Systematic Parasitology 18: 133-138, 1991. 133 © 1991 Kluwer Academic Publishers. Printed in the Netherlands.

A new species of the genus Zalophotrema (Digenea: Campulidae), Zalophotrema atlanticum n. sp., from the liver of the striped dolphin Stenella coeruleoalba (Meyen, 1833) (Cetacea: Delphinidae) in Atlantic waters

E. Abril, J.A. Balbuena and J.A. Raga Departamento de Biologfa Animal ( Zoologia), Facultad de Ciencias BiolOgicas, Universidad de Valencia, Dr. Moliner 50, 46100 Burjasot, Valencia, Spain

Accepted for publication 27th June, 1990

Abstract

Zalophotrema atIanticum n. sp. from the liver of a striped dolphin, Stenella coeruleoalba (Meyen, 1833), stranded in the Canary Islands is described. This new species differs from the other Zalophotrema species in body dimensions and relative size and position of the suckers and cirrus-sac. This is the first record of a species of the genus Zalophotrema in the striped dolphin, and the Atlantic Ocean constitutes a new locality record for this genus.

Introduct ion

On April 9, 1985, a female striped dolphin, Stenella coeruleoalba (Meyer, 1833), stranded in Playa de Arencibia (Lanzarote, Canary Islands) was examined by Mr V.M. Martel (Sociedad para el Estudio de los Mam]feros Marinos del Archipi- 61ago Canario). During the dissection of the car- cass various parasite species were detected. Hel- minth specimens were collected and subsequently sent to us for further studies. A careful morpho- metric study of some trematodes from the liver suggests that they represent a new species of the family Campulidae Odhner, 1926.

The trematode parasites of cetaceans belong to nine families of which only four, the Brauninidae Bosma, 1931, Pholeteridae Dollfus, 1939, Nasitre- matidae Yamaguti, 1951 and Campulidae, are typical for this group of mammals. These families are exclusively formed by parasites of cetaceans with the exception of the family Campulidae,

which also includes several parasite species of pin- nipeds (Raga, in press).

The campulid trematodes are mainly parasites of the digestive tract of marine mammals, except for those of the genus Hunterotrema McIntosh, 1960, which occur in the lungs of freshwater dol- phins (Dailey, 1985). The life-cycles of the Cam- pulidae remain totally unknown and consequently their possible taxonomic relationships are mainly based on the adult morphology. Traditionally this family has been considered close to the Fascioli- dae Railliet, 1895 (Beverley-Burton, 1972). This hypothesis was initially supported by cladistic studies (Brooks et al., 1985). However, Brooks et al. (1989), in a subsequent taxonomic revision using cladistic analysis, suggested that affinity be- tween the Campulidae and the family Acanthocol- pidae Ltihe, 1906 exist: a possibility which was previously suggested by Cable (1974).

The taxonomy of the family Campulidae is, at present, rather controversial. Yamaguti's (1971)

134 E. Abril et al.

classification into six subfamilies was reviewed by Skrjabin (1976), who invalidated the subfamily Synthesinae Yamaguti, 1958. More recently, Adams & Rausch (1989) have not accepted as valid the Odhneriellinae Yamaguti, 1958, trans- ferring its species to the subfamily Orthosplanch- ninae Yamaguti 1958. Thus, pending further re- visions, only four subfamilies within the Campulidae are currently recognised: Campulinae Stunkard & Alvey, 1930, Hunterotrematinae Yamaguti, 1971, Lecithodesminae Yamaguti, 1958 and Orthosplanchninae.

Materials and methods

Four mature specimens previously fixed and pre- served in 70% ethanol were stained in alum car- mine and mounted in Canada Balsam. Measure- ments are given in micrometres unless otherwise stated, with the mean in parentheses. Figures were made with the aid of a drawing tube. Serial sections of 15/xm were cut and stained in Mayer's haematoxylin and eosin.

Zalophotrema atlanticum n. sp. (Figs 1, 2)

Definitive host: Striped dolphin, Stenella coeru- leoalba (Meyen, 1833) (Cetacea: Delphinidae). Site: Hepatic ducts. Type-locality: Canary Islands, central Atlantic Ocean. Intensity of infestation: Four individuals in one host. Type-material: Holotype in British Museum (Natural History) (Reg. No. 1989.9.11.1) and par- atypes in Department of Animal Biology, Univer- sity of Valencia (Coll. No. Sc-IC 001/85.04.09). Etymology: The specific name atlanticum is de- rived from the type-locality, emphasizing that this is the first occurrence of the genus Zalophotrema in the Atlantic Ocean.

Description

Body elongate, flattened dorso-ventrally, 18.79- 24.08 (20.18) mm long; maximum width at an-

terior half of body, 2.39-3.08 (2.64) mm (Fig. 1A). Tegument armed with small spines, more abundant anteriorly. Length of tegumental spines 39.6-43.2 (41.4). Oral sucker terminal, subcircu- lar, 951-1208 (1096) x 1,002-1,237 (1,111). Acet- abulum situated at beginning of middle third of body; similar in size to oral sucker, 925-1,413 (1,137) x 882-1,285 (1,041); distance to oral sucker 5,859-8,147 (6,560); ratio to body length 0.310-0.338 (0.323) : 1. Oral sucker to acetabulum ratios, 1.02-0.85 (1.05):1 (lengths) and 1.13-0.96 (1.06):1 (widths). Prepharynx short, 113-237 (160). Pharynx pyriform, 618-659 (639) × 391- 464 (423). Oesophagus very short. Intestine H- shaped exhibits median and lateral diverticles throughout its length. Posterior caeca terminating blindly, close to posterior margin of body; an- teriorly directed caeca extend close to level of oral sucker. Excretory vesicle tubular, pore terminal.

Testes deeply lobed, tandem, contiguous, lo- cated within posterior half of body. Anterior testis 1,440-1,979 (1,658) × 1,516-1,850 (1,619). Post- erior testis 2,008-3,224 (2549) × 1,184-1,669 (1/552) situated at 5,243-6,656 (5834) from caudal extremity of body; ratio to body length 0.2508- 0.3524 (0.2891) : 1. Cirrus-sac short, stout, 1,616- 1,928 (1,741) × 514-668 (572) never extending posteriorly beyond acetabulum. Ratio of cirrus- sac length to body length 0.080-0.095 (0.086):1. Cirrus unarmed. Internal seminal vesicle 668- 1,362 (964) × 308-514 (424). Genital pore medial, opens at 360-875 (584) from anterior margin of acetabulum and at 5,962-8,965 (6,785) from an- terior extremity of body. Ratio of the latter to body length 0.248-0.444 (0.336) : 1 (Fig. 2A).

Ovary deeply lobed, pre-testicular, medial, al- most contiguous with anterior testis; 591-874 (694) × 899-1,156 (990). Situated at 1,208-1,491 (1,238) from acetabulum, ratio to body length 0.055-0.064 (0.061):1. Mehlis' gland dorsal to ovary. Laurer's canal present. Vitellarium follicu- lar, profusely developed, occupying whole an- terior half of body from post-pharyngeal level to level of genital pore; diverging posteriorly from level of genital pore in two lateral fields, terminat- ing at 124-299 (227) from caudal extremity. Vitel- line reservoir oval, postero-dorsal to ovary; 70-

A new campul id f rom the str iped dolphin 135

I 2 , 5 m m

A O S

IC

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R

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Fig. 1. Zalophotrem atlanticum n. sp. A, Entire specimen, ventral view; B, Eggs. Abbreviations: A, acetabulum; CP, cirrus-sac; IC, intestinal caecum; O, ovary; OS, oral sucker; P, pharynx; T, testis; U, uterus; V, vitellarium; VD, vitelloduct: VR, vitelline reservoir.

136 E. Abril et al.

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0,5 rnm CP

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Fig. 2. Zalophotrema atlanticurn n. sp. Detail of terminal geni- talia. Abbreviations: A, acetabulum; CP, cirrus-sac; DMD, distal male duct; GP, genital pore; ISV, internal seminal ves- icle; M, metraterm; MS, muscular sphincter; U, uterus

133 × 152-278 (109 × 202). Medial, anteriorly descending vitelloduct bifurcates to form pair of ducts at level of genital pore, which pass around uterine field and open separately into vitelline res- ervoir. Pair of posteriorly ascending vitelloducts run parallel to one another along both lateral vit- elline fields and open into vitelline reservoir. Ut- erus voluminous, deeply coiled, pre-ovarian, dor- sal to acetabulum. Metraterm present, opening into genital pore. Eggs oval, operculate, circular in cross section; 54-61 (58) x 40-47 (43) (Fig. 1B).

Discuss ion

The morphology of the present material conforms with that of the family Campulidae and, more

precisely, with the subfamily Campulinae because of the vitellarium arrangement and the presence of intestinal caeca with median and lateral di- verticles (Yamaguti, 1971). According to Yama- guti (1971), this subfamily comprises two genera: Campula Cobbold, 1858 and Zalophotrerna Stun- kard & Alvey, 1929. In spite of the confusion concerning the validity of some genera of the Campulidae (see Adams & Rausch, 1989; Bal- buena et aI., 1989), the generic identity of Zalo- photrema seems to be well established because the eggs of the species of this genus are circular in cross section (Price, 1932; Delyamure, 1955; Yamaguti, 1971). Our specimens exhibit this fea- ture and thus are assigned to this genus.

So far, four Zalophotrema species have been described: (1) Z. hepaticum Stunkard & Alvey, 1929, a parasite from the bile ducts of Californian sea lions, Zalophus californianus (Lesson, 1828), in captivity (Stunkard & Alvey, 1930; Price, 1932); also reported in the wild from Californian and Steller's sea lions, Eumetopias jubatus (Schreber, 1776), off the Pacific coast of North America (Stroud & Dailey, 1978; Sweeney & Gil- martin, 1974) [Grafton (1968) tentatively ident- ified as Z. hepaticum some digeneans parasitising the liver Of an Amazon River dolphin, Sotalia fluviatilis (Gervais, 1853), found dead in a com- mercial aquarium, however, no further details on the identity of these worms are available]; (2) Z. curilensis Gubanov in Delyamure, 1955 a bile- duct parasite of the sperm whale Physeter macro- cephalus L., 1758 in the Okhotsk Sea (Delya- mure, 1955); (3) Z. lubimowi Petrov & Chert- kova, 1963 reported parasitising the liver of a southern sea lion Otaria byronia (Blainville; 1820) at Moscow Zoo (Petrov & Chertkova, 1963); and (4) Z. pacificum Dailey & Perrin, 1973 from the bile and pancreatic ducts of spinner and spotted dolphins, Stenella longirostris (Gray, 1828) and S. attenuata Gray, 1846 (= S. graffmani), in the eastern Tropical Pacific and the SW Indian Ocean (Dailey & Perrin, 1973; Gibson & Harris, 1979).

Z. hepaticum possesses a shorter and wider body than that of the present material. In ad- dition, the oral sucker of this species is consider- ably larger than the acetabulum and the latter is

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A new campulid from the striped dolphin 137

located on the anterior third of the body (Table I) (Stunkard & Alvey, 1930; Price, 1932).

The species Z. curilensis differs from the speci- mens examined in much greater maximum width attained at the testicular level. The acetabulum is larger than the oral sucker and both suckers are smaller than those of the helminths studied. In addition the testes of Z. curilensis are consider- ably larger than those of the present material (Table I) (Delyamure, 1955).

Z. lubimowi possesses a shorter and wider body than that of our digeneans. The size of the acet- abulum is approximately half of that of the pre- sent material and it is situated on the anterior third of the body (Table I). Furthermore, no an- teriorly confluent vitelline fields are present (Pe- t rov& Chertkova, 1963).

Some of the body ratios of Z. pacificum are similar to those of the present material. However, this species differs greatly from our helminths in body dimensions, the latter being in body length, maximum width and sucker size at least twice those of mature specimens of Z. pacificum (Table I). In addition, examination of six type-specimens of Z. pacificum from eastern Tropical Pacific wat- ers and 16 specimens from SW Indian Ocean re- vealed a more acute anterior extremity of the body. Also, the genital pore opens closer to the anterior margin of the acetabulum (220-288 (257) vs. 360-875 (584) in our specimens). Remarkable differences in shape and disposition of the cirrus- sac were also observed. Notably, the cirrus-sac of Z. pacificum is disposed along the longitudinal axis of the body dorsally to the acetabulum, while this structure is situated more transversally, sur- rounding the acetabulum in the Atlantic speci- mens. Furthermore, the ratio of the cirrus-sac length to body length in Z. pacificum is clearly different (0.031-0.048 (0.038):1 vs. 0.080-0.095 (0.086) : 1 in the present material).

In view of the above mentioned differential characters, it is considered that the material stud- ied represents a new species of the genus Zalopho- trerna, namely Z. atlanticum n. sp. This is the first report of a member of the genus Zalophotrema parasitising the striped dolphin and the Atlantic Ocean is a new locality record for this genus.

138 E. A b r i l et al.

Acknowledgements

T h e au thors wish to t h a n k M r V . M . M a r t e l ( S E M -

M A C ) who k ind ly m a d e the d i g e n e a n spec imens

ava i lab le for s tudy. T h a n k s are also due to D r

M . D . D a i l e y (Ca l i fo rn ia S ta te Un ive r s i ty ) , D r

J .R . L ich tenfe l s (Na t iona l Paras i t e Co l l ec t ion ,

U S D A ) , D r D . I . G i b s o n and Mrs E . A . Ha r r i s

(Bri t ish M u s e u m (Na tu ra l H i s to ry ) ) for the loan

of t y p e - s p e c i m e n s of Z. paci f icum.

Cri t ic i sm and sugges t ions f rom two a n o n y m o u s

re fe rees and the E d i t o r - i n - C h i e f of Systematic

Parasi tology are g ra te fu l ly a c k n o w l e d g e d .

This inves t iga t ion was s u p p o r t e d by the G e n e r a l

D i r e c t o r a t e o f Scientif ic and Techno log ica l Re-

search ( D G I C Y T ) of the Span ish G o v e r n m e n t

(Pro jec t No . PB87-997) . J . A . B a l b u e n a holds a

doc to ra l scho la r sh ip f rom the Conse l l e r i a de Cul-

tura E d u c a c i o i C ienc ia of the G e n e r a l i t a t Va len-

c iana.

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