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Original Article • Rev. Bras. Parasitol. Vet. 29 (1) • 2020 • https://doi.org/10.1590/S1984-29612020005 copy

Phyllodistomum vaili(Plagiorchiida: Gorgoderidae) infecting Parupeneus rubescens (Perciformes: Mullidae): morphology and phylogeny

Phyllodistomum vaili (Plagiorchiida: Gorgoderidae) infectando Parupeneus rubescens (Perciformes: Mullidae): morfologia e filogenia

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Knowledge of the Arabian Gulf fish’s parasite fauna is very poor. Until recently, only scattered reports from different locations are known for ecto- and endoparasites. Therefore, the present study aimed to investigate the digenean species that infects one of the most economically fish species in the Arabian Gulf, the rosy goatfish Parupeneus rubescens . One plagiorchiid species has been described, belonging to the Gorgoderidae family, and has been named as Phyllodistomum vaili Ho, Bray, Cutmore, Ward & Cribb, 2014 based on its morphological and morphometric characteristics. In order to accurately classify and characterize this plagiorchiid species, molecular analysis was carried out using both nuclear 18S and 28S rRNA gene regions and revealed that the present plagiorchiid species was associated with other species belonging to the Gorgoderidae family and deeply embedded in the Phyllodistomum genus, closely related to the previously described P. vaili (gb| KF013187.1, KF013173.1). The present study therefore revealed that the species Phyllodistomum is the first account as endoparasites from the rosy goatfish inhabiting the Arabian Gulf.

Keywords:
Rosy goatfish; Digenean parasites; Gorgoderidae; Plagiorchiida; Arabian Gulf

Parasite species	Host (Locality)	Body size	Dimensions of different body parts
Parasite species	Host (Locality)	Body size	Oral sucker	Ventral sucker	Vitelline glands	Anterior testis	Posterior testis	Ovary	Eggs
*P. magnificum* Cribb, 1987	Anguilla reinhardtii(New Zealand)	1.92-4.54 (2.93) × 0.66-2.18 (1.33)	0.20-0.36 (0.27) × 0.17-0.31 (0.24)	0.20-0.45 (0.34) × 0.19-0.47 (0.34)	--	0.16-0.39 (0.27) × 0.11-0.33 (0.21)	0.22-0.48 (0.31) × 0.11-0.33 (0.23)	0.08-0.22 (0.16) × 0.07-0.18 (0.13)	0.036-0.043 (0.038) × 0.023-0.027 (0.024)
*P. funduli* Helt et al., 2003	Fundulus sciadicus(Nebraska)	1.10-5.49 (2.06) × 0.46-2.73 (1.09)	0.20-0.83 (0.33) × 0.20-0.78 (0.32)	0.15-0.73 (0.29) × 0.12-0.71 (0.29)	L: 0.07-0.36 (0.18) × 0.05-0.27 (0.09) R: 0.07-0.49 (0.18) × 0.05-0.24 (0.08)	0.07-0.32 (0.21) × 0.05-0.54 (0.19)	0.10-0.85 (0.24) × 0.07-0.73 (0.23)	0.10-0.51 (0.20)	0.01-0.04 (0.03) × 0.01-0.03 (0.02)
*P. simile* Sey et al., 2004	Cirrhinus marginipinnis(Thailand)	1.6-1.9 ×1.0	0.20-0.22	0.31-0.35 × 0.30-0.35	L: 0.75 × 0.10 R: 0.06-0.07 × 1.0-1.25	0.25-0.40 × 0.20-0.25	0.40-0.42 ×0.20-0.25	0.15-0.17 × 0.10	0.026-0.030 × 0.018-0.020
*P. inecoli* Razo-Mendivil et al., 2013	Heterandria bimaculata(Mexico)	1.15-2.08 (1.60) × 0.49-1.13 (0.80)	0.16-0.30 (0.23) × 0.14-0.25 (0.21)	0.14-0.27 (0.20) × 0.14-0.27 (0.19)	L: 0.06-0.12 (0.09) × 0.04-0.10 (0.07) R: 0.06-0.16 (0.09) × 0.04-0.10 (0.07)	0.10-0.39 (0.23) × 0.06-0.21 (0.13)	0.08-0.39 (0.23) × 0.06-0.21 (0.14)	0.05-0.20 (0.13) × 0.06-0.17 (0.11)	0.023-0.028 (0.026) × 0.014-0.018 (0.016)
*P. biringo* Shimazu, 2005	Gymnogobius breunigii(Japan)	0.70-1.44 ×0.37-0.71	0.08-0.12 × 0.09-0.11	0.12-0.14 × 0.11-0.16	0.05-0.06 × 0.09-0.11	0.09-0.17 × 0.09-0.14	0.09-0.17 × 0.09-0.14	0.06-0.15 × 0.09-0.14	0.033-0.048 × 0.021-0.024
*P. carassii* Shimazu, 2005	Carassius auratus(Japan)	3.92-5.37 × 2.96-3.42	0.56 × 0.45-0.48	0.61-0.62 × 0.53-0.64	0.48-0.75 × 0.05-0.12	0.35 × 0.27	0.19-0.29 × 0.10-0.24	--	0.017-0.019 ×0.013
*P. mogurndae* Shimazu, 2005	Odontobutis obscura(Japan)	1.74-4.01 × 1.03-1.98	0.25-0.43 × 0.20-0.41	0.19-0.33 × 0.21-0.34	0.09-0.25 × 0.11-0.25	0.18-0.41 × 0.17-0.28	0.20-0.34 × 0.16-0.41	0.13-0.43 × 0.19-0.35	0.016-0.017 × 0.011-0.013
*P. hoggettae* Ho et al., 2014	Plectropomus leopardus(Great Barrier Reef)	3.48-4.76 (4.14) × 0.96-1.85 (1.50)	0.28-0.44 (0.33) × 0.28-0.41 (0.30)	0.36-0.55 (0.43) × 0.36-0.51 (0.44)	L: 0.12-0.27 (0.17) × 0.07-0.21 (0.12) R: 0.10-0.28 (0.19) × 0.05-0.22 (0.12)	0.15-0.34 (0.27) × 0.09-0.39 (0.25)	0.17-0.45 (0.30) × 0.15-0.54 (0.28)	0.07-0.33 (0.20) × 0.06-0.23 (0.16)	0.036-0.057 (0.049) × 0.021-0.033 (0.029)
*P. vaili* Ho et al., 2014	Mulloidichthys vanicolensis	1.49-2.30 (1.84) × 0.40-0.68 (0.54)	0.13-0.20 (0.16) × 0.12-0.20 (0.15)	0.11-0.18 (0.14) × 0.09-0.17 (0.14)	L: 0.052-0.093 (0.074) × 0.051-0.083 (0.054) R: 0.049-0.125 (0.078) × 0.033-0.081 (0.053)	0.08-0.19 (0.14) × 0.06-0.18 (0.12)	0.06-0.21 (0.15) × 0.06-0.17 (0.12)	0.05-0.15 (0.10) × 0.04-0.13 (0.08)	0.027-0.050 (0.041) × 0.014-0.029 (0.022)
*P. parasiluri* Shimazu, 2005	Silurus asotus(Japan)	1.13-3.49 × 0.41-1.04	0.09-0.25 × 0.11-0.24	0.16-0.35 × 0.16-0.33	0.04-0.16 × 0.09-0.22	0.22-0.63 × 0.12-0.41	0.25-0.82 × 0.14-0.51	0.09-0.32 × 0.09-0.25	0.011-0.022 × 0.008-0.016
*P. cribbi* Pérez-Ponce de León et al., 2015	Zoogoneticus quiteoensis(Mexico)	0.92-1.84 (1.46) × 0.47-1.22 (0.90)	0.17-0.29 (0.23) × 0.14-0.28 (0.23)	0.14-0.25 (0.20) × 0.14-0.27 (0.22)	L: 0.05-0.10 (0.07) × 0.06-0.14 (0.10) R: 0.04-0.09 (0.06) × 0.06-0.14 (0.11)	0.12-0.27 (0.19) × 0.09-0.26 (0.18)	0.08-0.30 (0.17) × 0.10-0.28 (0.18)	0.06-0.17 (0.11) × 0.12-0.15 (0.13)	0.018-0.037 (0.028) × 0.013-0.026 (0.020)
*P. kanae* Nakao, 2015	Hynobius retardatus(Japan)	4.0-4.9 × 2.0-2.1	0.48-0.49 × 0.51-0.55	0.83-0.85 × 0.60-0.70	L: 0.22-0.29 × 0.16-0.17 R: 0.23-0.27 × 0.14-0.18	0.69-0.83 × 0.52-0.54	0.88-0.92 × 0.41-0.52	0.39-0.40	0.049-0.054 × 0.034-0.037
*P. wallacei* Pérez-Ponce de León et al., 2015	Xenotaenia resolanae (Mexico)	0.71-1.61 (1.24) × 0.44-1.22 (0.79)	0.14-0.28 (0.19) × 0.11-0.32 (0.19)	0.11-0.18 (0.16) × 0.09-0.21 (0.16)	L: 0.03-0.11 (0.06) × 0.03-0.13 (0.08) R: 0.03-0.11 (0.07) × 0.03-0.13 (0.08)	0.06-0.25 (0.12) × 0.07-0.13 (0.10)	0.09-0.19 (0.13) × 0.08-0.16 (0.11)	0.05-0.20 (0.13) × 0.12-0.15 (0.13)	0.019-0.032 (0.025) × 0.013-0.23 (0.018)
*P. hyporhamphi* Cutmore and Cribb, 2018	Hyporhamphus regularis(Australia)	1.83-5.08 (3.40) × 0.87-2.92 (1.71)	0.25-0.52 (0.41) × 0.19-0.44 (0.34)	0.13-0.28 (0.22) × 0.14-0.31 (0.23)	L: 0.10-0.28 (0.19) × 0.12-0.29 (0.18) R: 0.11-0.30 (0.19) × 0.12-0.32 (0.19)	0.13-0.42 (0.22) × 0.14-0.43 (0.26)	0.16-0.53 (0.26) × 0.14-0.43 (0.26)	0.14-0.32 (0.23) × 0.133-0.44 (0.23)	--
*P. pacificum* Cutmore and Cribb, 2018	Carangoides equula(Japan)	4.57-5.33 (4.95) × 1.11-1.32 (1.22)	0.31-0.41 (0.35) × 0.31-0.38 (0.33)	0.26-0.34 (0.29) × 0.26-0.32 (0.28)	L: 0.09-0.17 (0.12) × 0.11-0.18 (0.14) R: 0.08-0.16 (0.11) × 0.12-0.19 (0.14)	0.32-0.48 (0.39) × 0.24-0.42 (0.30)	0.41-0.59 (0.50) × 0.27-0.48 (0.35)	0.16-0.30 (0.20) × 0.12-0.24 (0.16)	0.032-0.051 (0.042) × 0.021-0.032 (0.26)
*P. punctati* Jithila and Prasadan, 2018	Channa punctata(India)	1.51-6.13 (2.92) × 1.03-4.32 (2.92)	0.33-0.82 (0.47) × 0.35-0.76 (0.46)	0.28-0.29 (0.44) × 0.29-0.73 (0.45)	L: 0.09-0.32 (0.20) × 0.05-0.30 (0.17) R: 0.09-0.29 (0.17) × 0.06-0.27 (0.16)	0.12-0.51 (0.29) ×0.07-0.32 (0.18)	0.09-0.68 (0.28) × 0.11-0.33 (0.17)	0.11-0.43 (0.26) × 0.10-0.37 (0.23)	0.024-0.029 (0.025) × 0.012-0.020 (0.016)
*P. vaili* (Present study)	Parupeneus rubescens(Saudi Arabia)	1.38-2.10 (1.75±0.1) × 0.41-0.63 (0.52±0.01)	0.11-0.18 (0.14±0.01) × 0.10-0.18 (0.12±0.01)	0.10-0.16 (0.13±0.01) × 0.08-0.14 (0.12±0.01)	L: 0.054-0.098 (0.081±0.001) × 0.051-0.083 (0.054±0.001) R: 0.049-0.118 (0.086±0.001) × 0.035-0.087 (0.064±0.001)	0.09-0.17 (0.15±0.01) × 0.07-0.15 (0.13±0.01)	0.06-0.19 (0.16±0.01) × 0.06-0.16 (0.13±0.01)	0.06-0.17 (0.11±0.01) × 0.04-0.15 (0.09±0.001)	0.032-0.059 (0.050±0.001) × 0.015-0.027 (0.020±0.001)

Parasite species	Order/Family	Host species	Accession no.	Percent identity (%)	GC content
Phyllodistomum vaili	Plagiorchiida/Gorgoderidae	Mulloidichthys vanicolensis	KF013187.1	99.50%	53.25%
Phyllodistomum vaili	Plagiorchiida/Gorgoderidae	Mulloidichthys flavolineatus	KF013173.1	99.50%	53.34%
Phyllodistomum pacificum	Plagiorchiida/Gorgoderidae	Pantolabus radiatus	MG845599.1	98.73%	52.93%
Phyllodistomumsp.	Plagiorchiida/Gorgoderidae	Epibulus insidiator	KF013179.1	91.58%	54.30%
Phyllodistomumsp.	Plagiorchiida/Gorgoderidae	Cephalopholis boenak	KF013175.1	91.09%	54.24%
Phyllodistomum hoggettae	Plagiorchiida/Gorgoderidae	Plectropomus leopardus	KF013191.1	90.10%	55.14%
Gorgodera cygnoides	Plagiorchiida/Gorgoderidae	Pelophylax ridibundus	AY222264.1	89.08%	53.88%
Polylekithum ictaluri	Plagiorchiida/Allocreadiidae	Ictalurus furcatus	EF032697.1	88.66%	52.06%
Phyllodistomum kanae	Plagiorchiida/Gorgoderidae	Hynobius retardatus	AB979868.1	88.53%	54.02%
Phyllodistomum brevicecum	Plagiorchiida/Gorgoderidae	Umbra limi	KC760204.1	88.39%	53.84%
Phyllodistomum spinopapillatum	Plagiorchiida/Gorgoderidae	Profundulus balsanus	KM659382.1	88.24%	52.64%
Phyllodistomum folium	Plagiorchiida/Gorgoderidae	Pisidium amnicum	KJ729541.1	88.24%	53.22%
Phyllodistomum inecoli	Plagiorchiida/Gorgoderidae	Profundulus sp.	KM659389.1	87.82%	52.38%
Polylekithum catahoulensis	Plagiorchiida/Allocreadiidae	Ictalurus furcatus	EF032698.1	87.82%	52.35%
Cephalogonimus mukerjius	Plagiorchiida/Cephalogonimidae	Pila globosa	KF977406.1	87.76%	49.27%
Phyllodistomum lacustri	Plagiorchiida/Gorgoderidae	Ameiurus melas	EF032692.1	87.56%	53.76%
Phyllodistomumsp.	Plagiorchiida/Gorgoderidae	Pisidium amnicum	AY281126.1	87.39%	53.74%
Phyllodistomum macrocotyle	Plagiorchiida/Gorgoderidae	Dreissena polymorpha	AY288830.1	87.39%	50.95%
Brachylecithum kakea	Plagiorchiida/Dicrocoelidae	Acrocephalus arundinaceus	MG560851.1	86.55%	52.94%
Stromitrema koshewnikowi	Plagiorchiida/Dicrocoelidae	Hirundo rustica	MG560850.1	86.55%	54.53%
Campula oblonga	Plagiorchiida/Brachycladiidae	East Asian finless porpoise	KX354834.1	86.55%	55.60%
Megasolena hysterospina	Plagiorchiida/Haploporidae	Archosargus rhomboidalis	MH244121.1	86.55%	52.02%
Phyllodistomumsp.	Plagiorchiida/Gorgoderidae	Channa striata	MG976755.1	86.46%	53.75%
Lepidapedon elongatum	Plagiorchiida/Lepocreadiidae	Gadus morhua	AJ405266.1	86.19%	52.94%
Lepidapedon beveridgei	Plagiorchiida/Lepocreadiidae	Coryphaenoides armatus	AJ405263.1	86.19%	53.60%
Gibsonivermis berryi	Plagiorchiida/Gibsonivermidae	Sillago ciliata	MH157070.1	86.19%	53.41%
Isorchis currani	Plagiorchiida/Atractotrematidae	Selenotoca multifasciata	MF803157.1	86.13%	54.09%
Haplometroides intercaecalis	Plagiorchiida/Plagiorchiidae	Phalotris matogrossensis	MH206169.1	85.77%	52.88%

Parasite species	Order/Family	Host species	Accession no.	Percent identity (%)	GC content
Gorgoderina lufengensis	Plagiorchiida/Gorgoderidae	Nanorana yunnanensis	MH285258.1	93.11%	50.50%
Gorgodera sp.	Plagiorchiida/Gorgoderidae	Rana ridibunda	AJ287518.1	92.81%	49.87%
Ragaia lizae	Plagiorchiida/Haploporidae	Liza aurata	FJ211231.1	91.19%	51.77%
Haploporus benedeni	Plagiorchiida/Haploporidae	Liza ramado	FJ211228.1	90.92%	51.81%
Dicrogaster perpusilla	Plagiorchiida/Haploporidae	Liza ramado	FJ211230.1	90.88%	51.17%
Saccocoelium cephali	Plagiorchiida/Haploporidae	Mugil cephalus	FJ211232.1	90.75%	51.52%
Orchipedum tracheicola	Echinostomida/Orchipedidae	Cygnus olor	AJ287551.1	90.45%	51.05%
Prosthenhystera obesa	Plagiorchiida/Callodistomidae	Hoplias sp.	AY222108.1	90.27%	50.56%
Rubenstrema exasperatum	Plagiorchiida/Plagiorchiidae	Crocidura leucodon	AJ287572.1	90.16%	50.43%
Stephanostomum gaidropsori	Opisthorchiida/Acanthocolpidae	Gaidropsarus mediterraneus	DQ248208.1	90.16%	50.97%
Campula oblonga	Plagiorchiida/Brachycladiidae	Phocoena phocoena	KM258665.1	90.02%	52.03%
Opisthioglyphe ranae	Plagiorchiida/Plagiorchiidae	Rana arvalis	AY222157.1	90.01%	49.97%
Haematoloechus longiplexus	Plagiorchiida/Haematoloechidae	Rana catesbeiana	AJ287520.1	89.88%	50.23%
Oschmarinella rochebruni	Plagiorchiida/Brachycladiidae	Stenella coeruleoalba	KM258667.1	89.87%	51.05%
Paragonimus iloktsuenensis	Plagiorchiida/Troglotrematidae	Rattus norvegicus	AY222141.1	89.85%	51.77%
Nasitrema globicephalae	Opisthorchiida/Nasitrematidae	--	AJ004968.1	89.85%	51.05%
Synthesium pontoporiae	Plagiorchiida/Brachycladiidae	--	FJ357162.1	89.85%	51.23%
Nephrotrema truncatum	Plagiorchiida/Troglotrematidae	Neomys anomalus	AY222139.1	89.85%	51.07%
Brachycladium goliath	Plagiorchiida/Brachycladiidae	Balaenoptera acutorostrata	KR703279.1	89.85%	51.68%
Stephanostomum cestillium	Opisthorchiida/Acanthocolpidae	Lophius piscatorius	DQ248213.1	89.85%	51.05%
Skrjabinoeces similis	Plagiorchiida/Plagiorchiidae	Rana ridibunda	AJ287575.1	89.51%	50.17%
Auridistomum chelydrae	Plagiorchiida/Auridistomidae	Chelydra serpentina	AY222159.1	89.40%	50.88%
Pseudomegasolena ishigakiense	Plagiorchiida/Haploporidae	Scarus rivulatus	AJ287569.1	88.97%	49.92%
Lissorchis kritskyi	Plagiorchiida/Lissorchiidae	Carpiodes cyprinus	AY222136.1	88.79%	50.25%

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