Comp. Parasitol. 71(1), 2004, pp. 9–12

Heterophyopsis hawaiiensis n. sp. (: ) from the Hawaiian Monk Seal, Monachus schauinslandi Matschie, 1905 (Carnivora: Phocidae)

1,4 2 3 MURRAY D. DAILEY, MICHAEL M. KLIKS, AND RICHARD S. DEMAREE 1 The Marine Center, Marin Headlands, 1065 Fort Cronkhite, Sausalito, California 94965, U.S.A. (e-mail: [email protected]), 2 CTS Foundation, 3081 G. Paty Drive, Honolulu, Hawaii 96822, U.S.A., and 3 Department of Biological Sciences, California State University, Chico, California 95929, U.S.A.

ABSTRACT: Heterophyopsis hawaiiensis n. sp. (: Heterophidae) is described from the ileum and colon of the endangered Hawaiian monk seal, Monachus schauinslandi. An 11-mo-old juvenile female M. schauinslandi found dead on Eastern Island of Midway Atoll, Northwestern Hawaiian Islands, U.S.A., contained approximately 7,000 specimens of this species. The new species differs from existing Heterophyopsis species in having a trilobed ovary, testes slightly oblique, and vitellaria reaching posterior of the body. This is the first report of the genus Heterophyopsis found in both a marine mammal and in the central Pacific region. KEY WORDS: Digenea, Heterophyidae, Heterophyopsis hawaiiensis, Hawaiian monk seal, Monachus schauinslandi, Midway Atoll, Northwestern Hawaiian Islands, U.S.A.

The Hawaiian monk seal, Monachus schauinslandi, was stored in 70% ethyl alcohol for later examination. is an endangered species that has been intensively Worms were stained in aqueous carmine or Erlich’s hematoxylin, dehydrated in 100% alcohol, cleared in xylene, studied by the National Marine Fisheries Service for and mounted in Canada balsam. Worms selected at random the past 10 yr. Its helminth fauna has been examined were dehydrated and embedded in LR white acrylic resin, opportunistically or systematically on various occa- sectioned at 8 lm, and stained with methylene blue and sions during the past 75 yr (Chapin, 1925; Golvan, azure B. Additional worms were dehydrated in 100% ethanol and dried in hexamethyldisilazane, gold coated, 1959; Whitlow et al., 1979; Dailey et al., 1988; Banish and examined by scanning electron microscopy. Drawings and Gilmartin, 1992). Before this report, eggs of an were made with a drawing tube mounted on an Olympus unknown digenetic trematode were found in 8 of BX50F3Ò microscope. All measurements are ranges 82 monk seal feces samples collected in the North- followed parenthetically by means and are presented in western Hawaiian Islands (NWHI) (Dailey et al., micrometers unless otherwise indicated. The neotype of Heterophyopsis expectans (Africa and 1988). Eggs identical to those of the trematode Garcia, 1935; Tubangui and Africa, 1938) deposited by described below were recovered by way of fecal loop Velasquez (1973) in the U.S. National Parasite Collection from 4 of 288 Hawaiian monk seals sampled at French (USNPC 72449) was examined during this study to verify Frigate Shoals, NWHI (M.M.K., unpublished data). morphological differences between species. During the examination of a formalin-fixed in- testinal tract of an 11-mo-old juvenile female Heterophyopsis hawaiiensis n. sp. Hawaiian monk seal that died on Eastern Island of (Figs. 1–3) Midway Atoll on 31 March 2001, approximately Description 7,000 heterophyid trematodes were collected from the Based on 20 specimens, Heterophyinae Leiper, last 6 m of the ileum and colon. These worms 1909. With characters of the genus: body, length 1.4– belonged to an undescribed species of Heterophyop- 2.3 (2.0) mm, maximum width 570–750 (648) at sis Tubangui and Africa, 1938. ovary, hind body moderately expanded. Tegumental spines prominent on anterior, becoming less prom- MATERIALS AND METHODS inent posteriorly. Oral subterminal, length 95– The preserved intestine was divided into 1-m sections, slit 125 (106), width 100–130 (113); prepharynx, length longitudinally, and washed into a container. The cleaned 55–175 (112); pharynx, length 117–152 (130), width mucosal surface was then scraped to remove any remaining helminths and observed for lesions. All washings were 67–86 (75); esophagus short, length 12–50 (26); cecal repeatedly rinsed in tap water, and the remaining material bifurcation 242–362 (301) from oral sucker, extend- ing to posterior end of body. Ventral sucker, length 250–280 (260), width 100–262 (233). Testes 2, 4 Corresponding author. entire, slightly oblique in posterior of body, right

9 10 COMPARATIVE PARASITOLOGY, 71(1), JANUARY 2004

Figures 1–3. Heterophyopsis hawaiiensis n. sp. 1. Whole specimen, ventral view. 2. Genital pore surrounded by hooked bars. 3. Enlarged drawing (diagrammatic) of hooked bar.

testis usually larger than left; right testis, length 175– nonserrated bars, each 17.5 long. This entire complex 322 (207), width 137–170 (157); left testis, length is set in a weakly muscular cone-shaped gonotyl, 150–217 (183), width 130–187 (155). Seminal width 187–212. Ovary trilobed, length 90–150 (119), vesicle with 3 parts joined by constriction. Cirrus width 125–180 (158). Seminal receptacle large, sub- pouch lacking. Genital pore surrounded by an armed spherical, immediately posterior to ovary, length 150– genital sac containing a circle of 80–90 sclerotized 320 (235), width 130–187 (155). Uterus partially DAILEY ET AL.—HETEROPHYOPSIS HAWAIIENSIS FROM THE HAWAIIAN MONK SEAL 11 overlapping ceca and extending to posterior part of of this genus from a marine mammal as well as the body. Vitellaria posterior to testes, extending to level of first report from the central Pacific region. Hetero- gonotyl. Egg, length 27.5–32.5 (28), width 12.5–16 phyopsis hawaiiensis differs from both H. expectans (15). Excretory bladder Y shaped, reaching anterior to and H. continua in the relative position of the testes, level of ovary. Laurer’s canal not seen. which are opposite to slightly oblique rather than tandem in H. hawaiiensis; the shape of the ovary, Taxonomic summary which is distinctively trilobed rather than entire in H. hawaiiensis; and the distribution of vitellaria, which Type host: Hawaiian monk seal, M. schauinslandi reach the posterior end of body in H. hawaiiensis but Matschie, 1905. do not extend past the testes in H. expectans and Type locality: Eastern Island of Midway Atoll, H. continua. NWHI, U.S.A. (288129N; 1778209W). Collection date: 31 March 2001. Site of infection: Ileum and colon. ACKNOWLEDGMENTS Specimens deposited: Holotype and paratypes The authors thank Dr. George ‘‘Bud’’ Antonelis, USNPC, Beltsville, Maryland, 092301, 092302; Chief, Protected Species Investigation, NMFS–Hon- paratypes, Bernice P. Bishop Museum, Honolulu, olulu Laboratory, for making the specimens available Hawaii, F217, F218, F219. in addition to financial support for M.M.K. We also Etymology: This species is named after the host thank Dr. Mike Kinsella for his helpful comments; collection locality. Mr. David Wood for his illustrations; Dr. Eric Hoberg and Mrs. Pat Pilitt, United States National Parasite DISCUSSION Collection, for the loan of specimens; and The There are currently 2 species, H. expectans (Africa Marine Mammal Center, Sausalito, California, for and Garcia, 1935) Tubangui and Africa, 1938, and their continued support. Heterophyopsis continua (Onji and Nishio, 1916) Price, 1940, and a subspecies, Heterophyopsis continua major Yamaguti, 1939, considered valid in LITERATURE CITED the genus Heterophyopsis (Yamaguti, 1971). Hetero- Africa, C. M., and E. Y. Garcia. 1935. Heterophyid phyopsis expectans was originally described by trematodes of man and dog in the Philippines with Africa and Garcia (1935) in the genus descriptions of three new species. Philippine Journal of Cobbold, 1886, from the intestine of a dog examined Science 57:253–267. in Luzon, Philippine Islands. Tubangui and Africa Banish, L., and W. G. Gilmartin. 1992. Pathological findings in the Hawaiian monk seal. Journal of Wildlife (1938) later made it the type species for a new genus, Diseases 28:428–434. Heterophyopsis, differentiating it from the genus Chapin, E. A. 1925. Descriptions of new internal parasites. Heterophyes in arrangement of the testes, placement Proceedings of the United States National Museum 68: of vitellaria, and presence of comb-like sclerotized 1–4. bars instead of fine spines around the genital sucker. Dailey, M. D., R. V. Santangelo, and W. G. Gilmartin. 1988. A coprological survey of helminth parasites of Price (1940) accepted Heterophyopsis as a valid the Hawaiian monk seal from the Northwestern genus and transferred Heterophyes continua Onji and Hawaiian Islands. Marine Mammal Science 4:125–131. Nishio, 1916, from Heterophyes to Heterophyopsis Golvan, Y. J. 1959. Acanthocephales du genre Corynosoma with H. expectans as the type. Onji and Nishio (1916) Luhe, 1904, Parasites de mammiferes d’ Alaska et de Midway. Annales de Parasitologie Humaine et Com- had described H. continua from naturally infected paree 34:288–321. fish-eating in Japan. The same authors also Kim, K.-H., E.-S. Choi, and H.-J. Rim. 1996. Conger reported this species from man and dog in Japan. myriaster, a new second host of Heterophyopsis Yamaguti (1939) also lists a –fish cycle in Japan continua (Digenea: Heterophyidae). The Korean Jour- for his subspecies H. c. major. Velasquez (1973) nal of Parasitology 34:283–285. Onji, Y., and T. Nishio. 1916. On a new species of redescribed H. expectans from experimentally in- trematode belonging to the genus Heterophyes. Iji fected kittens fed metacercaria from the muscles of Shimbun 954:941–946. a fish (Pelates quadrilineatus Bloch) collected off Price, E. W. 1940. A review of heterophyid trematodes, Davao, Mindanao Island, Philippines. Kim et al. with special reference to those parasitic in man. Proceedings for the 3rd International Congress for (1996) report H. continua from excysted metacercaria Microbiology, New York, Section V:446–447. taken from a variety of brackish water and marine Tubangui, M. A., and C. M. Africa. 1938. The system- fishes. Heterophyopsis hawaiiensis is the first report atic position of some trematodes reported from 12 COMPARATIVE PARASITOLOGY, 71(1), JANUARY 2004

the Philippines. Philippine Journal of Science 67:117– seal. (’Elapaio) Journal of the Hawaiian Audubon 127. Society 38:83–84. Velasquez, C. C. 1973. Observations on some Hetero- Yamaguti, S. 1939. Studies on the Helminth Fauna of Japan phyidae (Trematoda: Digenea) encysted in Philippine XXV. Japanese Journal of Zoology 8:129–210. fishes. Journal of Parasitology 59:77–84. Yamaguti, S. 1971. Synopsis of digenetic Trematodes of Whitlow, G. C., G. H. Balaz, and G. D. Schmidt. 1979. Vertebrates. Vols. I and II. Keigaku Publishing Co., Parasitic ulceration of the stomach in a Hawaiian monk Tokyo. 1074 pp.

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