Philiohthalmus hechingeri, Sasaki & Miura & Nakao, 2022

Sasaki, Mizuki, Miura, Osamu & Nakao, Minoru, 2022, Philophthalmus hechingeri n. sp. (Digenea: Philophthalmidae), a Human-Infecting Eye Fluke from the Asian Mud Snail, Batillaria attramentaria, Journal of Parasitology 108 (1), pp. 44-52 : 48-49

Philiohthalmus hechingeri n. sp. Sasaki and Miura

( Figs. 4–6 )

Adult (based on 7 whole-mounted specimens): Body slightly constricted at level of ventral sucker, 1,350–2,150 (1,650 6 278) long by 480–740 (581 6 85) wide in maximum ( Fig. 4 ). Tegument spinose only in anterior part of body. Oral sucker subterminal, 170–191 (179 6 9) long by 204–258 (229 6 19) wide. Prepharynx invisible. Pharynx large, 122–167 (143 6 21) long by 129–177 (151 6 13) wide. Esophagus absent. Ventral sucker large, 320–391 (348 6 26) long by 344–394 (366 6 23) wide. Ratio of width of oral to ventral sucker 1:1.6. Caeca arise directly behind pharynx, extending posteriorly to near end of body. Genital pore just postbifurcal. Genital atrium absent. Cirrus sac large, 747–835 (787 6 34) long by 57–91 (75 6 14) wide in maximum, extending beyond posterior margin of ventral sucker. Seminal vesicle tubular, situated inside cirrus sac. Testes slightly lobed, tandemly located at posterior end. Anterior testes, 153–247 (196 6 37) long by 313–380 (344 6 26) wide. Posterior testes, 155–244 (209 6 34) long by 344–381 (356 6 17) wide. Ovary spherical, pretesticular, 124–168 (136 6 15) long by 142–190 (169 6 20) wide. Uterus tubular, occupying space bounded by anterior testes, ventral sucker, and caeca. Egg in uterus, 68–76 (72 6 3) long by 29–37 (33 6 2) wide. Vitellarium bilateral, present between levels of posterior 1/5 and 2/5 of body length, consisting of 4–6 and 4–8 independent follicles on left and right sides, respectively. Excretory vesicle oval or Y-shaped, located beneath posterior testis. Excretory pore terminal.

Redia (based on 10 living specimens): Daughter redia translucent, 672–1,322 (1,012 6 191) long by 181–283 (228 6 33) wide, containing 15–23 mature and immature cercariae ( Fig. 5A ). Mouth present at anterior end with muscular pharynx. Prepharhynx invisible. Caecum thick, extending straight to level of anterior one-fourth of body length. Posterior lappets rudimentary.

Cercaria (based on 10 living specimens): Body oval, narrower in lower half, 393–575 (471 6 53) long by 164–210 (183 6 18) maximum wide ( Fig. 5B ). Tegument spineless. Oral sucker round, 54–85 (62 6 9) long by 54–85 (68 6 10) wide. Ventral sucker round, situated slightly below body midline, 52–78 (61 6 7) long by 54–89 (70 6 10) wide. Prepharynx present. Pharynx small, 30– 60 (45 6 9) long by 21–25 (23 6 2) wide. Caecum bifurcated. Excretory duct present near posterior end, forming closed loop. Tail unbranched, 276–532 (389 6 70) long by 22–41 (27 6 6) wide, with terminal gland.

Metacercaria (based on 10 living specimens): Cyst flask-shaped, 360–400 (385 6 14) long by 162–200 (189 6 13) wide in maximum ( Fig. 6 ). Neck portion of cyst narrow, 72–95 (80 6 8) wide in minimum. Excysted juvenile more slender than cercarial body, 464–612 (511 6 41) long by 102–155 (133 6 15) wide ( Fig. 5C ). Oral sucker 51–72 (61 6 7) long by 55–77 (67 6 7) wide. Ventral sucker, 56–70 (64 6 5) long by 51–75 (63 6 7) wide. Pharynx 33–60 (48 6 10) long by 15–25 (20 6 4) wide.

Taxonomic summary

Type host: Batillaria attramentaria (Sowerby, 1855)

Site of infection: Gonad and hepatopancreas.

Type locality: Kanonji, Kagawa Prefecture, Japan.

Natural definitive host: Unknown.

Experimental and accidental definitive hosts: Coturnix japonica Temminck and Schlegel, 1849 ; Homo sapiens Linnaeus, 1758 .

Site of infection of the definitive hosts: Conjunctival cavity.

Type specimens: The type series consists of 6 specimens (experimentally raised adults) deposited in Meguro Parasitological Museum (Tokyo, Japan); holotype ( MPM21745 ) and paratypes ( MPM21746 ) .

DNA sequences: The accession numbers of DDBJ/ENA/ GenBank databases are LC623767 (28S rDNA) and LC626029 – 57 (COI haplotypes).

ZooBank registration: urn:lsid:zoobank.org:act:C65CA007- 7181-42FB-89FE-A0C1B5F26CC7.

Synonymous taxa: Philophthalmid sp. 1 sensu Hechinger, 2007.

Etymology: The new species is named after Dr. Ryan F. Hechinger, who found it from B. attramentaria in Japan in 2003, provided provisional descriptions of the larval stages, and suggested that it was a species of Philopthalmus.

Remarks

The new species was morphologically compared with congeners in their adult stage. Species infecting the intestine of definitive hosts or having tubular vitellarium were excluded from the comparison because the new species was an eye-infecting parasite and had follicular vitellarium. As shown in Table I , the new species was distinguishable from other closely related congeners ( Braun, 1902; Penner and Fried, 1963; Howell and Bearup, 1967; Penner and Trimble, 1970; Kanev et al., 1993) by a combination of the following characteristics: the size of the whole body, the ratio of the width of the oral sucker to ventral sucker, the presence or absence of esophagus, the length of cirrus sac, the shape of testes, and the number of vitelline follicles. The new species is most similar to Philophthalmus hegeneri Penner and Fried, 1963 , from North America and P. lacrymosus from South America. The new species is distinguishable from P. hegeneri by the absence of an esophagus, the smaller size ratio of the oral sucker to ventral sucker, and the enlargement of the cirrus sac beyond the posterior margin of the ventral sucker. When compared with P. lacrymosus , a longer cirrus sac is distinctive of the new species. Further, the 28S rDNA and COI sequences of the new species are quite different from those of P. lacrymosus (see Figs. 2 , 3A ).

It is also possible to compare the larval stages of P. hechingeri to those of P. hegeneri , which have been described from the batillariid snail, Lampanella minima (Gmelin, 1791) , in seashores of the Gulf of Mexico ( Penner and Fried, 1963). The new species is distinguishable from P. hegeneri by the smaller size of the cercarial body ( Trimble and Penner, 1971). The flask-shaped metacercarial cyst of the new species has a relatively longer neck than that of P. hegeneri . The larval stage of P. lacrymosus is unknown, precluding comparison with its larval stages.

Figures

Figure 2. A maximum likelihood phylogenetic tree of the family Philophthalmidae. The tree was made using sequences of 28S rDNA (874 nucleotide sites) under the substitution model GTRþI. The tree was rooted by the outgroup taxon, Sphaeridiotrema globulus (GQ890331). The outgroup was removed from the tree to save space. The isolates obtained in this study are highlighted in bold face. The DNA accession number of each philophthalmid is shown in parentheses. Bootstrap percentages are indicated at branching points. A scale bar indicates the number of substitutions per nucleotide site.

Figure 3. Mitochondrial DNA-based genetic analyses of philophthalmid species. (A) A maximum likelihood phylogenetic tree of the genus Philophthalmus. The tree was made using sequences of COI (693 nucleotide sites) under the substitution model HKYþG. The DNA accession number of each taxon is shown in parentheses. The tree was rooted by the outgroup taxon, Fasciola hepatica (M93388). The outgroup was removed from the tree to save space. Bootstrap percentages are indicated at branching points. A scale bar indicates the number of substitutions per nucleotide site. (B) A parsimony network of COI haplotypes (849 nucleotide sites) of Philophthalmus hechingeri n. sp. in a seashore of the Seto Inland Sea. The size of circles indicates the frequency of the haplotypes. Numerals within the circles mean the number of haplotypes. A closed circle indicates a haplotype, which is identical to that of Philophthalmus sp. from human in Aichi Prefecture (Sato et al., 2019). Tiny circles are hypothetical haplotypes.

Figure 4. The adult stage of Philophthalmus hechingeri n. sp. Line drawing of ventral view. Abbreviations: c, cirrus; ca, caecum; cs, cirrus sac; gp, genital pore; mg, Mehlis’ gland; mt, metraterm; o, ovary; os, oral sucker; p, pharynx; sr, seminal receptacle; sv, seminal vesicle; t, testis; u, uterus; v, vitellarium; vs, ventral sucker.

Figure 5. The larval stages of Philophthalmus hechingeri n. sp. (A) Daughter redia. (B) Cercaria. (C) Excysted juvenile.

Figure 6. The flask-shaped metacercariae of Philophthalmus hechingeri n. sp.