Cratera cuarassu, Carbayo, Fernando & Almeida, Ana Laura, 2015

Carbayo, Fernando & Almeida, Ana Laura, 2015, Anatomical deviation of male organs of land planarians from Rio de Janeiro, Brazil, with description of two new species of Cratera (Platyhelminthes, Tricladida), Zootaxa 3931 (1), pp. 27-40 : 29-33

Cratera cuarassu sp. nov.

Etymology. The name cuarassu is a free composition of the Tupi (indigenous Brazilian language) words cuara (meaning hole, cave) and assu (meaning large (Tibiriçá, 1984)). It refers to the large intra-penial cavity.

Type material. All specimens were collected in areas covered with Atlantic forest in the Parque Estadual do Desengano, Santa Maria Madalena, State of Rio de Janeiro, Brazil, by Júlio Pedroni et al. (see Acknowledgements). Holotype PL 348 (field number, F2189): (S 2152'36'', W 4155'11''). 18/Mar/2008. Anterior end: sagittal sections on 5 slides; portion containing ovaries: sagittal sections on 64 slides; body region posterior to ovaries: horizontal sections on 27 slides; pre-pharyngeal region: transverse sections on 20 slides; pharynx: sagittal sections on 40 slides; copulatory apparatus: sagittal sections on 76 slides. Paratype PL 349 (field number, F2191): (S 2152'17'', W 4154'53''). 17/Mar/2008. Portion containing ovaries: horizontal sections on 31 slides; body region posterior to ovaries: sagittal sections on 57 slides; pre-pharyngeal region: transverse sections on 17 slides; copulatory apparatus: sagittal sections on 70 slides. Paratype PL 350 (field number, F2192): (S 2152'36'', W 4155'11''). 18/Mar/2008. Anterior end: horizontal sections on 3 slides; pre-pharyngeal region: transverse sections on 12 slides; pharynx and copulatory apparatus: sagittal sections on 82 slides. Paratype PL 351 (field number, F2193): (S 2152'36'', W 4155'11''). 18/Mar/2008. Pre-pharyngeal region: transverse sections on 32 slides; copulatory apparatus: sagittal sections on 45 slides. Paratype PL 809 (field number, F4074): 13/Aug/2009. Incompletely mature. Pharynx and copulatory apparatus: sagittal sections on 6 slides. Paratype PL 805 (field number, F4006): Preserved in 80% ethanol.

Type-locality. Parque Estadual do Desengano, municipality Santa Maria Madalena/RJ, Brazil.

Synonymy. Geoplana sp. 5 in Carbayo et al. (2013).

Cratera sp. 5 in Carbayo et al. (2013).

Diagnosis. The species is distinguished from its congeners by its black blue dorsum with submarginal zinc yellow stripe. The peculiar shape of the male organs, i.e., a very short and wide penis papilla projecting vertically downwards from the roof of the male atrium, and possessing a large intra-penial cavity, readily distinguishes this from any other species of Geoplaninae .

External aspect. Only the paratype PL 805 was measured in life, reaching 11 cm in length and 0.6 cm in width at maximum extension ( Fig. 1 ). After fixation adults measured 7 to 11 centimeters in length. Body margins parallel, anterior end rounded, posterior one pointed. Dorsum convex-flat, ventral side flat, 1 to 1.9 mm in height.

Dorsal color black blue with a submarginal zinc yellow stripe on each side of the body. The stripes have 1/9th of body width, running from nearly the anterior tip of the body to the posterior end. Ventral side light ivory, becoming brown beige in the anterior end ( Fig. 2 ). After fixation, colors of dorsal and ventral side faded and a faint graphite black dark midline of the dorsurn became visible ( Fig. 3 ).

In the six, fixed mature specimens, the mouth lies at a distance from anterior tip equal to 69–76% (mean 70%) of body length; the gonopore, 78–86% (mean 82%). The eyes are of the pigmented-cup type, 35–40 µm in diameter, surrounded by clean halos, and arranged marginally from the very anterior tip of the body to the posterior end. They are distributed in an irregular row consisting of one to three eyes in the black-blue colored body margin.

Internal morphology. The sensory pits are simple invaginations 35 µm deep, located ventro-marginally in a single row in the anterior third of the body. The width of the creeping sole is 90% of body width at the prepharyngeal region.

The conspicuous glandular margin ( Fig. 4 ) is constituted by very abundant gland cells containing xanthophilic granules and scarce gland cells containing cyanophilic granules. The cutaneous musculature comprises the three typical layers of Geoplaninae in the same way throughout the body, i.e., a subepithelial circular layer followed by two diagonal layers with decussate fibers, and then a longitudinal layer with fibers arranged in bundles of 43–73 fibers each. The longitudinal fibers lying immediately under the decussate fibers do not run in the anteroposterior axis of the body, but slightly obliquely to the body margins ( Figs. 5–6 ). The thickness of cutaneous muscle ranges from 6% to 14% (mean 10%) to body height in the pre-pharyngeal region. The three common geoplaninid parenchymal muscle layers, all well developed, are present throughout the body: a dorsal layer of diagonal decussate fibers, a transverse supraintestinal layer, and a transverse subintestinal one ( Fig. 7 ).

The mouth lies in the middle of the pharyngeal pouch. The bell-shaped pharynx ( Fig. 7 ) occupies about 2/3 of the pharyngeal pouch. An esophagus is absent. The pouch is lined by a flat ciliated epithelium, surrounded by a thin muscle layer of longitudinal muscle. Three types of glands (erythrophilic, xanthophilic and scarce cyanophilic) secrete through the distal pharyngeal epithelium.

The outer and inner pharyngeal epithelia are flat, ciliated. The outer epithelium is underlain by a layer of longitudinal muscle (15 µm) followed by a layer of circular muscle (45 µm); the inner epithelium is underlain by a layer of circular muscle (60 µm) followed by a layer of longitudinal muscle (10 µm).

The testes are dorsal, located between the supraintestinal parenchymal muscle layer and the intestine, extending posteriad to ovaries (9 mm in the holotype, 8% of body length) to nearly level with dorsal pharyngeal insertion. The sperm ducts run immediately above the subintestinal muscle layer. Each sperm duct communicates with the anterior tip of the respective branch of the very long, canalicular prostatic vesicle ( Figs. 8, 13–15 ). This vesicle runs posteriorly, gradually inclined dorsad, and subsequently penetrates the dorso-anterior aspect of the common muscle coat and continues posteriorly to nearly level with the gonopore. The epithelium of the prostatic vesicle is lined with a ciliated, columnar to cuboidal epithelium, pierced by numerous openings of gland cells containing erythrophilic granules. It is underlain by a layer of nearly longitudinal muscles. The ejaculatory duct is a sinuous, descending canal, lined with a cuboidal epithelium, opening into a small 700-µm-long proximal cavity at the base of a large, distal intra-penial cavity ( Figs. 9–11, 13–15 ). This distal cavity is laterally compressed, and 4- mm long. The penis is of the protrusible type. The proximal cavity is lined with a non-ciliated epithelium underlain by a layer of circular muscles. It is pierced by scarce gland cells producing xanthophilic granules. The distal cavity is lined with a ciliated, apically erythrophilic epithelium, the free surface of which is sinuous. This epithelium is pierced by openings of numerous gland cells containing xanthophilic granules. Additionally, two types of gland cells discharge their secretion into the cavity, those producing pale-cyanophilic granules pierce the intermediate portion of the epithelium; those producing cyanophilic large granules pierce the distal portion of the cavity. The epithelium of this large cavity is surrounded by a subepithelial layer of circular muscle, followed by a layer of longitudinal muscle.

The penis papilla is short and much widened along the longitudinal axis of the body. It projects vertically downwards from the roof of the male atrium, even in incompletely mature specimens ( Fig. 17 ), slightly inclined to the right. The penis papilla is covered with a nucleated, ciliated epithelium transversed by gland cells containing xanthophilic granules. It is underlain with a subepithelial layer of circular muscles, followed by a layer of longitudinal muscles. The penis bulb is well muscularized, comprising decussated fibers. The penis papilla fills almost all the male atrium, this having two conspicuous, horizontal folds that encircle the papilla. Anteriorly, these folds may be divided into 3–5 minor folds. The folds are covered with a ciliated, apically erythrophilic epithelium, through which sparsely scattered xanthophilic glands discharge, and is underlain by a subepithelial thin layer of circular muscles, followed by a layer of longitudinal muscles. The gonopore lies in the middle of the male atrium.

The ovaries are ellipsoid, ~300 µm in diameter. They are located immediately above the ventral nerve plate, at a distance from the anterior tip equal to 21% of body length. The ovovitelline ducts arise from the dorso-external side of the ovaries, and run backwards above the ventral nerve plate, externally to the sperm ducts. The ovovitelline ducts pass posteriorly and in the proflex condition with dorsal approach, unite with the female genital duct. The ovovitelline ducts join each other to form the common glandular ovovitelline duct. This duct opens into the genital female canal, a C-shaped duct in lateral view. It is slightly dilated in the intermediate portion; the distal portion runs forwards ventrally to open into the posterior region of the female atrium ( Figs. 12–14, 16 ). The female atrium is a dorso-ventrally compressed, narrow cavity. The length of the female atrium: male atrium ratio is 1:6.

Ovovitelline ducts and common glandular ovovitelline duct are lined with a columnar, ciliated epithelium. The female genital canal is lined with an apically erythrophilic epithelium, pierced by gland cells containing cyanophilic fine granules. It is ciliated only in the portion close to the common glandular ovovitelline duct. The epithelial cells lining the dilated portion are taller and have the free surface sinuous. The female atrium is lined with a flat, non-ciliated erythrophilic epithelium, pierced with scarce openings of glands secreting fine cyanophilic granules, and surrounded by a thin layer of circular muscle.

Remarks. Among the geoplaninids, the external aspect of living specimens of Cratera cuarassu sp. nov. can be confounded with Imbira marcusi . The latter species is widely distributed across the Atlantic forest of Southeast and South Brazil, but Cratera cuarassu sp. nov. and Imbira marcusi are not sympatric. Imbira marcusi displays several patterns in the color of the dorsum which differentiate it from that of the new species, and even in the most similar combination of color and pattern its lateral yellow stripes are half or less in width than those of Cratera cuarassu sp. nov.

Among the current 23 genera of Geoplaninae , the new species matches only the diagnostic features of Cratera , excepting in one feature. The cavity into which the ejaculatory duct opens does not occupy only the apical portion of the penis papilla but extends inwards to the base of the papilla, resulting in a large intra-penial cavity.

This large intra-penial cavity and the remarkably vertical projection from the roof of the male atrium of the papilla are characters that distinguish the new species from the others of the genus, even from any other species of Geoplaninae . Our decision about placing the species in Cratera is supported by molecular data shown in Carbayo et al. (2013); the new species forms part of a clade constituted exclusively by species of Cratera .

The presumed torsion of the penis papilla in C. cuarassu results in a morphological deviation from its congeners, and thus it resembles geoplaninids of other genera, viz., Issoca rezendei ( Schirch, 1929) , Gigantea gouvernoni Jones & Sterrer, 2005 , and the following Peruvian species of Geoplana listed as incertae sedis; Geoplana cantuta du Bois-Reymond Marcus, 1951, G. chalona du Bois-Reymond Marcus, 1951, G. gabriellae du Bois-Reymond Marcus, 1951, G. l a m b a y a du Bois-Reymond Marcus, 1958, G. quichua du Bois-Reymond Marcus, 1951, G. shapra du Bois-Reymond Marcus, 1957 (see Carbayo et al., 2013).

Figures

FIGURES 1 – 3. Cratera cuarassu sp. nov. (1) living paratype PL 805 creeping in dorsal view. About 60 mm in length. (2) living paratype PL 805 in ventral view. (3) fixed holotype on a millimetered paper after cutting off a piece of the central body.

FIGURES 4 – 7. Cratera cuarassu sp. nov. Micrographs of the holotype. (4) micrograph of the glandular margin of holotype in a transverse section of the pre-pharyngeal region. (5) micrograph of the ventral cutaneous musculature tangentially cut in a horizontal section. Red line indicates longitudinal fibers; the pinkish line indicates decussate fibers. Anterior to the bottom. (6) micrograph of a detail of ventral cutaneous musculature tangentially cut in a horizontal section. Red line indicates longitudinal fibers; the pinkish line delimits the decussate fibers. Anterior to the bottom. (7) micrograph of a sagittal section of the pharynx of the holotype. Anterior to the right.

FIGURES 8 – 13. Cratera cuarassu sp. nov. Holotype. Anterior to the right. (8 – 9) micrographs of a sagittal section of the copulatory apparatus of the holotype. (10) micrograph of a detail of the large cavity within the penis papilla of the holotype. (11) micrograph of a parasagittal section of the copulatory apparatus of the holotype. (12) micrograph of the genital female canal and posterior aspect of the female atrium of the holotype in a sagittal section. (13) diagrammatic reconstruction of copulatory apparatus of the holotype from sagittal sections.

FIGURES 14 – 17. Cratera cuarassu sp. nov. Micrographs. (14) common glandular duct and female atrium of the paratype F 2192 in a sagittal section. Anterior to the right. (15) sagittal section of the paratype F 2192 showing the small cavity into which opens the ejaculatory duct. (16) sagittal section of the paratype F 2192 showing the genital female canal and posterior aspect of the female atrium. Anterior to the right. (17) sagittal section of the copulatory apparatus of the paratype PL 809, incompletely developed. Anterior to the left.