Leuceruthrus Marshall and Gilbert, 1905

Bullard, Matthew R. Womble and Stephen A., 2022, Azygiid Parasites Of North American Endemic Pleurocerids And Centrarchids: Revision Of Leuceruthrus Marshall And Gilbert, 1905 (Digenea: Azygiidae), Description Of Two New Species, And Phylogenetic Analysis, Journal of Parasitology 108 (4), pp. 374-394 : 378-380

Leuceruthrus Marshall and Gilbert, 1905 , emended

( Figs. 1 18 ; Tables I , II)

Diagnosis: Adult body large, lingulate, broadly rounded anteriorly and tapering posteriad, forebody shorter than hindbody. Excretory system Y-shaped, with 2 branches joining within intercecal space in hindbody. Oral sucker subterminal. Ventral sucker smaller than oral sucker. Mouth anteroventral, subterminal. Pharynx at level of posterior margin of oral sucker; esophagus bifurcating immediately posterior to pharynx; esophageal branches joining with intestinal ceca; intestinal ceca inverse U-shaped inclusive of esophageal branches, comprising paired dextral and sinistral ceca, extending sinuously posteriad approximately parallel with lateral body margin. Testes 2 in number, intercecal, preovarian, immediately posterior to ventral sucker. Prostatic sac medial, anterior to ventral sucker. Seminal vesicle convoluted, entirely within prostatic sac. Pars prostatica present. Ejaculatory duct straight. Terminal genitalia joining within sinus organ; hermaphroditic pore opening into genital atrium; genital atrium communicating with hermaphroditic pore and genital pore; genital pore medial, immediately anterior to ventral sucker, posterior to anterior margin of prostatic sac. Ovary medial, intercecal, posttesticular. Laurer’s canal present. Uterus distributing primarily within hindbody, occupying nearly all intercecal space between ovary and ventral sucker, originating posterior to testes, extending between testes. Metraterm present. Vitellarium follicular, ventral to ceca, not extending anteriad into forebody, bilaterally symmetrical, extending along lateral margins of body ventral to ceca, not becoming confluent posteriorly. Uterine eggs densely distributed throughout uterus. Parasitic in stomach of North American freshwater fishes (typically of Centrarchidae ). Cercaria furcocystocercous, comprising distome (‘‘cercarial body,’’ the individual that develops into the adult) and tail (tail stem and paired furcae). Distome oblong. Oral sucker subterminal. Ventral sucker smaller than oral sucker. Alimentary system (mouth, pharynx, esophagus, ceca) as in adult. Position of testes and prostatic sac as in adult. Female genitalia present as anlagen only. Ovary posttesticular. Uterus originating posterior to testes, passing between testes. Uterine eggs not observed (cercaria is evidently not progenetic). Parasitic in North American freshwater snails of Pleuroceridae and typically of black basses ( Micropterus spp. ).

Type species: Leuceruthrus micropteri Marshall and Gilbert, 1905 .

Other species: Leuceruthrus stephanocauda ( Faust, 1921) n. comb. and Leuceruthrus ocalana ( Smith, 1935) n. comb.

Differential diagnosis: Adult body lingulate, broadly rounded anteriorly and tapering posteriad. Testes 2 in number, paired, preovarian, immediately posterior to ventral sucker. Ejaculatory duct straight. Ovary posttesticular. Uterus originating posterior to testes, extending between testes. Vitellarium not extending anteriad into forebody, not becoming confluent posteriorly. Genital pore immediately anterior of ventral sucker, posterior to anterior margin of prostatic sac. Cercaria furcocystocercous, comprising distome and tail stem having paired furcae. Testes paired, preovarian. Evidently not progenetic.

Taxonomic remarks on Leuceruthrus

Leuceruthrus , Azygia , and Proterometra comprise azygiids that infect freshwater fishes and that have a straight ejaculatory duct, a vitellarium that is not confluent posteriorly, and a genital pore immediately anterior to the ventral sucker (Marshall and Gilbert, 1905; Manter, 1926; Stunkard, 1956; Gibson, 2002; Gibson et al., 2002; Womble et al., 2015). Otodistomum includes marine and estuarine species that infect stomach and body cavity of chondrichthyans (Gibson and Bray, 1977). It differs from the freshwater azygiid genera by having a coiled ejaculatory duct, a vitellarium that is confluent posteriorly, and a genital pore near the pharynx and anterior to the prostatic sac (Marshall and Gilbert, 1905; Goldberger, 1911; Manter, 1926; Stunkard, 1956; Wootton, 1957; Schell, 1972; Gibson and Bray, 1977; Curran and Overstreet, 2000; Barger, 2014; Womble et al., 2015). Leuceruthrus and Azygia reportedly lack progenetic cercariae and mature in the stomach and intestine, respectively, of fishes ( Stunkard, 1956; Wooton, 1957; present study). They have a vitellarium that does not extend anteriad into the forebody and a uterus that fills the intercecal space between the ovary and ventral sucker. Leuceruthrus has oblique and preovarian testes, whereas Azygia has tandem and postovarian testes (Marshall and Gilbert, 1905; Goldberger, 1911; Manter, 1926; Stunkard, 1956; Wootton, 1957; Gibson, 2002; Barger, 2014; Womble et al., 2015). Proterometra includes progenetic cercariae, comprises ectoparasites of the buccal cavity ( Womble et al., 2015), and further differs from Azygia and Leuceruthrus by having a suboval body with broadly rounded ends, testes abreast in the posterior body extremity, and a uterine field and vitellarium extending well anteriad into the forebody (Gibson, 2002; Womble et al., 2015).

Relative to other azygiid genera, Leuceruthrus has been relatively little studied regarding azygiid systematics. Manter (1926) reviewed and redescribed all ‘‘forms’’ of Azygia from North America and accepted Azygia acuminata Goldberger, 1911 , Azygia angusticauda (Stafford, 1904) Manter, 1926 , and Azygia longa (Leidy, 1851) Manter, 1926 . He also reviewed several European species, which he suspected were conspecific with A. lucii . Stunkard (1956) also reviewed Azygia , accepted Azygia sebago Ward, 1910 , demonstrated its life cycle, and concluded that A. lucii (long considered endemic to Europe) ranged in North America. Wootton (1957) reviewed the cercariae of Azygia and determined the life cycle of A. acuminata . Manter (1926) provided a detailed study of Otodistomum cestoides (van Beneden, 1871) Odhner, 1911 from the Atlantic Ocean. Gibson and Bray (1977) later reviewed Otodistomum , redescribed O. cestoides and Otodistomum veliporum (Creplin, 1837) Stafford, 1904 , detailed Otodistomum plunketi Fyfe, 1953 , described metacercariae of these species from a variety of hosts, and summarized the available information regarding metacercariae of Otodistomum spp. For Proterometra, Horsfall (1934) and Dickerman (1934) described adults and cercariae of the type species Proterometra macrostoma (Faust, 1918) Horsfall, 1933 . Womble et al. (2015, 2016a, 2016b) treated life cycles and revised the taxonomy of 5 species of Proterometra . Marshall and Gilbert (1905) made Leuceruthrus available for L. micropteri but did not diagnose the genus, provide insights on generic vs. specific features, or compare the type species with other azygiids. Goldberger (1911) supplemented their description of L. micropteri and diagnosed Leuceruthrus ; however, neither Marshall and Gilbert (1905) nor Goldberger (1911) assigned the genus to a family. Goldberger (1911, p. 32) stated, ‘‘ Leuceruthrus will be found to represent the type of at least a new subfamily...and probably of a new family.’’ Based on similarities of the male genitalia between Azygia spp. and L. micropteri, Odhner (1911) assigned Leuceruthrus to Azygiidae (see Manter, 1926). Yamaguti (1958) provided the only diagnosis of the genus that considered comparable features in other azygiid genera. Yamaguti (1971), Gibson and Bray (1979), and Gibson (2002) provided diagnoses for the subfamily Leuceruthrinae Goldberger, 1911 . Leuceruthrus herein is emended to include features of the body, alimentary system, genitalia, and cercaria.

Figures

Figures 1, 2. (1) Adult of Leucer- uthrus micropteri Marshall and Gil- bert, 1905 from largemouth bass, Micropterus salmoides from Wheeler Reservoir, Alabama (USNM 1593581) showing mouth (m), oral sucker (os), pharynx (p), ceca (c) near origin, prostatic sac (ps), genital atrium (ga), genital pore (gp), ventral sucker (vs), distal end of uterus (ud), testes (t), vitellarium (vi), uterus origin (uo) near ovary (o), vitelline reservoir (vr), con- fluence of excretory ducts (ed), excre- tory bladder (eb), and excretory pore (ep). Ventral view. (2) Terminal male genitalia of L. micropteri (USNM 1593581) showing comparable features as illustrated in Fig. 1 plus seminal vesicle (sv), pars prostatica (pp), me- traterm (mt), and hermaphroditic pore (hp). Ventral view.

Figures 3–8. Naturally shed cercaria of Leuceruthrus cf. stephanocauda from Elimia spp. from Big Canoe Creek, Alabama. (3) Cercaria (USNM 1593584) showing tail cavity opening (tco), position of tail stem spines (s), anterior (ats) and posterior tail stem (pts) regions, location of the distome, showing pharynx (p), ceca (c), prostatic sac (ps), ventral sucker (vs), testes (t), ovary (o),, and paired lanceolate furcae (f). Dorsal view. (4) Anterior tail stem region showing anterior row of tail stem spines (arrowheads). (5) Tail stem spine. (6) Tail stem spine. (7) Anterior tail stem showing posterior row of tail stem spines (arrowheads). (8) Posterior tail stem showing marginal placement of associated protuberances (p).

Figures 9–14. Leuceruthrus from Holmes Creek, Florida. (9–13) Naturally shed cercaria of Leuceruthrus ksepkai n. sp. from Elimia floridensis from Holmes Creek, Florida. (9) Cercaria (USNM 1593587) showing tail cavity opening (tco), position of anterior ridge (ar), and anterior collar (ac), anterior (ats) and posterior tail stem (pts) regions, location of the distome, showing pharynx (p), ceca (c), prostatic sac (ps), ventral sucker (vs), testes (t), ovary (o), and paired oblong furcae (f). Dorsal view. (10) Anterior portion of tail stem accommodating the withdrawn distome. (11) Illustration of posterior tail stem showing position of associated protuberances. (12) Posterior tail stem showing position of associated protuberances. SEM. (13) Highmagnification view of a posterior tail stem protuberance. SEM. (14) Adult of Leuceruthrus cf. ksepkai from stomach of largemouth bass, Micropterus salmoides from Holmes Creek, Florida (USNM 1593590) showing mouth (m), pharynx (p), ceca (c), prostatic sac (ps), genital pore (gp), ventral sucker (vs), testes (t), distal portion of uterus (ud), vitellarium (vi), origin of uterus (uo), ovary (o), vitelline reservoir (vr), excretory duct (ed), excretory bladder (eb), and excretory pore (ep). Ventral view.

Figures 15–17. Naturally shed cercaria of Leuceruthrus blaisei from Elimia sp. 2 from Simmons Creek, Alabama. (15) Cercaria (USNM 1593592) showing pharynx (p), ceca (c), prostatic sac (ps), ventral sucker (vs), ovary (o), testes (t), and furcae (f). Dorsal view. (16) Anterior tail stem showing tegumental protuberances densely distributed near tail cavity opening (arrowheads). (17) Furcae (f).

Figure 18.—Maximum likelihood phylogenetic tree based on the internal transcribed spacer 2 (ITS2). Support values aside each node. Cercariae accompany the end of each branch.