Choeradoplana riutortae Lago-Barcia & Carbayo, 2021

Lago-Barcia, Domingo, Silva, Marcos Santos & Carbayo, Fernando, 2021, Revision and description of six species of Choeradoplana (Platyhelminthes, Tricladida), with an emendation to the genus, ZooKeys 1016, pp. 1-48 : 1

Choeradoplana riutortae Lago-Barcia & Carbayo sp. nov. Figures 19 , 20 , 21 , 22

Material examined.

All specimens were collected in the Parque Nacional da Serra dos Orgãos, Teresópolis, State of Rio de Janeiro, Brazil (-22.48, -43.06) by F. Carbayo and co-workers, January 6th, 2010. Holotype MZUSP 2274 (field code, F4218), transverse sections of the cephalic region on 5 slides; horizontal sections of the portion behind the cephalic region on 6 slides; sagittal sections of ovarian region on 6 slides; horizontal sections of the testes on 4 slides; transverse sections of the pre-pharyngeal region on 7 slides; sagittal sections of the pharynx and copulatory apparatus on 9 slides. Paratype MZUSP PL 1174 (field code, F4217), transverse sections of the cephalic region on 9 slides; horizontal sections of the ovarian region on 7 slides; transverse sections of the pre-pharyngeal region on 8 slides; sagittal sections of the pharynx and copulatory apparatus on 12 slides. Paratype MZUSP PL 2275 (field code, F4261), transverse sections of the pre-pharyngeal region on 16 slides; sagittal sections of the pharynx and copulatory apparatus on 27 slides.

Distribution.

Only known from the type locality, Parque Nacional da Serra dos Orgãos, municipality of Teresópolis, State of Rio de Janeiro, Brazil.

Etymology.

The specific epithet honors Prof. Marta Riutort for her contributions to understanding the evolution of flatworms.

Diagnosis.

Choeradoplana species with a light ivory background color covered by numerous sepia brown spots except for the anterior extremity which is red orange. The ventral surface is pale orange in the cephalic region, and light grey in the rest of the body. Part of the longitudinal cutaneous musculature is sunken in the parenchyma of the ventral side. The prostatic vesicle has a paired extrabulbar dish-shaped portion, and an elongated intrabulbar portion with an irregular epithelium. It has a short copulatory apparatus (the length:height ratio of the copulatory apparatus is 2.6:1). The male atrium presents the same size as the female atrium.

Description.

The preserved animals measure between 37-42 mm in length and 2.5-3 mm in width (n = 3). The body is slender and subcylindrical. The cephalic region is differentiated from the remaining body by a ‘neck’, laterally dilated and rolled up so that the ventral surface, provided with prominent glandular cushions, is facing out (Fig. 19A-C ); the posterior extremity is pointed. The creeping sole is as wide as 72-75% of body width in the pre-pharyngeal region (n = 3). The mouth is positioned at a distance from the anterior extremity equal to 63-67% of body length, and the gonopore is 72-78% (n = 3).

The dorsal coloration in live specimens consists of a light ivory (RAL 1015) background color, with numerous sepia brown (RAL 8014) spots which are more (F4218) or less (F4217) merged with each other, with the latter situation presenting a somewhat homogeneous aspect. A midline with the background color may extend along the body length (paratype F4217) or is restricted to the anterior region of the body (paratype F4261). The spots extend to the body sides, where they are scattered so as to create an irregular bordering line, followed by the background color of the sides of the body. A curled anterior extremity is red orange (RAL 2001). The ventral surface is pale red orange in the cephalic region, and light grey (RAL 7035) in the rest of the body (Fig. 19B ).

The eyes are formed by a one-pigmented cup of 46-50 μm in diameter. There are no halos around them. Eyes are absent in the very anterior extremity of the body equivalent to 1% of the body length (F4218). Eyes behind the anterior tip are distributed marginally in a row of two or three eyes and extend along the entire body until the posterior extremity.

Sensory pits are 15 μm deep, distributed ventro-laterally in a uniserial row initiating 0.3 mm behind the anterior extremity (the equivalent of 1% of the body length in paratype F4217), and from the very anterior tip in holotype.

In the pre-pharyngeal region, very abundant rhabditogen gland cells pierce the dorsal and marginal epidermis. These types of cells are scarce on the ventral epidermis; instead, there are gland cells producing erythrophil granules and scarce gland cells secreting cyanophil granules. There is no glandular margin (Fig. 19D ).

The cutaneous musculature of the pre-pharyngeal region consists of a subepithelial circular muscle, followed by a diagonal layer with decussate fibers, and a longitudinal muscle organized in bundles (Fig. 19D ). This longitudinal muscle is 80-100 μm-thick dorsally and organized in tight bundles with approximately 60-110 fibers each; it is ventrally divided into a 28-30 μm-thick muscle organized in bundles with 10-27 fibers each, and a 55-65 μm-thick muscle sunken into the parenchyma and constituted of bundles with 18-40 fibers each (Fig. 19D ). The thickness of the cutaneous muscle coat is 22-25% (n = 3) of the body height. There are three parenchymal muscles in the pre-pharyngeal region, namely a dorsal decussate muscle (46-50 μm thick), transverse supra-intestinal muscle (25-30 μm), and transverse subintestinal muscle (70-75 μm) (n = 3) (Fig. 19D ).

The cutaneous and parenchymal musculature is organized in the cephalic region as in Ch. iheringi . A portion of the retractor muscle of the head is delta-shaped in a cross-section and ranges between 2-5 mm (or 5-14% of body length) from behind, 1-1.3 mm (2-3%) of the anterior extremity of the body (Fig. 19E ), and its thickness equals 36% of the height of the cephalic region. The Muskelgeflecht is 200-210 μm thick (30% of body height). The subneural parenchymal muscle consists of transverse fibers. Glandular cushions are composed of very numerous rhabditogen cells and scarce gland cells produce erythrophil granules (Fig. 19E ).

The mouth is located in the middle of the pharyngeal pouch (n = 3) (Fig. 20A ). The pharynx is bell-shaped, and has its dorsal insertion shifted posteriorly with the equivalent to 44% of the pharynx length. The esophagus length is 20% of the pharyngeal length. The pharyngeal pouch is lined with a non-ciliated, low epithelium underlain by a one-fiber-thick layer of longitudinal muscle followed by 20 µm-thick layer of circular muscle. The outer pharyngeal epithelium is flat, ciliated, and underlain by a one-fiber-thick longitudinal muscle, followed by a 15 µm-thick muscle with some longitudinal fibers interspersed. The inner pharyngeal epithelium is flat, ciliated, and underlain by a mixed layer of circular muscle with longitudinal muscle (75 μm thick). The pharynx presents numerous erythrophil and xanthophil gland cells interspersed.

The testes are mature and dorsally located under the supra-intestinal transverse muscle layer, mostly placed between the intestinal diverticula. They extend from 12.7 mm (30% of body length, holotype) of the anterior extremity of the body to 0.5 mm before the root of the pharynx. Sperm ducts run immediately above the subintestinal parechymatic muscle layer. The sperm ducts bend dorsally close to the copulatory apparatus, and subsequently penetrate the ventral proximal region of the common muscle coat to open into the respective dilated branch of the prostatic vesicle (Fig. 20B ). The prostatic vesicle is divided into two differentiated halves; the anterior half proximally presents a dilated and paired portion oriented vertically which opens into a broadened, dish-shaped section located above the paired portion (Figs 20B , 21A, B ). This proximal half is extrabulbar and lined by a columnar-to-cuboidal epithelium which is pierced by gland cells producing xanthophil granules. These gland cells are much more abundant in the dish-shaped portion, and present a reddish appearance; the border of this dish-shaped section of the prostatic vesicle is also pierced by gland cells producing cyanophil granules. The distal half is intrabulbar, and is a straight tube running postero-dorsally to open into the proximal region of the male atrium. This half is lined by a columnar epithelium with a sinuous surface which is pierced along its whole length by gland cells producing cyanophil granules; additionally, gland cells producing xanthophil granules pierce its distal portion. The lining epithelium of the proximal half of the prostatic vesicle is coated by a 20 μm-thick circular muscle; the distal half is coated by a 1 µm-thick circular muscle, followed by a 15 µm-thick longitudinal muscle. The male atrium is the same size as the female atrium, and is divided into a proximal, narrow half and a distal, dilated half with some small folds (Figs 21 , 22 ).

The male atrium is lined by a cuboidal, non-ciliated epithelium, and underlain by a 45-80 µm-thick layer of circular muscle with numerous interspersed longitudinal fibers (n = 3). The proximal half of the atrium receives two types of gland cells, one producing erythrophil granules, and a second type of scarce gland cells producing xanthophil granules; the distal half of the male atrium receives abundant gland cells producing xanthophil granules and the sub-apical portion of the cells of the lining epithelium contains xanthophil granules. The extrabulbar portion of the prostatic vesicle is coated by additional muscle fibers attaching it to the common muscle coat (Figs 21 , 22 ).

The ovaries are mature, ovoid, 190 μm in length, and placed above the ventral nerve plate, and at a distance from the anterior body tip equal to 27% of body length (11.5 mm from anterior tip) (holotype). Ovovitelline ducts emerge from the dorso-lateral aspect of the ovaries and run above the ventral nerve plate. Lateral to the female atrium, the ovovitelline ducts bend medially and dorsally, then unite above the postero-dorsal section of the female atrium (Figs 21 , 22 ). The common glandular ovovitelline duct is outside the common muscle coat, and runs posteriorly, progressively inclining to the ventral side to communicate with the posterior section of the female atrium.

The female atrium is divided into a dilated canal running ventro-anteriorly and outside the common muscle coat, and a distal, funnel-shaped half is widely communicated with the male atrium (Figs 21 , 22 ). The female atrium is lined with a 35 µm high epithelium. This epithelium is pierced by gland cells producing fine erythrophil granules. The subapical portion of lining cells of the distal half of the atrium contains xanthophil granules. The lining epithelium of the female atrium is underlain by a layer of mixed circular and longitudinal fibers 10 µm high.

The common muscle coat is a very dense layer composed by densely packed muscle fibers variously oriented (Figs 21 , 22 ). The length:height ratio of the copulatory apparatus enveloped by the common muscle coat ranges between 2.2-2.7:1 (n = 3).

Remarks.

Choeradoplana riutortae Lago-Barcia & Carbayo, sp. nov. matches all diagnostic characteristics of Choeradoplana . The external dorsal coloration resembles 11 species inside the genus with the background color being brownish with dark black or dark brown spots over it, namely Choeradoplana abaiba , Ch. agua , Ch. banga , Ch. benyai , Ch. bocaina , Ch. cyanoatria , Ch. longivesicula , Ch. pucupucu , and the herein described Ch. onae Lago-Barcia & Carbayo, sp. nov., Ch. eudoxiae Silva & Carbayo, sp. nov. and Ch. claudioi Lago-Barcia & Carbayo, sp. nov. However, none of them present the prominent cushions found in this species, nor the conspicuous red-orange coloration of the cephalic region.

With respect to the internal morphology, Ch. riutortae Lago-Barcia & Carbayo, sp. nov. is only similar to Ch. onae Lago-Barcia & Carbayo, sp. nov., Ch. bocaina and Ch. claudioi Lago-Barcia & Carbayo, sp. nov. in that the extrabulbar section of the prostatic vesicle is dish-shaped. However, the female atrium in Ch. claudioi Lago-Barcia & Carbayo, sp. nov. is partially below the male one (vs. behind, in Ch. riutortae Lago-Barcia & Carbayo, sp. nov.), whereas the male atrium in Ch. onae Lago-Barcia & Carbayo, sp. nov. has the same height along its length, (vs. a proximal, narrow half, and a distal, widened half). Finally, the male atrium in Ch. bocaina is 3 × as long as the female, whereas this ratio is 1.2 in Ch. riutortae Lago-Barcia & Carbayo, sp. nov.

Figures

Figure 19. Choeradoplana riutortae Lago-Barcia & Carbayo, sp. nov. A dorsal view of the creeping live paratype F 4217 B the live holotype twisted showing the ventral surface C dorsal view of the anterior region of paratype F 4217 D photomicrograph of a transverse section of the pre-pharyngeal region of holotype E photomicrograph of a transverse section of the cephalic region of holotype. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.

Figure 20. Choeradoplana riutortae Lago-Barcia & Carbayo, sp. nov., holotype. Photomicrographs of sagittal sections A pharynx B prostatic vesicle. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.

Figure 21. Choeradoplana riutortae Lago-Barcia & Carbayo, sp. nov., holotype A photomicrograph of a sagittal section of the copulatory apparatus C Diagrammatic representation of the copulatory apparatus. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.

Figure 22. Choeradoplana riutortae Lago-Barcia & Carbayo, sp. nov. Photomicrographs of sagittal sections A copulatory apparatus of paratype F 4217 B copulatory apparatus of paratype F 4261. Abbreviations: cm common muscle coat, co common glandular ovovitelline duct, dd decussate dorsal cutaneous muscles, dm diagonal decussate muscles, e eye, ej ejaculatory duct, ep esophagus, er erythrophil secretion, fa female atrium, fd female genital duct, g gonopore, i intestine, lc longitudinal cutaneous muscles, ma male genital atrium, mk Muskelgeflecht (Graff, 1899), mo mouth, o ovary, ov ovovitelline duct, ph pharyngeal pouch, pp penis papilla, pv prostatic vesicle, px pharynx, rg rhabditogen glands, r retractor muscle, sb subintestinal transverse muscles, sd sperm duct, sg shell glands, sk sunken longitudinal cutaneous muscles, sm spermatophore, sn subneural transverse muscles, sp supra-intestinal transverse muscles, t testis, vi vitellaria, vn ventral nerve plate.