Research Article |
Corresponding author: Norma Emilia González-Vallejo ( negv0707@hotmail.com ) Academic editor: Eike Neubert
© 2021 Norma Emilia González-Vallejo, Stephanie Amador-Carrillo.
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:
González-Vallejo NE, Amador-Carrillo S (2021) Assessment of Megadenus holothuricola Rosén, 1910 (Eulimidae), an endoparasite of Holothuria mexicana Ludwig, 1875 (Holothuriidae) in the southern Gulf of Mexico and the description a new species. ZooKeys 1016: 49-61. https://doi.org/10.3897/zookeys.1016.55071
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As part of a study on holothurians from the southern Gulf of Mexico, some Holothuria mexicana Ludwig, 1875 were obtained for gut analysis. In two of them, a couple of eulimids were located inside the main tube of the respiratory tree. They were identified as Megadenus holothuricola Rosén, 1910, described from the Bahamas Islands, based on five specimens attached to the respiratory tree of H. mexicana. The original description was brief with few details, the type material is lost, and the species has not been found again. In this contribution, this species is confirmed for Campeche Bay, Mexico. The adult shell is globular to conical, transparent, thin, and fragile. Megadenus smithi sp. nov. from Palmyra Atoll, Central Pacific is described based on adult specimens. It differs from its congeneric species in its more robust shell, the pseudopallium does not cover the shell, and its short and contracted proboscis forms a thick disc. Further research on these eulimid parasites is now complicated in the southern Gulf of Mexico because of the holothurian population collapse due to over-exploitation of the fishery.
Campeche, Eulimidae, gastropods, holothurians fishery, new species, Palmyra Atoll, symbiosis
Eulimidae form a large group of parasitic snails infesting sea urchins, holothurians, starfish, and feather stars. Genera vary in their physical characteristics and lifestyle (
Our knowledge of marine parasites is fragmentary. This observation, especially in the case of invertebrate hosts, is probably caused by their low occurrence rates (
The fishery of holothurians has increased in Campeche Bay during the last eight years. As part of a study of their feeding habits, some holothurians were obtained. After examining the internal organs, several endoparasites were located attached to or immersed in the main tube of the respiratory tree of Holothuria (Halodeima) mexicana Ludwig, 1875. One of the endoparasitic species was identified as Megadenus holothuricola Rosén, 1910. This eulimid was found attached to the respiratory tree of H. mexicana. The type locality of this species is the Bahamas Islands; the type series contained five specimens, and the original shell description was brief with few details only. The type material is lost, and the species has not been found again (
Comparison of the main character states separating the species of Megadenus. The information provided is based on literature (
Species | Shell/size/sex | Pseudopallium | Proboscis | Host/attach site | Geographical distribution & depth |
---|---|---|---|---|---|
M. holothuricola Rosén, 1910 | Globose to conical, thin, transparent, fine striae, 4.0–5.5 mm length × 2.0–1.5 mm width | Bowl-shaped with pleated margin | Funnel-shaped, white, flexible, rough cuticular surface; not retractable | Holothuria mexicana respiratory tree | Bahamas, Campeche Bay, shallow water |
M. voeltzkowi Shepman & Nierstrasz, 1913 | Ovoid transparent to whitish, slightly smooth 6.5 × 4 mm | Arises from folds of foot | Suction disc form, contracted and wrinkled | Holothuria pardalis? esophageal region | Zanzibar East Africa, shallow water? |
M. cantharelloides Humphreys & Lützen, 1972 | Cyrtoconoid and globose, transparent ♀ 5.7 × 4.5 mm | Bowl-shaped fold of tissue, more extensive in male than female | Chanterelle-shaped, darkened, contracted | Stichopus chloronotus intestine | Picard Island, Aldabra, India, shallow water |
M. oneirophantae Bouchet & Lützen, 1980 | Globose, vitreous ♀ 9.3 × 7.5 mm, ♂ 3.0 × 1.6 mm | Base partly covered by foot and its folds | Long, thin | Oneirophanta mutabilis within galls in intestine | Bay of Biscay, 4796 m abyssal depth |
M. atrae Takano,Warén & Kano, 2017 | Globose, pyriform to biconical, transparent to whitish ♀ 5.2 mm; ♂ 2.0–1.5 mm | Cauldron-shaped | Long, thickened at the middle into a collar-like | Holothuria atra, cloacal chamber and respiratory tree | Japan, New Caledonia, India Australia, tidal waters |
M. smithi sp. nov. | Globose to biconical, transparent,finally axial striae ♀6.5 mm L ♂ 4.0 mm | In folds of foot and cauldron-shaped | Suction disc form, slightly dark colored retractable | Holothuria atra cloacal chamber | Palmyra Atoll, shallow water |
One hundred holothurians were collected and donated by fisherman for gut-analyses and molecular studies. Holothurians were collected at 5 m depth in mixed sea grass meadows and sandy areas off the coast of Lerma (19°49.31'N, 90°36.51'W), Campeche Bay, Mexico, on 4 May 2012. Two species of holothurians were identified, H. mexicana and H. floridana; the identification was confirmed by molecular studies and the analysis of calcareous ossicles (following
The Eulimidae were photographed with a stereomicroscope and a Cannon EOS T6i camera, mounted with an adapter into the ocular tube. Measurements were made with a micro ruler (mm). Digital plates were assembled with Adobe Photoshop CC. Holothurians and eulimids were deposited in the collections of El Colegio de la Frontera Sur (
The endoparasite M. holothuricola was found in only two holothurians. In the first one, there were two adult specimens and one juvenile; all were immersed in the skin of the main tube of the respiratory tree (Fig.
Megadenus holothuricola Rosén, 1910 A two adults between filaments of the respiratory tree B, C detached adult shells, SL = 5.5 mm and 4.5 mm; right side juvenile attached SL = 1.0 mm D broken adult shell SL = 2.5 mm E subadult SL = 2.0 mm with everted proboscis L = 2.5 mm. Scale bars: 1.6 mm (A); 1.8 mm (B); 1.4 mm (C); 0.2 mm (D); 1.1 mm (E).
Megadenus holothuricola Rosén, 1910 A adults immersed in the main tube of the respiratory tree B, C two adults showing the mottled skin of the respiratory tree and the pseudopallium covering shell; proboscis slightly rolled, and another adult stretched to the maximum D cephalic view, 40× E two egg capsules, L = 2 mm F view of the distal part of an adult proboscis. Scale bars: 1.2 mm (A); 2.3 mm (B); 1.65 mm (C); 0.8 mm (D); 0.6 mm (E); 0.5 mm (F). Abbreviations: e: eyes; eg: egg capsules; p: proboscis; pg: pedal gland; pp: pseudopallium; rt: respiratory tree; s: shell; t: tentacle.
Order Littorinimorpha Golikov & Starobogatov, 1975
Familia Eulimidae Philippi, 1853
Megadenus holothuricola Rosén, 1910:18 by monotypy.
Shell conical to globular, translucent, colorless, sculpture of fine axial striae. Pseudopallium covers the shell or not; proboscis large or short forming a thick contracted disc; large pedal gland (
Megadenus species are found in shallow waters in tropical or subtropical regions, especially as endoparasites of Aspidochirotida (Echinodermata, Holothuroidea); usually they live in the cloacal chamber or attached to the respiratory tree. Megadenus oneirophantae Bouchet & Lützen, 1980 is the only abyssal species (4796 m).
Megadenus holothuricola Rosén, 1910:18–49 pl. 1 figs 1, 2 (type locality: Bahamas Islands; Type material lost).
four adult specimens
Bahamas and Lerma, Campeche, Mexico.
Shell
conical to globose, translucent, thin, fragile, sculpture consists of fine striations and growth scars from earlier positions of outer lip, two or three in random position per whorl. Adult size 4.0–5.5 mm long and 2.5–3.5 mm wide range (N = 6) (Fig.
Body
fully retractable into shell, mantle light cream-colored, pseudopallium whitish to light yellow in color; short and rounded tentacles, eyes round, black at the base of each tentacle (Fig.
Proboscis
funnel-shaped, forming a flexible, semi-transparent or white non-retractable tube (Fig.
The larval shell shows some intraspecific variations in adults. It is glassy, low, and rounded to mucronate. This seems to be related to the protection of the pseudopallium when it is immersed inside the respiratory tube. The juvenile develops the pseudopallium relatively early, when it has 1.5 whorls, and protects the shell from this stage onwards; at the same time, it is attached to an area of the host’s skin respiratory tree (Fig.
Inside the posterior whorls of the shell, all adults and subadults presented pink oocytes or germinal cells. Two oval-shaped egg capsules were found situated between the shell and the pseudopallial folds, in one specimen (Fig.
Holotype
(
Palmyra Atoll, Central Pacific Ocean, shallow water in reef lagoon.
This species is being named after the collector Mr. J. Smith, as a means of recognition, for his sampling efforts.
Known only from the type locality.
Female shell globose to conical, transparent, fragile, glassy, colorless, fine incremental axial stria; apex mucronate glassy white not tilt; proboscis slightly dark; large pedal gland.
Shell
globose, translucent, thin, fragile, colorless, smooth sculpture, with fine axial striae, several growth scars of earlier outer lip positions are irregularly spaced, suture impressed. Adult shell 6.5 mm long; 4.0 mm wide; body whorl 4.5 mm long (holotype Fig.
Soft tissues
pale cream with reddish pigmentation, seen through transparent shell. Pseudopallium cauldron-shaped in sub-adults arising from the aperture and covering large part of shell, or short mantle folds not covering female shells, smooth. When skin was removed, a thick, rounded pedal gland was visible in the aperture (Fig.
The new species shares several shell and morphological traits with the other five congeneric species. A comparison of the most important structures, almost all based on the literature, is provided in Table
Megadenus smithi sp. nov. A holotype female in apertural and posterior views (
Megadenus holothuricola Rosén, 1910 was described from the Bahamas Islands, Caribbean, more than one hundred years ago. The low occurrence of finding this kind of endoparasites, 2% as in this study, had already been reported elsewhere:
Holothuria mexicana is the largest holothurian in the Gulf and Mexican Caribbean Sea, reaching up to 50 cm in length. The hindgut (cloaca) bears highly branched outgrowths that extend anteriorly, the respiratory trees. The function of the pair of respiratory trees is to take oxygen from the water, but at the same time they are excretory organs in combination with the intestine. Nitrogenous waste (ammonia) is carried by coelomocytes to the respiratory trees and released through pumping systems (
An egg capsule was described and illustrated by
Another pending question is how these endoparasites migrate from one to another holothurian. Juveniles were found attached to the pseudopallial wall of an adult specimen and was immersed in the same main respiratory tree tube of the host (Fig.
Further research on this eulimid parasites is now compromised in the southern Gulf of Mexico, because the holothurian populations have collapsed due to over exploitation. This illegal practice has been interdicted by a law that prohibits the extraction of holothurians in the area (
Unai Markaida helped by contacting the fishermen and provided lab facilities in