Research Article |
Corresponding author: Carolina Lenis ( leniscarolina16@gmail.com ) Academic editor: Tom Artois
© 2020 Carolina Lenis, Freddy Ruiz, Carlos Muskus, Antonio Marcilla, Imelda Vélez.
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:
Lenis C, Ruiz F, Muskus C, Marcilla A, Vélez I (2020) A new flatworm species of Temnocephala (Rhabdocoela, Temnocephalidae) ectosymbiont on the freshwater crab Valdivia serrata (Decapoda, Trichodactylidae) from Amazonas, Colombia. ZooKeys 918: 1-14. https://doi.org/10.3897/zookeys.918.38201
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A new species of temnocephalan is described from the branchial chambers of Valdivia serrata in Colombia as Temnocephala ivandarioi sp. nov. The most distinctive characters of the new species are in the cirrus and the epidermal ‘excretory’ syncytial plates. In the present study, the terminology to describe the cirrus of species of Temnocephala is updated. Comparison between the shape of the cirrus of the temnocephalans associated with trichodactylid crabs is also provided.
Crustacea, Reserva Natural Tanimboca, taxonomy, Temnocephala ivandarioi sp. nov.
The genus Temnocephala Blanchard, 1849 includes 37 species of symbiotic freshwater rhabdocoels from the Neotropics, which are associated with a large variety of hosts including chelonians (3), mollusks (6), insects (7) and crustaceans (21) (
Eleven specimens of Valdivia serrata White, 1847 (crab) were manually collected from the Reserva Natural Tanimboca, Leticia, Amazonas (4°07'39.8"S, 69°57'13.0"W), Colombia. The specimens were transported alive to the Programa de Estudio y Control de Enfermedades Tropicales (PECET) laboratory and identified using a decapod key (
Phylum Platyhelminthes Minot, 1876
Order Rhabdocoela Ehrenberg, 1831
Suborder Dalytyphloplanida Willems, Wallberg, Jondelius, Littlewood, Backeljau, Schockaert & Artois, 2006
Infraorder Neotyphloplanida Willems, Wallberg, Jondelius, Littlewood, Backeljau, Schockaert & Artois, 2006
Parvorder Limnotyphloplanida Van Steenkiste, Tessens, Willems, Backeljau, Jondelius & Artois, 2013
Section Temnocephalida Blanchard, 1849
Superfamily Temnocephaloidea Baer, 1953
Family Temnocephalidae Monticelli, 1899
Valdivia serrata White, 1847 (Fig.
Branchial chambers.
36% of the eleven hosts were infected.
Kilómetro 11, Reserva Natural Tanimboca, Leticia, Amazonas (4°07'39.8"S, 69°57'13.0"W), Colombia.
Holotype: CCH.116 (159); Paratypes: CCH.116 (160).
10 whole mounted specimens; 5 stained in Meyer’s paracarmine; 5 stained in Borax carmine; 6 dissected cirrus; 2 samples observed by SEM, 5 unhatched eggs observed by SEM.
External characteristics.
Body (without tentacles) 1.36–2.26 mm (1.75 ± 0.25) long by 1.18–1.56 mm (1.36 ± 0.11) wide; adhesive disk ventral, subterminal 280–520 (370 ± 82) long by 320–520 (400 ± 40) wide (Figs
Alimentary system.
Mouth surrounded by a large muscular sphincter 200–280 (220 ± 26) long by 210–310 (248 ± 32) wide; pharynx 330–620 (417 ± 56) long by 450–620 (511 ± 52) wide; intestine saccular, without septations (Fig.
Glands.
Rhabditogenic glands forming bunches in the lateral fields of the body extending from the pharynx to the middle level of the adhesive disk. Haswell cells in front of the eyespots and the brain. Disk glands between the adhesive disk and the genital complex (Fig.
Female. Ovary ventral to the resorbens vesicle 57–100 (83 ± 13; N = 7), long by 60–145 (105 ± 26; N = 7) wide. Vagina elongated with strong muscular wall, connects to the genital atrium dorsally, 75–180 (125 ± 37; N = 4) long by 16–30 (23 ± 4; N = 6) wide with a widening of the distal portion; proximal vaginal sphincter symmetrical 16–34 (23 ± 6; N = 6) and distal vaginal sphincter symmetrical (16–20; N = 2) (Figs
Male. Two pairs of testes, medium-sized, usually rounded, slightly oblique, anterior testes 180–310 (231 ± 34) long by 120–320 (220 ± 48) wide; posterior testes 200–400 (260 ± 60) long by 110–360 (254 ± 65) wide (Fig.
The new species is dedicated to Dr. Iván Darío Vélez Bernal for his outstanding contributions to the study of helminthology and the understanding of tropical diseases in Colombia.
Temnocephalida is a monophyletic group within the Platyhelminthes included in Lymnotyphloplanida, which is part of the Dalytyphloplanida clade, a major group of Rhabdocoela (
Taxonomy of temnocephalans is based on morphology of adult specimens with emphasis on the reproductive system. The structure of the cirrus is the trait of greatest taxonomic value (
Nine species of Temnocephala are known for their association with crabs of the Trichodactylidae family. Of these, T. ivandarioi sp. nov., T. longivaginata Seixas, Amato & Amato, 2011, and T. lutzi Monticelli, 1913 (
Temnocephala ivandarioi sp. nov. can be distinguished by the combination of the following features: cirrus with a circle of small sclerites (range 18–20) in the distal portion of the introvert, without spines or ridges in the inner wall of the introvert (Fig.
On an ecological-level T. ivandarioi sp. nov., T. longivaginata, and T. lutzi inhabit the branchial chambers of trichodactylid crabs from the middle basin and lower basin of the Amazon River (Leticia, Amazonas, Colombia; Peixe-Boi, Pará State; Rio Amapá, Amapá State, northern Brazil, respectively). Temnocephala ivandarioi sp. nov. is the third species described from Colombia, and therefore V. serrata is registered as a new trichodactylid host for neotropical temnocephalans. Valdivia serrata is widely distributed throughout the Orinoco and Amazon River basins in Venezuela, the islands of Trinidad and Tobago, the Guianas, Colombia, Brazil, Peru and Bolivia (
In Colombia more than 132 species of decapod crustaceans have been recorded (
The cirrus is the only rigid structure and therefore of constant general morphology in juveniles and adults (except for small intraspecific variations) for each species. The morphology of the cirrus constitutes one of the few characters used and is the most valuable taxonomic character for species identification (
The cirrus is defined as the entire sclerotised male copulatory organ comprised of a ‘shaft’ (rigid, tubular region tapering distally; Fig.
The shape of the shaft may be described as a ‘funnel’, ‘goblet’, or ‘cone’. Funnel- or goblet-shaped shafts have a wide proximal region which tapers rapidly into a narrow tubular distal region (
The introvert shape can be described as ‘cylindrical’, ‘cone’; ‘scoop’, or ‘goblet’. Scoop- or goblet-shaped introvert have a wide middle region, which tapers into a narrow distal region. In addition, the introvert may be ‘unarmed’, armed with ‘grooves’ in the proximal limit of the introvert, or armed with ‘spines’, ‘sclerites’, and ‘ridges’ in the inner wall of the introvert. The distal opening of the introvert may be at right angles with respect to the proximal limit of the introvert i.e. ‘not oblique’, ‘oblique’, or ‘very oblique’ (modified from
The morphology of the cirrus is necessary for species identification and should be clearly described based on the terminology proposed in the present study. This new terminology can be applied to species of neotropical temnocephalans described to date.
Temnocephala ivandarioi sp. nov. and Valdivia serrata A paratype of Temnocephala ivandarioi sp. nov. showing an egg, ventral view B adult paratype stained in Meyer´s paracarmine C holotype stained in Borax carmine D male specimen of V. serrata E abdomen F gonopods, lateral view. Scale bars: 200 µm (A–C); 10 mm (D–F).
Temnocephala ivandarioi sp. nov. A adult specimen diagram, showing adhesive disk (ad), anterior testes (at), cyanophilous glands (cg), disk glands (dg), excretory vesicle (ev), Haswell´s glands (hg), intestinal sac (i), mouth (m), pharynx (ph), posterior testes (pt), rhabditogenic glands (rg), tentacles (t), and vitellarium (v) B reproductive system, showing female reproductive complex: anterior portion of the distal vaginal sphincter (advs), anterior portion of the proximal vaginal sphincter (apvs), genital atrium (ga), genital pore (gp), posterior portion of the distal vaginal sphincter (pdvs), posterior portion of the proximal vaginal sphincter (ppvs), ovary (ov), vagina (va), and resorbens vesicle (vr); and male reproductive organs: cirrus (c), prostatic bulb (pb), prostatic vesicle (pv), seminal vesicle (sv), and vasa deferentia (vd) C line drawing of cirrus in different focusing planes, showing the sclerites portion of the introvert (sp), and proximal limit of the introvert (arrows). Scale bars: 200 µm (A); 100 µm (B); 20 μm (C).
Temnocephala ivandarioi sp. nov. details of epidermal excretory syncytial plates (DLSPs) and eggs A antero-lateral area observed with SEM showing leftmost tentacle and left DLSP, arrow showing contour and position of excretory pores (n) B line drawing of entire specimen showing the DLSPs C egg observed with SEM showing the filament (fi), peduncle (pe), and plane of fracture of the operculum (pf) D line drawing of a whole egg showing the oblique fracture plane to the longitudinal axis of the egg E live adult specimen showing red eyespot pigment F unhatched egg showing the filament (fi) G, H live eggs deposited on branchial chambers of V. serrata. Scale bars: 100 μm (A–F); 1mm (G, H).
Details of the reproductive system of Temnocephala ivandarioi sp. nov. A, B partial female reproductive system, showing: anterior portion of the distal vaginal sphincter (advs), anterior portion of the proximal vaginal sphincter (apvs), distal vaginal sphincter (dvs), genital atrium (ga), posterior portion of the distal vaginal sphincter (pdvs), posterior portion of the proximal vaginal sphincter (ppvs), proximal vaginal sphincter (pvs), ovary (ov), vagina (va), and vesicula resorbens (vr) C, D partial male reproductive system, showing: cirrus (c), prostatic bulb (pb), seminal vesicle duct (svd), seminal vesicle (sv), and vasa deferentia (vd) E, F cirrus introvert observed in different focusing planes, view of the circle of sclerites (sp) in the distal portion of the introvert and the smooth portion (smp) in the proximal limit of the introvert (pli). Scale bars: 50 μm (A–D); 20 μm (E, F).
Diagrams of the cirrus of the species of Temnocephala associated with trichodactylid crabs. Terminology based on the cirrus structure (see comparative notes and Fig.
We are grateful to Dr. Antoni Cthulhu marinus for his support during the preparation of the manuscript. We thank Any Carolina Garcés MSc. for her valuable taxonomic comments. We also thank Carolina Duque (PECET) and Dr. Stanimir Vuk-Pavlovic for reviewing of manuscript. This work was partially supported by “Implementation of an early warning system for the prevention and control of the main VTE in the Department of Amazonas, Colombia”, General Royalty System (BPIN 2013000100240). All the specimens were collected under the “Permiso Marco”, Universidad de Antioquia, to collect research specimens. This permission has been granted to us by the National Authority of Environmental Sciences – ANLA. Ministry of Environmental, Republic of Colombia. Resolution 0524, 27 May 2014.