Emoleptalea Looss, 1900

Curran, Stephen S., Dutton, Haley R., Warren, Micah B., Preez, Louis du & Bullard, Stephen A., 2021, Two new species of Cephalogonimidae Looss, 1899 (Digenea: Plagiorchioidea) from Africa (Mozambique and Guinea), including a new phylogenetic hypothesis for related plagiorchioids, International Journal for Parasitology: Parasites and Wildlife 14, pp. 228-240 : 229-232

3.1. Genus Emoleptalea Looss, 1900

Emoleptalea mozambiquensis n. sp.

3.1.1. Description ( Figs. 1–3 )

[Based on three mature specimens] Body oval, 1050–1160 long, 480–520 wide at mid-body. Tegument spinous, spines minute, 5–6 long, becoming sparser near the posterior end. Oral sucker sub-terminal on ventral surface, subspherical with posterior margin truncated, 113–123 long, 115–123 wide. Prepharynx 20–25 long. Pharynx wider than long, 37–53 long, 68–75 wide. Oesophagus very short, 10 long in a single measurable specimen. Ventral sucker pre-equatorial, nearly circular, 125–138 long, 125–135 wide. Oral to ventral sucker width ratio 1:1.01–1.17. Forebody 300–325 long or 28% of body length. Intestine bifurcating in forebody at about halfway between suckers, caeca blind, terminating in vicinity of middle of post-testicular space. Postcaecal space 250–290 long or 22–27% of body length.

Testes subglobular, oblique, slightly overlapping with each other or separated by slight space, largely intercaecal but anterior testis overlapping caeca on one specimen; anterior testis 175–215 long, 168–205 wide, posterior testis 198–205 long, 198–220 wide. Post-testicular space 325–390 long or 31–34% of body length. Cirrus sac curving in a reverse C-shape, extending to near anterior margin of ventral sucker and partially overlapping sucker, 335–414 long, 60–70 wide. Cirrus sac containing bipartite seminal vesicle, pars prostatica with well-defined

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Species Family GenBank Reference accession no. a

Suborder Monorchiata

Monorchioidea

Lissorchis kritskyi Lissorchiidae EF 032689 Curran et al. (2006) Suborder Xiphidiata

Gorgoderoidea

Encyclometra Encyclometridae AF 184254 Tkach et al. (2000b) colubrimorum

Gorgodera Gorgoderidae AF 151938 Tkach et al. (2000b) cygnoides

Xystretrum solidum Gorgoderidae KF 013188 Cutmore et al.

(2013) Microphalloidea

Maritrema poulini Microphallidae KJ 144177 Presswell et al. (2014)

Maritrema Microphallidae AY 220631 Tkach et al. (2003) prosthometra

Prosthogonimus Prosthogonimidae MN 726975 Schwelm et al. ovatus (2020)

Plagiorchioidea

Auridistomum Auridistomidae AY 116872 Olson et al. (2003) chelydrae

Brachycoelium Brachycoeliidae AF 151935 Tkach et al. (2000a) salamandrae

Cephalogonimus Cephalogonoimidae HM137615 Razo-Mendivil and americanus P´erez-Ponce de

Le´on (2011) Cephalogonimus Cephalogonimidae AY 222276 Olson et al. (2003) retusus

Choanocotyle Choanocotylidae EU 196356 Tkach and Snyder hobbsi (2007)

Choanocotyle Choanocotylidae EU 196358 Tkach and Snyder nematoides (2007)

Dasymetra nicolli Reniferidae AF 433672 Tkach et al. (2001b) Emoleptalea Cephalogonimidae MW 586927 Present study mozambiquensis

n. sp.

Glypthelmins Glypthelminthidae HM 137608 Razo-Mendivil and pennsylvaniensis P´erez-Ponce de

Le´on (2011) Glypthelmins quieta Glypthelminthidae AY 222278 Olson et al. (2003) Haematoloechus Haematoloechidae AF 151916 Tkach et al. (1999) varigatus

Heterorchis cf. Incertae sedis MW 586924 Present study protopteri

Leptophallus Leptophallidae AF 151914 Tkach et al. (1999) nigrovenosus

Macrodera Leptophallidae AF 151913 Tkach et al. (1999) longicollis

Macroderoides Macroderoididae EU 850398 Tkach et al. (2008) texanus

Macroderoides Macroderoididae HQ 680849 Tkach and Kinsella typicus (2011)

Masenia baroensis Cephalogonimidae MW 586925 Present study

n. sp.

Masenia Cephalogonimidae MH 142268 Dumbo et al. nkomatiensis (2019a)

Mesocoelium sp. Mesocoeliidae AY 222277 Olson et al. (2003) Mesocoelium sp. Mesocoeliidae AF 433677 Tkach et al. (2001b) Neoglyphe locellus Plagiorchiidae AF 300330 Tkach et al. (2001a) Neoglyphe sobolevi Plagiorchiidae AF 300329 Tkach et al. (2001a) Omphalometra Omphalometridae AF 300333 Tkach et al. (2001a) fexuosa

Opisthioglyphe Telorchiidae AF 151929 Tkach et al. (2001a) ranae

Orientocreadium Orientocreadiidae MK 496882 Dumbo et al. batrachoides (2019b) Orientocreadium Orientocreadiidae MF 611697 Sokolov and pseudobagri Shchenkov (2017)

Leptophallidae AF 151910 Tkach et al. (1999)

Table 1 (continued)

prostatic bulb, and elongated cirrus (apparently unarmed). Proximal portion of bipartite seminal vesicle larger than distal portion; proximal portion 85–139 long, 53–63 wide; distal portion 75 long, 58–65 wide. Prostatic bulb pear-shaped, 43–53 long, 25–33 wide. Cirrus 165–188 long. Cirrus sac communicating with genital atrium dorsal to ventral sucker; genital atrium 26–38 long, 13–15 wide. Genital pore opening dorso-median, immediately posterior to anterior margin of oral sucker.

Ovary subglobular, submedian, amphitypic, situated on same side as posterior testis, 160–173 long, 140–148 wide. Seminal receptacle a transversely elongated to nearly subspherical sac containing sperm, dorso-median to and overlapping ovary, always smaller than ovary, 98–125 long, 75–80 wide. Oviduct leaving anterior ovary, extending toward median line of body, forming ootype surrounded by Mehlis’ gland between ovary and anterior testis (not clearly observed, partially observable in one dorsal specimen). Laurer’ s canal communicating with oviduct near junction with seminal receptacle, leading toward dorsal surface, opening at ovarian level on dorsal surface. Vitellarium comprised of two lateral bands of large irregularly shaped follicles; follicles surrounding caeca, extending from level at posterior margin of pharynx to approximately posterior third of testicular zone. Vitelline reservoir roughly triangular, median, or slightly submedian, overlapping posterior third of ventral sucker, situated ventral relative to ovary but with collection ducts running dorsal to ovary and anterior testis. Proximal uterus descending from ovarian complex between testes in dorsal hindbody, coiling extensively and occupying most of hindbody. Distal uterus ascending ventrally on ab-ovarian side. Metraterm thickwalled, adjacent to dorsally, and following path of cirrus sac, 190–275 long, 25–33 wide (width measured near proximal end). Eggs filling uterus, oval, operculated; distal eggs 23–25 long, 13–18 wide.

Excretory bladder Y-shaped, main stem (visible only in largest specimen), 310 long or 27% of body length, branching 50 posteriorly from posterior margin of posterior testis. Excretory system opening through excretory pore at terminal end with glandular cells surrounding stem near pore.

Type host: turquoise killifish, Nothobranchius furzeri Jubb, 1971 , (Cyprinidontiformes: Nothobranchiidae ).

Site in host: intestine.

Type locality: Karingani Game Reserve , Mozambique .

Prevalence: 3 worms infected one of five fish examined.

Specimens deposited: Holotype USNM 1642499 ; 2 paratypes USNM 1642450-1 .

Sequence deposited: GenBank No. MW586927.

ZooBank Life Science Identifier: urn:lsid:zoobank.org:pub:00977A33-A27A-4150-9385-7AF29064523C .

Etymology: The species is named for the country from which it was originally collected.

3.1.2. Remarks Emoleptalea mozambiquensis n. sp. conforms to the diagnosis for the

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Cephalogonimidae in having a small oval body, spinous tegument, genital pore at anterior extremity, and being parasitic in the digestive tract of a freshwater fish ( Jones and Bray, 2008). We placed the new species in Emoleptalea because the excretory vesicle lacks lateral diverticula, testes are oblique, the vitelline follicles are in lateral groups that span the region of the ventral sucker, and anterior tegumental spines are not enlarged and do not form a circumoral circlet. The new species has an amphitypic ovary ( Fischthal and Kuntz, 1963). Two of the three specimens had the ovary on the right side of midline and the third had the ovary on the left side of midline. The cirrus sac approached the genital atrium from the left side of the body, the anterior testis was on the left side, and the seminal receptacle on the right in the two similar specimens ( Fig. 1 ). In contrast, the positions of these same gonadal organs were reversed in the single specimen with the ovary on the right side ( Figs. 2 and 3 ).

There were nine accepted species belonging in Emoleptalea , all of which infect freshwater catfishes as adults. The discovery of E. mozambiquensis in a non-catfish host is remarkable but considering that only three specimens were collected from a single infected fish we cannot rule out the possibility that N. furzeri represents an accidental host and additional survey of a broad variety of fishes from the type-locality should be conducted. Four of the accepted species were described and are known from Africa: Emoleptalea exilis ( Looss, 1899) Looss, 1900 , Emoleptalea synodontidos Dollfus, 1950 , Emoleptalea rifaati ( Ramadan, Saoud & Taha, 1987) Jones & Bray, 2008 , and Emoleptalea nwanedi King, Smit, Baker & Luus-Powell, 2018 . Five species were described and are known from India: Emoleptalea horai ( Gupta, 1955) Jones & Bray, 2008 , Emoleptalea dollfusi Srivastava, 1960 , Emoleptalea loossi Srivastava (1960) , Emoleptalea hardayali (Kumar & Agrawal, 1980) Jones and Bray (2008) , and Emoleptalea kanungoi ( Agrawal and Agrawal, 1985) Jones & Bray, 2008 . Emoleptalea mozambiquensis is herein differentiated from eight congeners using combinations of features, including body size and shape, characteristics of suckers, gonads, digestive system, and position of the genital pore. We refrain from making comparisons with E. dollfusi and discuss this below.

Emoleptalea mozambiquensis differs from the type-species, E. exilis , which infects the bayad, Bagrus bajad (Forsskål) in the Nile River, Egypt, by having a more oval, less elongated body, oral sucker slightly smaller rather than much larger than the ventral sucker, shorter forebody representing 28% rather than 35% of body length, and more elongated bands of irregular vitelline follicles extending well into the testicular zone rather than condensed bands of elongated follicles confined posteriorly to the ovarian zone ( Looss, 1899).

Emoleptalea mozambiquensis resembles E. synodontidos , which infects the onespot squeaker, Synodontis notatus Vaillant, in the Democratic

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1:1.01–1.17 compared with 1.07–1.16: 1 in E. rifaati ), testes more anterior in the hindbody (post-testicular space 31–34% of body length) compared with ~19% in E. rifaati , and having vitelline bands extending well into the forebody compared with limited to the anterior margin of the ventral sucker in E. rifaati ( Ramadan et al., 1987) .

Emoleptalea mozambiquensis differs from E. nwanedi , which infects the silver catfish, Schilbe intermedius Rüppell , in Limpopo Province, South Africa, by having a larger body (1050–1160 μm compared with 582–722 μm long), a subspherical rather than elongated oral sucker, seminal receptacle smaller rather than larger than ovary, and the genital pore opens dorso-median near the anterior end of the body instead of submedian at the lateral edge of the ventral sucker as in E. nwanedi ( King et al., 2018) .

Republic of the Congo, but may be differentiated by having a smaller body (1050–1160 μm compared with 1770 μm long), much shorter oesophagus (10 μm compared with 48 μm long), and most significantly, the genital pore opens dorso-median near the anterior end of the body instead of submedian on the ventral surface at a level even with the posterior margin of the ventral sucker ( Dollfus, 1950).

Emoleptalea mozambiquensis differs from E. horai , which infects the stinging catfish, Heteropneustes fossilis (Bloch) , in India, by having a subspherical rather than a funnel-shaped oral sucker, caeca extending into the post-testicular space rather than limited to the posterior margin of the ovary, and by having the genital pore opening dorso-median near the anterior end of the body instead of ventro-lateral on the left side at the level of the pre-pharynx ( Gupta, 1955).

Emoleptalea mozambiquensis resembles E. loossi , which was described on the basis of specimens from H. fossilis in India, but may be differentiated by the near absence of a prepharynx and oesophagus (20–25 μm long and 0–10 μm long, respectively) compared with each being about the pharynx length, a shorter forebody (~28% compared with ~34% of body length), genital pore not submedian at the anterodorsal margin of oral sucker, and having more extensive vitelline bands that span the ventral sucker region and enter the forebody compared with being confined anteriorly at mid-ventral sucker level ( Srivastava, 1960).

Emoleptalea mozambiquensis differs from E. hardayali , which infects the striped dwarf catfish, Mystus vittatus (Bloch) , in India, by having oblique rather than tandem testes and the genital pore opening dorso-median near the anterior end of the body instead of ventrally in the pharyngeal zone ( Agrawal and Agrawal, 1985).

Emoleptalea mozambiquensis differs from E. kanungoi , which infects the freshwater bagrid catfish Rita rita (Hamilton) , in India, by having a subspherical rather than a funnel-shaped oral sucker, a short oesophagus, caeca extending into the post-testicular space rather than limited to the posterior margin of the testes, and a genital pore opening dorso-median near the anterior end of the body instead of laterally on the right side at the mid-level of the oral sucker ( Agrawal and Agrawal, 1985).

Emoleptalea mozambiquensis resembles E. rifaati , which infects two mochokid catfishes ( Synodontis schall [Bloch & Schneider] and Synodontis serratus Rüppell), in the Nile River Delta, Egypt, but may be differentiated by having a subspherical rather than funnel-shaped oral sucker, having the oral sucker slightly smaller than ventral sucker rather than the reverse condition (oral to ventral sucker width ratio

Figures

Fig. 1. Emoleptalea mozambiquensis n. sp. from intestine of turquoise killifish, Nothobranchius furzeri Jubb. Ventral view of holotype. Eggs are omitted from uterus and outline of uterus does not show extensive coiling. Abbreviations: caecum, c; cirrus sac, cs; excretory bladder, eb.

Fig. 2. Emoleptalea mozambiquensis n. sp. from intestine of turquoise killifish, Nothobranchius furzeri Jubb. Dorsal view of anterior end. Note the caeca are surrounded by the vitelline follicles and the terminal genitalia run ventral relative to caeca. This specimen has the ovary on the left side of body. Abbreviations: caecum, c; cirrus, ci; distal portion of seminal vesicle, ds; distal uterus, du; egg, e; genital atrium, ga; genital pore, gp; prostatic bulb, pb; proximal portion of seminal vesicle, ps.

Fig. 3. Emoleptalea mozambiquensis n. sp. from intestine of turquoise killifish, Nothobranchius furzeri Jubb. Dorsal view of ovarian complex. Mehlis’ gland cells and eggs are omitted. Abbreviations: anterior testis, at; Laurer’s canal, Lc; ovary, ov; oviduct, od; ootype, oo; posterior testis, pt; proximal uterus, pu; seminal receptacle, sr; vitelline follicle, vf; vitelline reservoir, vr.