp. differs from M. pomatomi Goto, 1899 by the smaller number of clamps, clamp size, larger genital atrium and a smaller number of testes (Table 3). This species is allegedly present in the Mediterranean (Euzet et al., 1993) but measurements are available only for specimens from the Atlantic (Table 3). The host is Pomatomus saltatrix (Pomatomidae), a fish with circumglobal distribution.
Microcotyle visa n. sp. differs from M. donavini van Beneden & Hesse, 1863 from Symphodus mediterraneus (Linnaeus) by the presence of two lateral expansions in the genital atrium, the larger number of clamps, smaller clamps size, smaller pharynx and genital atrium and a greater number of testes. Microcotyle donavini is allegedly present in the Mediterranean (Euzet et al., 1993) but measurements are available only for specimens from the Atlantic (Table 3) from the host Labrus bergylta (Labridae).
Distinguishing Microcotyle visa n. sp. from M. erythrini van Beneden & Hesse, 1863, a parasite of sparids, was a more difficult task. The two species share similarities such as locality (Algeria, Mediterranean Sea), host family (Sparidae), shape of genital atrium (especially the presence of two lateral expansions) and maximum number of clamps (Table 3). However, Microcotyle visa n. sp. can be differentiated from M. erythrini by the smaller clamps size, a larger pharynx and a greater number of testes. Our molecular analysis showed that the distance between the cox1 sequences of both species was 14%, strongly suggesting that the species are distinct.
Comparison with species from sparids not from the Mediterranean
Microcotyle visa n. sp. resembles M. omanae in the armament of the genital atrium and the number of clamps as well as their size. However, Microcotyle visa n. sp. differs from M. omanae by its distant location (Indian Ocean vs Mediterranean Sea), the presence of two lateral expansions in the atrium, and the smaller number of testes. Hosts are also different (Cheimerius nufar for M. omanae) (Table 4).
Microcotyle visa n. sp. resembles M. archosargi MacCallum, 1913 in the number of clamps and testes as well as the size of the genital atrium but differs by its locality (Off Algeria, Mediterranean Sea vs off New York, Western Atlantic) and host (P. caeruleostictus vs Archosargus probatocephalus (Walbaum)) as well as by the smaller clamp size and the shape and armature of genital atrium as the two lateral expansions and pockets are absent in M. archosargi (Table 4).
Species of Microcotyle from sparids
Sparid hosts are known to be parasitised with microcotylids. Eleven species recovered from sparids have been originally described as members of Microcotyle but have been transferred to other genera: Bivagina alcedinis (Parona & Perugia, 1889) Yamaguti, 1963; Sparicotyle chrysophrii (van Beneden & Hesse, 1863) Mamaev, 1984; Bivagina pagrosomi (Murray, 1931) Dillon & Hargis, 1965; Neobivagina canthari (van Beneden & Hesse, 1863) Dillon & Hargis, 1965; Pagellicotyle mormyri (Lorenz, 1878) Mamaev, 1984; Atrispinum salpae (Parona & Perugia, 1890); and Atrispinum sargi (Parona & Perugia, 1890) Euzet & Maillard, 1974 (see van Beneden & Hesse, 1863; Parona & Perugia, 1890; Yamaguti, 1963; Dillon & Hargis, 1965; Mamaev, 1984).
Only three monogenean species described from sparid hosts are still considered members of Microcotyle: M. omanae from Cheimerius nufar; M. archosargi from Archosargus probatocephalus; and M. erythrini from Pagellus erythrinus (see van Beneden & Hesse, 1863; MacCallum, 1913; Machkewskyi et al., 2013). Only the latter species occurs in the Mediterranean. Our study increases the number of Microcotyle spp. infecting sparid hosts up to four.
Microcotyle erythrini is exceptional by its wide host range and relatively large geographical distribution ranging from the Mediterranean to the Atlantic. Records in the Atlantic include off France (van Beneden & Hesse, 1863) and off Spain (Pérez-del-Olmo et al., 2007a, b); records in the Mediterranean include a number of localities (Parona & Perugia, 1890; Ulmer & James, 1981; Kouider El Ouahed-Amine, 1998; Jovelin & Justine, 2001; Pérez-del Olmo et al., 2007a, b; Fernandez-Jover et al., 2010; Strona et al., 2010; Marzoug et al., 2012; Akmirza, 2013; Papoutsoglou, 2016), from different host species, mainly sparids. Monogeneans are often considered to be strictly host-specific and this situation is puzzling. It is likely that the specific status of the M. erythrini-like specimens infecting sparid hosts would change if a detailed morphological and molecular study is performed.
Intraspecific morphometric and molecular variability in polyopisthocotylean monogeneans
In the course of our study, we found some variability in several measurements of the “soft” parts within our new species, but measurements of “hard” parts (clamps) and counts of organs, either hard (clamps, atrium spines) or soft (testes) did not differ significantly. A molecular study of the cox1 gene, unfortunately limited to a small number of samples, showed that the intraspecific distance was low (1.4%), especially when compared with distances between established species (10.2–15.0%). Intraspecific variations in body size in polyopisthocotylean monogeneans are well known, and the literature contains many examples of authors discussing artefacts of fixation and effect of flattening on the size of organs (Goto, 1894; Sproston, 1946; Justine, 2011; Machkewskyi et al., 2013). In Table 5, we compiled published results concerning the intraspecific differences of cox1 sequences. The difference found in the present specimens (1.4%) falls well within the intraspecific range found by various authors, thus confirming that a single species, here described as M. visa was present in our specimens.
The genus Paramicrocotyle Caballero & Bravo-Hollis, 1972
Caballero & Bravo-Hollis erected Paramicrocotyle Caballero & Bravo-Hollis 1972 for P. atriobursata Caballero & Bravo-Hollis, 1972 and P. tampicensis Caballero & Bravo-Hollis, 1972 (see Caballero y Caballero & Bravo-Hollis, 1972). They distinguished Paramicrocotyle from Microcotyle by the following features: structure of the haptor, structure and shape of the genital atrium and the presence of two vitello-vaginal pouches. They placed in their newly erected genus 16 species previously belonging to the genus Microcotyle. Later, Mamaev (1986) synonymised Paramicrocotyle with Microcotyle, and Paramicrocotyle was considered taxon inquirendum by Mendoza-Garfias et al. (2017).
Based on morphological similarities between the two genera (Table 6), we follow Mamaev (1986) and consider Paramicrocotyle a junior synonym of Microcotyle. Moreover, our molecular study included a member of Paramicrocotyle, which was placed amongst several species of Microcotyle without having a distinct branch, and the Microcotyle + Paramicrocotyle clade was well supported. Mamaev (1986) did not change the generic status of P. danielcarrioni Martinez & Barrantes, 1977 (probably omitted) nor that of P. moyanoi Villalba & Fernandes, 1986 (described simultaneously to his study) (see Martinez & Barrantes, 1977; Villalba & Fernández, 1986). After examining the original descriptions, we transfer these species as Microcotyle danielcarrioni (Martinez & Barrantes, 1977) n. comb. and Microcotyle moyanoi (Villalba & Fernandes, 1986) n. comb.
References
Akmirza, A. (2013). Monogeneans of fish near Gökçeada, Turkey. Turkish Journal of Zoology, 37, 441–448.
Aquaro, G., Salogni, C., Galli, P., Gibelli, L., & Gelmetti, D. (2012). Sciadicleithrum variabilum (Dactylogyridae: Monogenea) infection in Symphysodon discus: a case report. Fish Pathology, 47, 23–26.
Ariola, V. (1899). Di alcuni trematodi di pesci marini. Bollettino dei Musei e laboratori di zoologia e anatomia comparata della R. Università di Genova, 4, 1–12.
Ayadi, Z. E. M., Gey, D., Justine, J.-L., & Tazerouti, F. (2017). A new species of Microcotyle (Monogenea: Microcotylidae) from Scorpaena notata (Teleostei: Scorpaenidae) in the Mediterranean Sea. Parasitology International, 66, 37–42.
Boudaya, L., & Neifar, L. (2016). Triloculotrema euzeti n. sp. (Monogenea, Monocotylidae) from the nasal tissues of the blackspotted smooth-hound Mustelus punctulatus (Carcharhiniformes, Triakidae) from off Tunisia. Parasite, 23, 62.
Bowles, J., Blair, D., & McManus, D. P. (1995). A molecular phylogeny of the human schistosomes. Molecular Phylogenetics and Evolution, 4, 103–109.
Caballero y Caballero, E., & Bravo-Hollis, M. (1972). Monogenea (van Beneden, 1858) Carus, 1863 de peces marinos del litoral mexicano del Golfo de México y del Mar Caribe. V. Revista de Biologia Tropical, 20, 151–165.
Chaabane, A., Justine, J.-L., Gey, D., Bakenhaster, M. D., & Neifar, L. (2016a). Pseudorhabdosynochus sulamericanus (Monogenea, Diplectanidae), a parasite of deep-sea groupers (Serranidae) occurs transatlantically on three congeneric hosts (Hyporthodus spp.), one from the Mediterranean Sea and two from the western Atlantic. PeerJ, 4, e2233.
Chaabane, A., Neifar, L., Gey, D., & Justine, J.-L. (2016b). Species of Pseudorhabdosynochus (Monogenea, Diplectanidae) from groupers (Mycteroperca spp., Epinephelidae) in the Mediterranean and Eastern Atlantic Ocean, with special reference to the “beverleyburtonae group” and description of two new species. PLoS One, 11, e0159886.
Chaabane, A., Neifar, L., & Justine, J.-L. (2015). Pseudorhabdosynochus regius n. sp. (Monogenea, Diplectanidae) from the mottled grouper Mycteroperca rubra (Teleostei) in the Mediterranean Sea and Eastern Atlantic. Parasite, 22, 9.
Chaabane, A., Neifar, L., & Justine, J.-L. (2017). Diplectanids from Mycteroperca spp. (Epinephelidae) in the Mediterranean Sea: Redescriptions of six species from material collected off Tunisia and Libya, proposal for the ‘Pseudorhabdosynochus riouxi group’, and a taxonomic key. PLoS One, 12, e0171392.
Chaari, M., Derbel, H., & Neifar, L. (2016). Axinoides euzeti n. sp. (Monogenea: Axinidae) from the gills of the needlefish Tylosurus acus imperialis (Rafinesque) (Belonidae) off Tunisia, with an updated list of hosts and localities for Axinoides spp. Systematic Parasitology, 93, 917–926.
Dillon, W. A., & Hargis, W. J. (1965). Monogenetic trematodes from the Southern Pacific Ocean. 2. Polyopisthocotyleids from New Zealand fishes: the families Discocotylidae, Microcotylidae, Axinidae and Gastrocotylidae. Biology of the Antarctic Seas II, Antarctic Research Series, 5, 251–280.
Du Preez, L. H., Verneau, O., & Gross, T. S. (2007). Polystoma floridana n. sp. (Monogenea: Polystomatidae), a parasite in the green tree frog, Hyla cinerea (Schneider), of North America. Zootaxa, 1663, 33–45.
Euzet, L., Combes, C., & Caro, C. A check list of Monogenea of mediterranean fish. In: Second International Symposium on Monogenea, Montpellier/Sète, 1993.
Euzet, L., & Marc, A. (1963). Microcotyle donavini van Beneden et Hesse 1863 espèce type du genre Microcotyle van Beneden et Hesse 1863. Annales de Parasitologie Humaine et Comparée, 38, 875–886.
Fernandez-Jover, D., Faliex, E., Sanchez-Jerez, P., Sasal, P., & Bayle-Sempere, J. T. (2010). Coastal fish farming does not affect the total parasite communities of wild fish in SW Mediterranean. Aquaculture, 300, 10–16.
Fischer, W., Bauchot, M.-L., & Schneider, M. (1987). Fiches FAO d’identification des espèces pour les besoins de la pêche. (Révision 1). Méditerranée et mer Noire. Zone de pêche 37. Volume II. Vertébrés. Publication préparée par la FAO, résultat d’un accord entre la FAO et la Commission des Communautés Européennes (Projet GCP/INT/422/EEC) financée conjointement par ces deux organisations. Vo1ume 2. Rome: FAO, pp. 761–1530.
Goto, S. (1894). Studies on the Ectoparasitic Trematodes of Japan. Tokyo.
Hadi, R., & Bilqees, F. (2010). Microcotyle rubrum n. sp. (Monogenea: Microcotylidae) from Otolithus ruber of Karachi coast. Pakistan. Proceedings of Parasitology, 50, 115–126.
Hadi, R., & Bilqees, F. (2011). Microcotyle argenticus n. sp. (Monogenea) on the fish Pampus argenticus from Karachi coast. Proceedings of Parasitology, 51, 99–111.
Hadi, R., Bilqees, F., & Khatoon, N. (2011). Microcotyle jonii n. sp. of (Monogenea: Microcotylidae) in the fish Lutjanus jonii from Karachi coast. Proceedings of Parasitology, 52, 69–81.
Hasegawa, M., Kishino, H., & Yano, T.-A. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22, 160–174.
ICZN (2012). International Commission on Zoological Nomenclature: Amendment of articles 8, 9, 10, 21 and 78 of the International Code of Zoological Nomenclature to expand and refine methods of publication. Bulletin of Zoological Nomenclature, 69, 161–169.
Jovelin, R., & Justine, J.-L. (2001). Phylogenetic relationships within the polyopisthocotylean monogeneans (Platyhelminthes) inferred from partial 28S rDNA sequences. International Journal for Parasitology, 31, 393–401.
Justine, J.-L. (2011). Protocotyle euzetmaillardi n. sp. (Monogenea, Hexabothriidae) from the bigeye sixgill shark Hexanchus nakamurai Teng (Elasmobranchii, Hexanchidae) off New Caledonia. Systematic Parasitology, 78, 41–55.
Justine, J.-L., Rahmouni, C., Gey, D., Schoelinck, C., & Hoberg, E. P. (2013). The monogenean which lost its clamps. PLoS One, 8, e79155.
Kheddam, H., Justine, J.-L., & Tazerouti, F. (2016). Hexabothriid monogeneans from the gills of deep-sea sharks off Algeria, with the description of Squalonchocotyle euzeti n. sp. (Hexabothriidae) from the kitefin shark Dalatias licha (Euselachii, Dalatiidae). Helminthologia, 53, 354–362.
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.
Kohn, A., Baptista-Farias, M. F. D., & Cohen, S. C. (2000). Paranaella luquei gen. et sp. n. (Monogenea: Microcotylidae), a new parasite of Brazilian catfishes. Folia Parasitologica, 47, 279–284.
Kouider El Ouahed-Amine, F. (1998). Contribution à l’étude des Monogènes parasites des poissons Sparidae (Téléostéens) du littoral Algérois. Approche taxonomique et écologique (pp. 1–215). Thesis, USTHB, Alger, Algeria.
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.
Li, M., Shi, S.-F., Brown, C. L., & Yang, T.-B. (2011). Phylogeographical pattern of Mazocraeoides gonialosae (Monogenea, Mazocraeidae) on the dotted gizzard shad, Konosirus punctatus, along the coast of China. International Journal for Parasitology, 41, 1263–1272.
Littlewood, D. T. J., Rohde, K., & Clough, K. A. (1997). Parasite speciation within or between host species? - Phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology, 27, 1289–1297.
MacCallum, G. A. (1913). Further notes on the genus Microcotyle. Zoologische Jahrbücher Abteilung für Systematik, Geographie und Biologie der Tiere, 35, 389–402.
Machkewskyi, V. K., Dmitrieva, E. V., Al-Jufaili, S., & Al-Mazrooei, N. A. (2013). Microcotyle omanae n. sp. (Monogenea: Microcotylidae), a parasite of Cheimerius nufar (Valenciennes) (Sparidae) from the Arabian Sea. Systematic Parasitology, 86, 153–163.
Mamaev, Y. L. (1977). On one classification of monogeneans of the family Microcotylidae. Parazitologiya, 11, 98–103 (In Russian).
Mamaev, Y. L. (1984). The composition of the genera Atriaster and Atrispinum (Microcotylidae, Monogenea) and some peculiarities of their morphology. Parazitologiya, 18, 204–208 (In Russian).
Mamaev, Y. L. (1986). The taxonomical composition of the family Microcotylidae Taschenberg, 1879 (Monogenea). Folia Parasitologica, 33, 199–206.
Martinez, R., & Barrantes, I. (1977). Helmintos parásitos de Cheilodactylus variegatus Valenciennes, 1833, “pintadilla”. I. Paramicrocotyle danielcarrioni n. sp. (Monogenea: Microcotylidae). Biota (Lima), 11, 139–146.
Marzoug, D., Boutiba, Z., Kostadinova, A., & Pérez-del-Olmo, A. (2012). Effects of fishing on parasitism in a sparid fish: Contrasts between two areas of the Western Mediterranean. Parasitology International, 61, 414–420.
Mendoza-Garfias, B., García-Prieto, L., & León, G. P.-P. D. (2017). Checklist of the monogenea (Platyhelminthes) parasitic in mexican aquatic vertebrates. Zoosystema, 39, 501–598.
Mladineo, I., Šegvić, T., & Grubišić, L. (2009). Molecular evidence for the lack of transmission of the monogenean Sparicotyle chrysophrii (Monogenea, Polyopisthocotylea) and isopod Ceratothoa oestroides (Crustacea, Cymothoidae) between wild bogue (Boops boops) and cage-reared sea bream (Sparus aurata) and sea bass (Dicentrarchus labrax). Aquaculture, 295, 160–167.
Oliva, M. E., Sepulveda, F. A., & González, M. T. (2014). Parapedocotyle prolatili gen. n. et sp. n., a representative of a new subfamily of the Diclidophoridae (Monogenea), a gill parasite of Prolatilus jugularis (Teleostei: Pinguipedidae) from Chile. Folia Parasitologica, 61, 543.
Papoutsoglou, S. E. (2016). Metazoan parasites of fishes from Saronicos gulf, Athens-Greece. Thalassographica, 1, 69–102.
Park, J. K., Kim, K. H., Kang, S., Kim, W., Eom, K. S., & Littlewood, D. T. J. (2007). A common origin of complex life cycles in parasitic flatworms: evidence from the complete mitochondrial genome of Microcotyle sebastis (Monogenea: Platyhelminthes). BMC Evolutionary Biology, 7, 11.
Parona, C., & Perugia, A. (1890). Contribuzione per una monografia del genere Microcotyle. Annali del Museo Civico di Storia Naturale di Genova, Series, 2(5), 173–220.
Pérez-del Olmo, A., Fernandez, M., Gibson, D. I., Raga, J. A., & Kostadinova, A. (2007). Descriptions of some unusual digeneans from Boops boops L. (Sparidae) and a complete checklist of its metazoan parasites. Systematic Parasitology, 66, 137–157.
Pérez-del-Olmo, A., Raga, J. A., Kostadinova, A., & Fernández, M. (2007). Parasite communities in Boops boops (L.) (Sparidae) after the Prestige oil-spill: Detectable alterations. Marine Pollution Bulletin, 54, 266–276.
Radujkovic, B. M., & Euzet, L. (1989). Parasites des poissons marins du Monténégro: Monogènes. In: Radujkovic, B. M & Raibaut, A. (Eds) Faune des parasites de poissons marins des côtes du Monténégro (Adriatique Sud). Acta Adriatica, 30, 51–135.
Ratnasingham, S., & Hebert, P. D. N. (2007). BOLD: The Barcode of Life Data System (www. barcodinglife. org). Molecular Ecology Notes, 7, 355–364.
Sailaja, B., & Madhavi, R. (2011). Polylabris bengalensis sp. nov. (Monogenea, Microcotylidae) from siganid fishes of the Visakhapatnam coast, Bay of Bengal, India. Acta Parasitologica, 56(3), 290–295.
Sepúlveda, F. A., & González, M. T. (2015). Patterns of genetic variation and life history traits of Zeuxapta seriolae infesting Seriola lalandi across the coastal and oceanic areas in the southeastern Pacific Ocean: potential implications for aquaculture. Parasites & Vectors, 8, 282.
Shi, S.-F., Li, M., Yan, S., Wang, M., Yang, C.-P., Lun, Z.-R., et al. (2014). Phylogeography and demographic history of Gotocotyla sawara (Monogenea: Gotocotylidae) on Japanese Spanish mackerel (Scomberomorus niphonius) along the coast of China. Journal of Parasitology, 100, 85–92.
Sproston, N. (1946). A synopsis of the monogenetic trematodes. Transactions of the Zoological Society of London, 25, 185–600.
Strona, G., Stefani, F., & Galli, P. (2010). Monogenoidean parasites of Italian marine fish: An updated checklist. Italian Journal of Zoology, 77, 419–437.
Tambireddy, N., Gayatri, T., Gireesh-Babu, P., & Pavan-Kumar, A. (2016). Molecular characterization and phylogeny of some mazocraeidean monogeneans from carangid fish. Acta Parasitologica, 61, 360–368.
Tripathi, Y. R. (1956). Studies on the parasites of Indian fishes. IV. Trematoda: Monogenea. Microcotylidae. Records of the Indian Museum, 52, 231–247.
Ulmer, M. J., & James, H. A. (1981). Monogeneans of marine fishes from the Bay of Naples. Transactions of the American Microscopical Society, 100, 392–409.
Unnithan, R. V. (1971a). On the functional morphology of a new fauna of Monogenoidea on fishes from Trivandrum and environs. Part IV. Microcotylidae sensu stricto and its repartition into subsidiary taxa. American Midland Naturalist, 85, 366–398.
Unnithan, R. V. (1971b). [1967]). Patterns of secondary growth and a revision of the systematics in Microcotyloidea and Gastrocotylidae (Monogenoidea). Records of the Zoological Survey of India, Records of the Zoological Survey of India, 65, 17–88.
van Beneden, P. J., & Hesse, C. E. (1863). Recherches sur les Bdellodes (Hirudinées) et les Trématodes marins. Mémoires de l’Académie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique, 34, 1-150 + Plates.
Villalba, C., & Fernández, J. (1986). Dos nuevas especies de tremátodos parásitos de peces marinos en Chile. Parasitologia al Dia, 10, 45–51.
Ward, R. D., Zemlak, T. S., Innes, B. H., Last, P. R., & Hebert, P. D. (2005). DNA barcoding Australiaʼs fish species. Philosophical Transactions of the Royal Society of London, B Biological Sciences, 360, 1847–1857.
Williams, A. (1991). Monogeneans of the families Microcotylidae Taschenberg, 1879 and Heteraxinidae Price, 1962 from Western Australia, including the description of Polylabris sandersae n. sp. (Microcotylidae). Systematic Parasitology, 18, 17–43.
WoRMS (2018). Microcotyle van Beneden & Hesse, 1863. http://www.marinespecies.org/aphia.php?p=taxdetails&id=119381. Accessed on 17 November 2018.
Yamaguti, S. (1963). Systema Helminthum. Volume IV, Monogenea and Aspidocotylea. New York & London: Interscience, a division of John Wiley & Sons.
Yan, S., Wang, M., Yang, C.-P., Zhi, T.-T., Brown, C. L., & Yang, T.-B. (2016). Comparative phylogeography of two monogenean species (Mazocraeidae) on the host of chub mackerel, Scomber japonicus, along the coast of China. Parasitology, 143, 594–605.
Yoon, G., Al-Jufaili, S., Freeman, M., Bron, J., Paladini, G., & Shinn, A. (2013). Omanicotyle heterospina n. gen. et n. comb. (Monogenea: Microcotylidae) from the gills of Argyrops spinifer (Forsskål) (Teleostei: Sparidae) from the Sea of Oman. Parasites & Vectors, 6, 170.
Yoshinaga, T., Tsutsumi, N., Hall, K. A., & Ogawa, K. (2009). Origin of the diclidophorid monogenean Neoheterobothrium hirame Ogawa, 1999, the causative agent of anemia in olive flounder Paralichthys olivaceus. Fisheries Science, 75, 1167–1176.
Zhang, J., Wu, X., Xie, M., Xu, X., & Li, A. (2011). The mitochondrial genome of Polylabris halichoeres (Monogenea: Microcotylidae). Mitochondrial DNA, 22, 3–5.
Acknowledgements
The authors are grateful to the French Consulate in Algiers. We thank members of the administrative staff of ISYEB, MNHN, for help for the visa, namely Sabrina Permall, Guzide Selcuk-Shahine, Sylvianne Babin and Nora Tagnit-Hamou. The authors are indebted to the staff of LBEIG, Amina Boutellis, Zouhour El Mouna Ayadi and Samia Terkmani for their continued support of our research. Our thanks are also due to fishermen from Regaiia and especially Mohamed Kayrouz. We thank Marcelo Enrique Oliva and John D. Chero for providing references.
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Bouguerche, C., Gey, D., Justine, JL. et al. Microcotyle visa n. sp. (Monogenea: Microcotylidae), a gill parasite of Pagrus caeruleostictus (Valenciennes) (Teleostei: Sparidae) off the Algerian coast, Western Mediterranean. Syst Parasitol 96, 131–147 (2019). https://doi.org/10.1007/s11230-019-09842-2
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DOI: https://doi.org/10.1007/s11230-019-09842-2