Research Article |
Corresponding author: Ana Leal-Zanchet ( zanchet@edu.unisinos.br ) Academic editor: Tom Artois
© 2019 Giuly Gouvêa Iturralde, Ana Leal-Zanchet.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Iturralde GG, Leal-Zanchet AM (2019) Why be original? Two new species of Choeradoplana resembling the type species of the genus in their external aspects (Platyhelminthes, Continenticola). ZooKeys 813: 1-19. https://doi.org/10.3897/zookeys.813.29565
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The genus Choeradoplana Graff, 1896 encompasses 16 species, most of them found in Brazil. Herein two new species of this genus are described from remnants of Araucaria moist forests, located in the states of Paraná and Santa Catarina, south Brazil. Both species resemble the type-species of the genus, C. iheringi, showing brownish dorsal surface covered by dark-brown flecks. However, regarding their anatomy, the new species differ from C. iheringi and other congeners by a long and horizontal disposed permanent papilla. In such aspects, both species resemble C. benyai, but differ from this species, as well as from each other, in details of the prostatic vesicle, ejaculatory duct, and penis papilla.
Araucaria Forest, Neotropical region, taxonomy, Tricladida
The genus Choeradoplana, proposed by
The Araucaria forest is a phytophysiognomy of the Atlantic Forest, which harbours a high species richness of land flatworms (
Flatworms were sampled in two protected areas located in the Iguassu River Drainage Basin, in south Brazil, namely the Araucaria Natural Heritage Private Reserve (26°20.35'–26°26.13'S; 51°19.49'–51°25.29'W), in General Carneiro, state of Paraná, and Três Barras National Forest (26°09.27'–26°16.9'S; 50°16.0'–50°21.22'W), in Três Barras, state of Santa Catarina. Specimens were collected by visual search during the night, when they are more active.
Just after sampling, colour pattern, body shape and dimensions of live specimens were recorded. They were then euthanised using boiling water and fixed in neutral formalin 10%. After fixation, specimens were maintained in 70% ethyl alcohol. Methods described by
Type-material is deposited in the Museu de Zoologia da Universidade do Vale do Rio dos Sinos, São Leopoldo, state of Rio Grande do Sul, Brazil (MZU), and the Helminthological Collection of Museu de Zoologia da Universidade de São Paulo, state of São Paulo, Brazil (MZUSP).
Abbreviations used in the figures:
cmc common muscle coat;
cov common glandular ovovitelline duct;
cs creeping sole
de dorsal epidermis;
di dorsal insertion of pharynx;
dm dorsal cutaneous musculature;
e eyes;
ej ejaculatory duct;
fc female canal;
gc glandular cushions;
go gonopore;
i intestine;
im internal musculature;
m mouth;
mm mesenchymal muscles;
mn “muscle net”;
n nerve plate;
nlm normal longitudinal cutaneous muscles;
om outer musculature;
ov ovovitelline ducts;
p penis papilla;
pp pharyngeal pouch;
pv prostatic vesicle;
r retractor muscle;
rg rhabditogen glands;
sc secretory cells;
sg shell glands;
slm sunken longitudinal cutaneous muscles;
sv spermiducal vesicle;
t testes;
v vitelline follicles;
ve ventral epidermis;
vi ventral insertion of pharynx.
Holotype: MZUSP PL.2143: leg. JAL Braccini, 6 June 2015, General Carneiro (Araucaria Natural Heritage Private Reserve), PR, Brazil – anterior tip: transverse sections on 24 slides; anterior region at the level of the ovaries: sagittal sections on 27 slides; pre-pharyngeal region: transverse sections on 8 slides; pharynx: sagittal sections on 31 slides; copulatory apparatus: sagittal sections on 25 slides. Paratype: MZU PL.00292: leg. I Rossi, 6 June 2015, General Carneiro (Araucaria Natural Heritage Private Reserve), state of Parana, Brazil – anterior tip: transverse sections on 27 slides; anterior region at the level of the ovaries: sagittal sections on 24 slides; pre-pharyngeal region: transverse sections on 10 slides; pharynx: sagittal sections on 22 slides; copulatory apparatus: sagittal sections on 19 slides.
A species of Choeradoplana with dorsal surface covered by irregular small dark-brown flecks and thin median light stripe; pharynx bell-shaped; sperm ducts opening laterally into proximal wall of prostatic vesicle; prostatic vesicle tubular and unpaired, narrowing to open through tip of penis papilla as an ejaculatory duct; penis papilla cylindrical and almost symmetrical, filling entire common atrium; atrium oval-elongate and unfolded, without differentiation between male and female regions.
External features. Body elongate with parallel margins (Figs
Measurements, in mm, of specimens of Choeradoplana longivesicula sp. n. Abbreviations: * after fixation; DG distance of gonopore from anterior end; DM distance of mouth from anterior end; DMG distance between mouth and gonopore; DPVP distance between prostatic vesicle and pharyngeal pouch. The numbers given in parentheses represent the position relative to body length.
Measurement | Holotype MZUSP PL. 2143 | Paratype MZU PL.00292 |
---|---|---|
Length at rest | 34 | 47 |
Width at rest | 6 | 4 |
Maximum length in extension | 62 | 67 |
Maximum width in extension | 3 | 3 |
Length* | 52 | 49 |
Width* | 4 | 4 |
DM* | 33(63) | 30 (61) |
DG* | 39(75) | 35 (71) |
DMG* | 6 | 5 |
DPVP* | 1.8 | 1.6 |
Creeping sole % | 86 | 82 |
Ovaries | 18(35) | 16 (32) |
Anteriormost testes | 17(33) | 15 (30) |
Posteriormost testes | 28(54) | 26 (53) |
Length of prostatic vesicle | 2.5 | 2.3 |
Length of penis papilla | 2.1 | 1.9 |
Length of atrium | 2.4 | 2.3 |
Female canal | 0.8 | 0.7 |
Common glandular ovovitelline duct | 0.1 | 0.1 |
Live specimens with dorsal surface covered by dark-brown pigmentation constituted by irregular, small flecks. Yellowish ground colour visible on cephalic region, on body margins, as well as on thin median stripe occurring along the body except for cephalic region (Figs
Eyes absent on anterior tip (first 1.5 mm of body, corresponding to 3% of body length). Afterwards, eyes initially monolobate and uniserial. Eyes become trilobate and plurisserial after 3 mm and sparser towards posterior tip. No clear halos around eyes. Pigment cups between 20 µm and 30 µm in diameter.
Sensory organs, epidermis and body musculature. Sensory pits, as simple invaginations (15–20 µm deep), absent on anterior tip, occurring in a single row between 3% and 10% of body length. Three types of glands discharge through whole epidermis of pre-pharyngeal region: rhabditogen glands with xanthophil rhammites (ventrally with smaller rhabdites) and cyanophil glands with amorphous secretion, as well as few erythrophil glands with fine granular secretion (Figs
Cutaneous musculature with usual three layers (circular, oblique, and longitudinal layers), showing part of ventral longitudinal layer, as well as some muscle bundles of dorsal longitudinal layer, imbedded in mesenchyme (Fig.
Body height and cutaneous musculature in the median region of a transverse section of the pre-pharyngeal, in micrometres, and ratio of the thickness of cutaneous musculature to the height of the body (mc:h index) of specimens of Choeradoplana longivesicula sp. n.
Measurement | Holotype MZUSP PL.2143 | Paratype MZU PL.00292 |
---|---|---|
Dorsal circular | 3 | 4 |
Dorsal oblique | 25 | 24 |
Dorsal longitudinal | 100 | 108 |
Dorsal imbedded | 20 | 18 |
Dorsal total | 148 | 154 |
Ventral circular | 2 | 3 |
Ventral oblique | 15 | 13 |
Ventral longitudinal | 40 | 38 |
Ventral imbedded | 70 | 67 |
Ventral total | 127 | 121 |
Body height | 1421 | 1413 |
Mc:h(%) | 19 | 19 |
Mesenchymal musculature (Fig.
Digestive System. Pharynx bell-shaped, ca. 6% of body length, occupies ca. 90% of pharyngeal pouch. Mouth slightly posterior to dorsal insertion next to end of median third of pharyngeal pouch (Fig.
Reproductive organs. Testes in one or two irregular rows on either side of body, located beneath dorsal transverse mesenchymal muscles, between intestinal branches (Fig.
Prostatic vesicle lined with high pseudostratified epithelium with few ciliated cells, receiving numerous openings of glands with ill-stained, coarse granular secretion, sometimes containing an erythrophil core. In addition, sparse openings of other two types of glands occur throughout the epithelium of prostatic vesicle: cells with xanthophil, coarse granular secretion, and cell with amorphous, cyanophil secretion. Ejaculatory duct lined with columnar, densely ciliated epithelium. Both penis papilla and atrium lined with non-ciliated columnar epithelium, becoming cuboidal towards tip of papilla, showing a xanthophil apical region. Numerous glands of two types open through epithelial lining of penis papilla and atrium: one with xanthophil, coarse granular secretion and the other with amorphous, cyanophil secretion. In addition, a third type, with fine granular, erythrophil secretion, opens through epithelial lining of penis papilla. Muscularis of penis papilla (30–60 µm) composed of subepithelial layer with circular fibres followed by some longitudinal fibres; that of atrium composed of longitudinal and circular interwoven fibres (10–15 µm).
Vitelline follicles situated between intestinal branches, well developed. Ovaries ovoid, ca. twice longer than wide, measuring 0.2 mm in its antero-posterior axis. They are located dorsally to the ventral nerve plate, in anterior third of body. Ovovitelline ducts emerge laterally from median third of ovaries, then run posteriorly immediately dorsal to the nerve plate. Behind the gonopore, the ovovitelline ducts ascend posteriorly and medially inclined, and unite, dorsally to the female canal, forming the common glandular ovovitelline duct. Female canal relatively long and C shaped. This canal opens into bottom of posterior part of atrium, where a constriction occurs (Figs
Female canal lined with erythrophil, pseudostratified epithelium. Three types of glands open through the epithelium of female canal: abundant cells with finely granular, erythrophil secretion, cells with coarse granular, xanthophil secretion, and scarce cells with amorphous, cyanophil secretion. Muscularis of female canal composed of longitudinal and circular interwoven fibres (20–30 µm)
Gonopore canal almost vertical at the sagittal plane. Common muscle coat highly developed, especially at penis bulb (Figs
The name is composed of the Latin adjective longus (long) and the Latin vesicula, alluding to the elongate prostatic vesicle.
known only from the type-locality, General Carneiro, Paraná, Brazil.
Holotype: MZUSP PL.2144: leg. JAL Braccini, 2 June 2015, Três Barras (National Forest), state of Santa Catarina, Brazil – anterior tip: transverse sections on 17 slides; anterior region at the level of the ovaries: sagittal sections on 16 slides; pre-pharyngeal region: transverse sections on 7 slides; pharynx and copulatory apparatus: sagittal sections on 25 slides.
A species of Choeradoplana with dorsal surface covered by irregular small dark-brown flecks; pharynx bell-shaped; sperm ducts opening subterminally into prostatic vesicle; prostatic vesicle oval-elongate and folded, becoming funnel-shaped proximally and forming an elongate duct inside penis papilla; penis papilla, conical, long and almost symmetrical, with dorsal insertion shifted posteriorly, filling the whole atrium.
External features. Body elongate with parallel margins (Fig.
Measurements, in mm, of the holotype of Choeradoplana cyanoatria sp. n. Abbreviations: * after fixation; DG distance of gonopore from anterior end; DM distance of mouth from anterior end; DMG distance between mouth and gonopore; DPVP distance between prostatic vesicle and pharyngeal pouch. The numbers given in parentheses represent the position relative to body length.
Measurement | HolotypeMZUSP PL.2144 |
---|---|
Length at rest | 20 |
Width at rest | 4 |
Maximum length in extension | 28 |
Maximum width in extension | 3 |
Length* | 50 |
Width* | 4 |
DM* | 33(66) |
DG* | 40(80) |
DMG* | 7 |
DPVP* | 1.2 |
Creeping sole % | 89 |
Ovaries | 8 (16) |
Anteriormost testes | 9 (18) |
Posteriormost testes | 29 (58) |
Length of prostatic vesicle | 0.6 |
Length of penis papilla | 1.3 |
Length of the atrium | 1.6 |
Female canal | 0.4 |
Common glandular ovovitelline duct | 0.1 |
Live specimens with dorsal surface covered by irregular, small dark-brown flecks over all body length including cephalic region (Fig.
Eyes absent on cephalic region (first 1.2 mm of body, corresponding to 2.4% of body length). After that, eyes initially monolobate and uniserial. Eyes become trilobate and plurisserial after 3 mm, becoming sparser towards posterior tip. No clear halos around eyes. Diameter of pigment cups between 24 µm and 32 µm in diameter.
Sensory organs, epidermis and body musculature. Sensory pits, as simple invaginations (15–18 µm deep), absent on anterior tip, occurring in a single row between 3% and 10% of body length.
Three types of glands discharge through whole epidermis of pre-pharyngeal region: rhabditogen glands with xanthophil rhammites (ventrally with smaller rhabdites) and cyanophil glands with amorphous secretion, as well as few xanthophil glands with coarse granular secretion (Fig.
Cutaneous musculature with usual three layers (circular, oblique, and longitudinal layers), with part of ventral longitudinal layer, as well as few muscle bundles of dorsal longitudinal layer, imbedded in mesenchyme (Fig.
Body height and cutaneous musculature in the median region of a transverse section of the pre-pharyngeal, in micrometres, and ratio of the thickness of cutaneous musculature to the height of the body (mc:h index) of the holotype of Choeradoplana cyanoatria.
Measurement | Holotype MZUSP PL.2144 |
---|---|
Dorsal circular | 4 |
Dorsal oblique | 8 |
Dorsal longitudinal | 33 |
Dorsal imbedded | 27 |
Dorsal total | 72 |
Ventral circular | 2 |
Ventral oblique | 15 |
Ventral longitudinal | 130 |
Ventral imbedded | 5 |
Ventral total | 152 |
Body height | 1025 |
Mc:h(%) | 22 |
Mesenchymal musculature (Fig.
Digestive system. Pharynx bell-shaped, as long as 7% of body length, occupies almost entire pharyngeal pouch. Mouth almost at the same transversal level as dorsal insertion in the beginning of median third of pharyngeal pouch (Fig.
Reproductive organs. Testes in two or three irregular rows on either side of body, located beneath dorsal transverse mesenchymal muscles, between intestinal branches (Fig.
Prostatic vesicle and proximal third of ejaculatory duct receive abundant openings of cells with coarse granular, erythrophil secretion, besides sparse amorphous, cyanophil secretion, besides a third type of gland containing heavy cyanophil granules. Distal two thirds of ejaculatory duct receives openings from numerous glands with amorphous, cyanophil secretion. Muscularis of ejaculatory duct thin (5µm) composed of longitudinal fibres. Abundant glands with densely distributed, coarse granular, xanthophil secretion and numerous glands with amorphous, cyanophil secretion open through epithelial lining of penis papilla, besides sparse erythrophil glands through lining of penis papilla. Numerous glands with amorphous, cyanophil secretion and scattered glands with erythrophil, fine granular secretion open through epithelial lining of the atrium, which is cyanophil. Muscularis of penis papilla (40–80µm) composed of subepithelial layer with circular fibres followed by layer with longitudinal fibres, both layers well developed. Posteriorly to the gonopore, necks of cyanophil glands concentrate subepithelially; subepithelial muscle fibres of atrium scattered among these cell necks (Fig.
Vitelline follicles, situated between intestinal branches, well developed. Ovaries ovoid, 1.5 times longer than wide, measuring 0.3 mm in its antero-posterior axis. They are located dorsally to the ventral nerve plate, in anterior sixth of body. Ovovitelline ducts emerge laterally from median third of ovaries, and run posteriorly immediately above nerve plate. Behind gonopore, the ovovitelline ducts ascend posteriorly and medially inclined, uniting to form a common glandular ovovitelline duct. This duct is situated dorsally to the relatively long, C shaped female canal, which opens into the atrium (Figs
Shell glands of two types: with coarse granular, erythrophil secretion, as well as with coarse granular, xanthophil secretion, the cells bodies of which occur among cell bodies of cyanophil glands. Towards female canal, the lining epithelium becomes pseudostratified and erythrophil. Two types of glands open through the epithelium of the female canal: erythrophil glands with finely granular secretion and cyanophil glands with amorphous secretion both sparsely distributed. Muscularis of female canal (20–40µm) composed of interwoven circular and longitudinal fibres.
Gonopore canal vertical at the sagittal plane. Common muscle coat highly developed, especially at penis bulb (Figs
The name is a composite of the Latin adjective cyano (blue) and the Latin atria, referring to the abundant cyanophil secretion opening through the atrium.
Known only from the type-locality, Três Barras, Santa Catarina, Brazil.
Choeradoplana longivesicula was recorded only in its type-locality, the Araucaria Natural Heritage Private Reserve, state of Parana, in a site showing an initial stage of regeneration with poorly developed understorey (
Both new species described herein match the diagnostic features of the genus Choeradoplana, namely a cephalic region that is curved backwards, a cephalic glandulo-muscular organ, and a cutaneous longitudinal musculature with a portion internal to the subcutaneous nerve plexus throughout the body, among others (
Regarding external features, both new species resemble the type-species, C. iheringi, as well as C. banga Carbayo & Froehlich, 2012, C. bocaina Carbayo & Froehlich, 2012, C. benyai Lemos & Leal-Zanchet, 2014, C. agua
With respect to the anatomy of the copulatory organs, by presenting a long, permanent penis papilla, the new species are easily differentiated from the species with an eversible penis papilla, namely C. abaiba, C. agua, C. albonigra (
Both species share with C. benyai a long penis papilla with horizontal orientation. However, by having a cylindrical and long prostatic vesicle that traverses the penis papilla. Choeradoplana longivesicula differs from C. benyai that shows a globose prostatic vesicle with folded wall restricted to the penis bulb (
We acknowledge Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil, Nr. 306853/2015-9 and CNPq/PELD Site 9, Nr. 403817/20129) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) for research grants and fellowships in support of this study. We thank Prof. Dr. C.A. Sanquetta and his research group in the Universidade Federal do Paraná, especially Dr. A.L. Rodrigues, for their help in the planning and organization of the field trips. We acknowledge I Rossi and JAL Braccini for their help in sampling flatworms and E Benya for an English review of the text. I Rossi is also acknowledged for the photos in the figures 1, 2, and 12. Dr Fernando Carbayo and Dr Hugh Jones are thanked for their suggestions on an early draft of the manuscript.