Kawakatsua pumila Sluys, 2019

Sluys, Ronald & Laumer, Christopher, 2019, A new genus and species of a terrestrial cavernicolan planarian from Barro Colorado Island, Panama (Platyhelminthes, Tricladida, Cavernicola), Zootaxa 4586 (1), pp. 187-193 : 188-192

Kawakatsua pumila Sluys , sp. nov.

Etymology. The specific epithet is derived from the Latin pumilis, dwarfish, little, and alludes to the minute size of the specimens.

Diagnosis. As that of the genus.

Ecology and distribution. Specimens are known only from the type locality, Barro Colorado Island, where they were found in a large pile of humid leaf mulch accumulated between two buttress roots of an old broadleaf tree.

Material examined. Holotype: ZMA V.Pl. 7282.1, Barro Colorado Island , Panama, 09 o 09'09.6"N – 079 o 51'06.2"W, June 2010, sagittal sections on 2 slides.

Paratypes: ZMA V.Pl. 7282.2, ibid., sagittal sections of an immature specimen on 1 slide ; ZMA V.Pl. 7282.3, ibid., sagittal sections on 2 slides ; ZMA V.Pl. 7282.4, ibid., horizontal sections on 1 slide ; MCZ: IZ:149898, ibid., sagittal sections on 1 slide ; MCZ: IZ: 151261 , ibid., sagittal sections on 1 slide .

Description. Length of preserved specimens, as measured on histological sections, ranges between 2.4 – 2.55mm. Live animals white, without pigmentation or eyes, and with broadly rounded front end and obtusely pointed posterior end ( Fig. 1 ). Dorsal and ventral epidermis packed with rhabdites. Adhesive glands, at least at the anterior margin, discharge their secretion directly through the epidermis without the intervention of "Haftpapillen" or adhesive papillae, as the latter are absent ( Fig. 2 ). Cutaneous musculature simple, consisting of a single, subepidermal row of circular muscle, followed by one or two layers of longitudinal muscle.

The anterior intestinal trunk extends forwards up to the brain, i.e. it does not run dorsally or anteriorly to the brain; in other words, a precerebral gut branch is absent. The tubular pharynx measures between 1/6–1/7 of the body length in preserved specimens (as measured in histological sections); it is located well into the posterior half of the body ( Fig. 1 ). The pharynx is of the planariid type: outer lining epithelium underlain by a single, subepithelial layer of longitudinal muscle, followed by a single layer of circular muscle; inner pharyngeal epithelium underlain by a rather thin layer of circular muscle, consisting of only two rows of fibres ( Fig. 3 ), followed by a single layer of longitudinal muscle. Mouth opening located at the middle of the pharyngeal pocket ( Fig. 4 ).

Because of the posterior position of the pharynx, the entire copulatory apparatus is located in the far tail end of the body, relatively close to the posterior margin of the body ( Fig. 1 ).

Few testes, up to seven follicles, distributed irregularly in the body and extending from a position far posterior to the ovaries (about halfway between the ovaries and the root of the pharynx) to immediately in front of the male copulatory apparatus, i.e. directly behind the pharyngeal cavity. The testes are principally located ventrally ( Fig. 5 ), albeit that some follicles may occupy the entire dorso-ventral space.

Paired ovaries situated ventrally at some distance (100–200µm) behind the brain, i.e. at a location between 1/7–1/8 of the distance between the brain and the root of the pharynx ( Fig. 6 ).

Shortly behind the pharyngeal pocket the vasa deferentia expand to form spermiducal vesicles, filled with sperm. At about the level of the root of the penis papilla the sperm ducts turn dorsad and strongly recurve, thus forming a loop, before they unite to give rise to the ejaculatory duct ( Fig. 7 ). The latter runs to the tip of the penis papilla, meanwhile greatly decreasing in diameter. There is hardly any musculature surrounding the ejaculatory duct, which is lined with a cuboidal, nucleated epithelium.

The cone-shaped penis papilla is oriented horizontally, parallel to the anterior-posterior body axis. It is covered with a nucleated epithelium, which is underlain by a single, subepithelial layer of circular muscle, followed by a single layer of longitudinal muscle. A distinct, muscular penis bulb is absent.

Male and female atrium are lined by a layer of large, cuboidal, nucleated and ciliated cells. Posterior to the gonopore, the male atrium grades into the female atrium, the latter communicating with the horizontally oriented bursal canal, which is lined also with cuboidal, nucleated and ciliated cells. Posterior to the gonopore the oviducts turn dorso-medially and, subsequently, unite to form a common oviduct, which is oriented more or less perpendicular to the bursal canal and opens into it shortly before the canal communicates with the copulatory bursa ( Figs 7 , 8 ). Oviducts and common oviduct are lined with cuboidal, nucleated and ciliated cells and are surrounded by a thin layer of circular muscle fibres. The bursal canal is surrounded by a thin layer of subepithelial circular muscle, followed by an equally thin layer of longitudinal muscle. Shell glands discharge their cyanophil secretion into the most distal, posterior sections of the oviducts, as well as into the very dorsal section of the common oviduct. The sac-shaped copulatory bursa lacks a distinct, single lumen as it is mostly filled with a syncytial mass of cells, with interspersed nuclei ( Fig. 9 ).

Discussion. Although there is already ample molecular evidence that Kawakatsua pumila Sluys , gen. & sp. nov. falls well and truly within the Suborder Cavernicola, its anatomy underscores this taxonomic assignment. Sluys (1990) hypothesized the following three features as autapomorphies for the monotypic family Dimarcusidae : (1) penis bulb with glandular cells, (2) horizontally oriented bursal canal (or female genital duct) with a distinct Tjunction, formed by communication of the canal with the common oviduct, the latter oriented perpendicularly to the bursal canal, and (3) ovaries located at some distance posterior to the brain. Kawakatsua pumila fulfills two of these criteria as it does not exhibit a distinct penis bulb, nor glandular elements in it. However, there are also other dimarcusids that lack gland cells in their penis bulb, viz. Rhodax evelinae Marcus, 1946 , and Hausera hauseri Leal-Zanchet & Souza, 2014 , thus suggesting that this particular character should be removed from the diagnosis of the family Dimarcusidae .

It is noteworthy that a rather uncommon condition among aquatic planarians, the central mouth opening, has evolved several times within the Cavernicola. A mouth being located in the middle of the pharyngeal pocket occurs in Rhodax evelinae , Balliania thetisae Gourbault, 1978 (see Sluys 1990), and Kawakatsua pumila . Position of the mouth in Novomitchellia bursaelongata Harrath, Sluys & Riutort, 2016 was not described by Harrath et al. (2016), but it is at the posterior end of the pharyngeal cavity. Neither was the position of the mouth opening described for Hausera hauseri by Leal-Zanchet et al. (2014), albeit that their figure 12 seems to suggest that the mouth is at the middle of the pharyngeal pouch, although this may be due to a contraction artefact. All paratypes and additional specimens of H. hauseri are less contracted than the holotype, albeit that they also have a protruded pharynx, and have the mouth located close to the posterior end of the pharyngeal pocket (A. Leal-Zanchet, pers. comm.).

Although a mouth halfway in the pharyngeal cavity undoubtedly represents a derived character state, as the plesiomorphic state with the mouth at the hind end of the pharyngeal pouch is the basic condition for its sister group, the Maricola (see Sluys 1989), the feature does not coincide with a single monophyletic group within the Cavernicola. In this context it is interesting to note that K. pumila and H. hauseri both have vasa deferentia that form a distinct loop while recurving anteriad. Among the cavernicolans this feature is restricted to these two species and suggests that these two species share a sister-group relationship, an hypothesis which should be readily tested in future molecular phylogenetic work.

Within the Cavernicola only Balliania thetisae , Novomitchellia sarawakana (Kawakatsu & Chapman, 1983) and N. bursaelongata possess a primary copulatory bursa, lined with vacuolated and nucleated cells. Other species lack a bursa ( Rhodax evelinae , Hausera hauseri ) or exhibit a secondary bursa ( Opisthobursa mexicana Benazzi, 1972 , O. josephinae Benazzi, 1975 , Kawakatsua pumila ), the histology of which differs from a primary bursa ( Sluys 1990). The syncytial filling of the bursa of K. pumila indeed greatly differs from the lining with vacuolated, nucleated cells as present in primary bursae.

The ecology of the Cavernicola always has been a kind of conundrum, which only has increased with the discovery of more species of this suborder. Most species are known from an underground, hypogean habitat. Exceptions are formed by Rhodax evelinae , which is an epigean species, and Kawakatsua pumila of which specimens were found in a basically terrestrial, albeit humid, locality. Reconstructing the ancestral habitat and morphology of this intriguing taxon will require a more complete sampling of the presumably many stillundescribed species in the diverse habitats in which they might occur, and an accurate reconstruction of the internal phylogeny of the suborder.

Figures

FIGURE 7. Kawakatsua pumila. Holotype, ZMA V.Pl. 7282.1. Sagittal reconstruction of the copulatory apparatus; anterior to the right.

FIGURES 1–3. Kawakatsua pumila. (1) Dorsal view of live specimen; anterior end at the top. Scale bar not available. (2) ZMA V.Pl. 7282.3. Sagittal section of anterior end, showing adhesive secretion being discharged through the epidermis. (3) Holotype, ZMA V.Pl. 7282.1. Sagittal section through the pharynx; anterior to the right.

FIGURES 4–6. Kawakatsua pumila.(4) Holotype, ZMA V.Pl. 7282.1. Sagittal section through pharynx and pharyngeal pocket, showing the mouth opening. (5) ZMA V.Pl. 7282.3. Sagittal section through a testis follicle. (6) ZMA V.Pl. 7282.3. Sagittal section through the ovary.

FIGURES 8–9. Kawakatsua pumila. (8) MCZ: IZ:149898. Sagittal section through the copulatory apparatus; anterior to the right. (9) Holotype, ZMA V.Pl. 7282.1. Sagittal section through the copulatory apparatus, showing the syncytial copulatory bursa; anterior to the right.