Moniligerum blairi n. g., n. sp. and Nudacotyle undicola n. sp. (Trematoda: Digenea) from the West Indian Manatee, Trichechus manatus L.*. Murray D. Dailey 1, ...
Systematic Parasitology 11: 159-163, 1988 © Kluwer Academic Publishers, Dordrecht - Printed in the Netherlands
Moniligerum blairi n. g., n. sp. and Nudacotyle undicola n. sp. (Trematoda: Digenea) from the West Indian Manatee, Trichechus manatus L.* Murray D. Dailey 1, Wolfgang Vogelbein 2 and Donald J. Forrester 3
I Southern California Ocean Studies Consortium, California State University, Long Beach, CA 90840, USA 2Gulf Coast Research Laboratory, Ocean Springs, MS 39564, USA 3Department of Infectious Diseases, College of Veterinary Medicine, University of Florida, Gainesville, FL 32610, USA Accepted for publication 24thJuly, 1987
Moniligerum n. g. is erected for Moniligerum blairi n. sp. (Opisthotrematidae) and Nudacotyle undicola n. sp. (Nudacotylidae) is described, both from the small intestine of Trichechus manatus L. from Martin County, Florida. The new genus is placed in the family Opisthotrematidae Poche, 1926, subfamily Lankatrematinae Yamaguti, 1958. Moniligerum differs from other genera in the subfamily (Lankatrema Crusz & Fernand, 1954, and Lankatrematoides Blair, 1981) by the possession of an anterior collar and in the form of the ovary (compact and not transversely elongated) and vitellarium (single median lobed mass). Nudacotyle undicola differs from N. valdevaginatus, the most similar species, in body size, the length of the caeca, the shape of the vitellarium and the position of the genital pore, cirrus pouch and ovary.
In January 1980, the gastrointestinal tract of a West Indian manatee was received from D r Daniel K. Odell (University of Miami). The animal had been killed by a collision with a boat on 21 D e c e m b e r 1979 in H o b e Sound North, north of West Palm Beach, Florida, and its internal organs had been frozen until examined one month later at the University of Florida, Gainesville. The wall of the anterior small intestine contained small nodules which, when expressed, expelled small trematodes through an externalpore. Additional flukes of a dissimilar type were recovered in large numbers from the lumen of the small intestine in the same *Supported in part by Cooperative Agreement No. 14-16-0008-1204 from the US Department of Interior, Fish and Wildlife Service.Florida Agricultural Experimental StationsJournal Series No. 3820.
animal. These trematodes were found to be new to science and are described in this paper.
Materials and methods
The worms were fixed in alcohol-formalin-acetic acid for 24 hours and stored in 70% ethanol. Whole-mounts were stained with Semichon's acetocarmine and celestine blue B, dehydrated in a graded ethanol series, cleared in methyl salicylate and mounted in permount. Sections were cut at 8 and 12 micrometres. All measurements are in micrometres and are given as the mean with ranges in parentheses. Figures were made with the aid of a drawing tube.
Two new digeneans from a West Indian manatee
Family Opisthotrematidae Poche, 1926 Subfamily Lankatrematinae Yamaguti, 1958
ro 18 (17-20)x 8 (6-9); all with long polar filaments. Excretory pore terminal; vesicle Yshaped.
Moniligerum n. g. Diagnosis. Lankatrematinae. With distinct cephalic collar. Aspinose. Oral diverticula and dorsal cephalic lobes absent. Oesophageal bulb absent. Caeca terminate at mid-ovarian level. Uterus intercaecal and extracaecal. Vitellarium branched with eight to ten elongate lobes, extending laterally and anteriorly from centre. Excretory system not branched at periphery of body. Excretory vesicle Y-shaped. Parasites in small intestine of manatees. Type and only species: Moniligerum blairi n. sp. Etymology. The generic name Moniligerum (L. collar bearing) refers to the presence of a collar.
Type-host: Trichechus manatus L. (West Indian Manatee). Site in host: Encapsulated in wall of small intestine. Type-locality and date: Hobe Sound North, Martin County, Florida. 1979. Type-material: Holotype: USNM Helm. Coll. no. 79800. Paratypes: USNM Helm. Coll. no. 79800, University of Nebraska State Museum, H.W. Manter Laboratory no. 20792. Etymology: The specific name is for Dr David Blair, Department of Zoology, University of Canterbury, Christchurch, New Zealand, for his contributions to sirenian parasitology.
Discussion Moniligerum blairi n. sp. (Figs 1, 2) Description (Measurements based on 10 whole and 5 serially sectioned worms.) Body pyriform, 755 (585-881) long by 496 (312-632) wide with marked anterior collar and digitiform posterior projection. Tegument aspinose. Oral sucker subterminal, 129 (86179) long by 137 (101-187) wide. Pharynx absent. Oesophagus 100 x 17; caeca terminating at approximately two thirds of body length. Testes small, entire, oval, symmetrical, in posterior third of body, 65 (42-92) x 71 (42-120); cirrus pouch small, median, 84 x 12. Ovary large, 142 (112172) x 74 (56-98), immediately anterior to right testis (24-44% of body length from posterior end). Laurer's canal absent. Uterine seminal receptacle absent. Mehlis' gland median between testes. Uterus intercaecal and extracaecal, ascending and descending loops filling anterior (72%) of body. Male and female pores empty into common genital pore, median, ventral, anterior to digitiform posterior projection (Fig. 1). Vitellarium large, 241 (188-280) x 240 (192-300), median, immediately anterior to Mehlis' gland, composed of separate elongate extensions of various lengths. Eggs in ute-
The known monostome trematodes parasitizing mammals in the order Sirenia are of three families, the Labicolidae Blair, 1979, Rhabdiopoeidae Poche, 1926, and Opisthotrematidae Poche, 1926. The labicolids and rhabdiopoeids are restricted to dugongs, being found in the lips and gut respectively. The opisthotrematid digeneans represent a faunal link between these mammals and are found in both dugongs and manatees. Members of the genus Cochleotrema Travassos & Vogelsang, 1931 (C. indicum Sharma & Gupta, 1971; C. cochleotrema Travassos & Vogelsang, 1931) are found occupying a similar site (nasal passages) in the dugong and manatee respectively. The same situation (parasites occupying similar sites) occurs in the Lankatrema group where members are found encapsulated, similar to M. blairi, in various parts of the dugong stomach (Lankatrema mannarense, L. minutum) and ileum (L. microtyle, L. macrocotyle). An additional Moniligerum-like worm, as yet unpublished, has been found encapsulated in the small intestine of a beached dugong (personal observation, MDD). Blair (1981) reviewed the Opisthotrematidae, modifying the family diagnosis of Yamaguti (1971) and at the same time describing two new genera and six new species from the du-
M.D. Daily et al.
0 0.02I 5
4 Figs 1 & 2. Moniligerum blairi n. g., n. sp 1. Entire worm, ventral view. 2. Egg. Figs 3-5. Nudacotyle undicola n. sp. 3. Entire worm, ventral view. 4. Genitalia, dorsal view. 5. Egg. Abbreviations: AU, ascending uterus; C, collar; CP, cirrus pouch; DU, descending uterus; E, oesophagus; ESV, external seminal vesicle; IC, intestinal caecum; ISV, internal seminal vesicle; LC, Laurer's canal; M, metraterm; MG, Mehlis' gland; MS, muscular sphincter; O, ovary; OD, oviduct; OS, oral sucker; T, testis; U, uterus; V, vitellarium; VD, vitelline duct; VE, vas efferens. Scales in millimetres.
Two new digeneans from a West Indian manatee
gong. He recognized that the five genera in the family could be divided among three natural groups. Moniligerum blairi does not conveniently fall into any of these. However, by the length of its caeca (overlapping anterior half of ovary), postcaecal testes, small cirrus pouch and location in host (encapsulated in wall of intestine), M. blairi appears closest to the Lankatrema group (genera Lankatrema Crusz & Fernand, 1954 and Lankatrematoides Blair, 1981). The new genus can be distinguished from both the above by its possession of an anterior collar, the form of the ovary (entire instead of lobed and transversely elongated) and the form of its vitellarium (single, median lobed mass instead of two submedian or lateral groups of follicles).
Family Nudacotylidae Barker, 1916 Nudacotyle undicola n. sp. (Figs 3-5) Description (Measurements based on 10 whole mounts.) With characters of Nudacotyle. Body ovoid, 655 (601725) x 414 (382--452); maximal width at or near middle. Tegument aspinose. Oral sucker subterminal, 57 (52-64) wide by 55 (49--64) long, with mouth antero ventral. Oesophagus 41 (32-62) long. Intestinal bifurcation 10-13% of body length from anterior end; caeca 22 (18-28) wide extending length of body, ending blindly lateral to posterior quarter of ovary. Excretory system not branched laterally. Testes smooth, asymmetrical, with anterior tips partially overlapping posterior margin of vitelline mass; right testis larger than left, 142 (118181) x 106 (97-118); left testis 127 (109-175) x 95 (89-111). Male and female pores empty into common genital pore, sinistral, ventral, anterior to vitelline mass (53-60% of body length from anterior end). Cirrus pouch 238 (200-260)x 67 (56-80), curved, thick-walled, extending diagonally from external seminal vesicle to approximately equidistance between median line and left margin; containing internal seminal vesicle. External seminal vesicle 36 (29-45) long, extending diagonally from
area just anterior of ovary to anterior tip of right vitelline mass then recurving to base of cirrus pouch. Ovary pyriform, 118 (94-145) × 68 (57-77), located between testes, extending to near posterior body margin. Seminal receptacle absent. Laurer's canal present, passing between left vitelline duct and vas efferens. Vitelline masses compact, lobed, symmetrical 100 (77-133) long by 64 (52-79) wide. Uterus filling most available space in midbody, intracaecal and extracaecal. Metraterm thickwalled.
Type-host: Trichechus manatus L. Site in host: Lumen of small intestine. Type-locality and date: Hobe Sound North, Martin County, Florida. 1974. Type-material: Holotype: USNM Coll. no. 79801. Paratypes: USNM Coll. no. 79802, University of Nebraska State Museum, H.W. Manter Laboratory no. 20793. Etymology: The species name undicola (L) means sea-dwelling, referring to the fact that this is the first of this genus to be described from a marine host.
Discussion Currently, there are four species described in the genus Nudacotyle Barker, 1916 (N. novicia Barker, 1916; N. valdevaginatus Travassos, 1922; N. tertius Travassos, 1939; N. quartus Zdzitowiecki, 1980). Nudacotyle undicola closely resembles N. valdevaginatus in the position of the genital pore, cirrus pouch and ovary. In both species the cirrus pouch and genital pore are sinistral and the ovary is median. In N. novicia and N. tertius the cirrus pouch and genital pore are dextral, while the ovary is sinistral. Marshall & Miller (1979) reported N. novicia from an Ecuadorian bat with these organs in a reversed position. N. quartus has lobed testes and ovary, a follicular vitellarium and a large bodysize (963-1493). N. undicola differs from N. valdevaginatus in total length, (620-720 in N. undicola, 1300 in N. valdevaginatus) and width (450 in N. undicola, 800 in N. valdevaginatus). In addition,
M.D. Daily et al. the caeca, which extend to the posterior extremity in N. undicola, terminate anteriorly to the testes in N. valdevaginatus. Furthermore, the vitelline masses are compact and large in N. undicola, but are follicular and medium sized in N. valdevaginatus. This is the first report of this genus from a marine mammal.
Overstreet, Gulf Coast Research Laboratory, Dr Lee Goff, University of Hawaii, and Linda Ennis, Southern California Ocean~ Studies Consortium, for their help during the preparation of the manuscript.
References Acknowledgements We express appreciation to Daniel K. Odell and John E. Reynolds III at the University of Miami for providing the specimens, Cathy Beck Bonde, Robert K. Bonde of the U.S. Fish and Wildlife Center Sirenia Project, and Pamela P. Humphrey of the University of Florida for assistance in obtaining the specimens. We also thank Dr Robin
Blair, D. (1981) The monostome flukes (Digenea: Families OpisthotrematidaePoche and RhabdiopoeidaePoche) para~ sitic in sirenians (Mammalia:Sirenia).Australian Journal of Zoology, Suppl. Ser., No. 81, 1-54. Marshall, M.E. & Miller, G.C. (1979) New digenetictrematodes from Ecuadorian bats. Journal of Parasitology, 65, 913-917. Yamaguti, S. (1971) Synopsis of digenetic trematodes of vertebrates. Tokyo:KeigakuPublishingCo., 1074pp.