Cestoda: Dilepididae) from the Whiskered Auklet, Aethia Pygmaea, in the Western Aleutian Islands, Alaska, with a Comment on the Genera Alcataenia and Rissotaenia

Proc. Helminthol. Soc. Wash. 51(2), 1984, pp. 315-319

Alcataenia pygmaeus sp. n. (Cestoda: Dilepididae) from the Whiskered Auklet, Aethia pygmaea, in the Western Aleutian Islands, Alaska, with a Comment on the Genera Alcataenia and Rissotaenia

ERIC P. HOBERG Wildlife Science, College of Forest Resources AR-10, University of Washington, Seattle 98195

ABSTRACT: Alcataenia pygmaeus sp. n. is described from whiskered auklets, Aethia pygmaea (Gmelin), from the western Aleutian Islands, Alaska. It is distinguished from its congeners by the overall small size of the strobila and a combination of other characters. The rostellum is armed with 34-38 hooks that measure 41-49 fj.m in length. The cirrus sac is relatively short, 101-174 jum in length, and reaches or just crosses the poral osmoregulatory canals. There are 36-50 testes located entirely posterior to the female organs. The scolex is deeply embedded in the mucosal tissue of the duodenum of the host. This is the first dilepidid to be recorded from Aethia pygmaea. In addition the genus Rissotaenia Spasskaia and Kolitolova, 1972 was found to be identical to Alcataenia Spasskaia, 1971 and is suppressed as a synonym.

Dilepidid cestodes representing a previously 156-212 wide at base of scolex. Scolex (TV = 20) undescribed species of Alcataenia Spasskaia, 1971 354-495 (452) in transverse diameter. Suckers have been collected from whiskered auklets, Ae- (JV =42) 153-203 (180) in greater diameter. thia pygmaea (Gmelin) (Charadriiformes: Alci- Rostellum (N = 12) strongly muscular, 232-389 dae), in the western Aleutian Islands, Alaska. (284) long by 120-229 (193) at apex; armed with Immature cestodes were recovered from three 34-38 (36) (N = 15 scolices) hooks in two reg- birds collected in 1974, and several mature spec- ularly alternating rows, measuring 41-49 (43) imens and a single gravid specimen were found (N=SQ). Blade 15.1-20.1 (17.9) long, handle in four of five birds collected in 1982. This is the 20.9-30.2 (25.5) long; blade: handle ratio 1:0.54- first dilepidid cestode to be described from birds' 0.94. Rostellum with minimum of four glandular of the genus Aethia. In addition only one other regions terminating near center of rostellar pad. cestode, Diorchis pelagicus Hoberg, 1982, typi- Rostellar sac 217-261 in diameter containing cally occurs in seabirds of this genus (Hoberg, mass of densely staining tissue with prominent 1982). nuclei surrounding base of rostellum. Dorsal ex- cretory canals 4-7.5 in diameter; ventral canals Materials and Methods 11-21, connected by transverse canal 6-10 in In the field, cestodes from auklets were either fixed diameter near posterior border of segment. Oc- in boiling 10% formalin (1974) or killed with boiling casionally ventral canals joined by multiple anas- water prior to fixation with 10% buffered formalin tomoses. Genital pores irregularly alternating. (1982). Portions of the host intestine with worms in Genital atrium (7Y= 14) muscular, 73-102 long situ were also preserved. Cestodes were stained in Semichon's acetic carmine and prepared as whole by 58-73 wide, situated in anterior Vi of pro- mounts. Two specimens, fixed in situ, were prepared glottid. Genital ducts passing dorsally to osmo- as 15-Mm paraffin sections stained in hematoxylin-eos- regulatory canals. Genital anlagen visible by 1 Oth in. All measurements are in micrometers unless stated segment; testes by about 19th; ovary by about otherwise; ranges of measurements are followed by mean values in parentheses. The following description 30th; fully mature by 40th; and first ova appear is based on 20 specimens mounted entire, and 2 spec- in uterus about 50th segment. Cirrus sac (N = imens sectioned in situ. 30) cylindrical, just reaching across poral osmoregulatory canals, 101-174 (130) long by 23- Alcataenia pygmaeus sp. n. 49 (36); containing coiled vas deferens. Cirrus (Figs. 1-5) (7Y= 11) unarmed, 14-26 (21) in diameter. Vas DESCRIPTION: Strobila weakly craspidote, up deferens highly coiled, dorsal to ovary up to 17 to 16 mm long and with 76 proglottids. Segments in diameter. Testes (N= 30 segments) 36-50 (42) wider than long: immature, 200-413 long by 448- in number; (N = 50) 61-81 (71) long by 44-70 590 wide; mature, 531-731 long by 672-1,191 (55) situated in two layers entirely posterior to wide; gravid, 879 long by 2,109 wide. Neck short, female organs. Vagina (N = 20) thick-walled,

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14.5-29 in diameter with lumen 3-6; maximum Systematics and taxonomy length 213-348 in mature and pregravid segments; entering genital atrium posterior to cirrus The genus Alcataenia Spasskaia, 1971 was es- sac. Seminal receptacle (N = 15) pyriform, 87- tablished for three species of dilepidid cestodes 174 (137) long by 29-75 (51), situated dorsal to from Alcidae (Charadriiformes), viz., A. cam- ovary; proximal end with strongly developed pylacantha (Krabbe, 1869) from Cepphus spp. sphincter. Ovary highly lobed, with two wings; (type); A. armillaris (Rudolphi, 1810) and A. smaller poral wing joined to larger antiporal wing meinertzhageni (Baer, 1956) from Uria spp. by narrow isthmus; situated in anterior '/2 of (Spasskaia, 1971). It was distinguished from proglottid ventral to other female organs except Anomotaenia Cohn, 1900 on the basis of the uterus; overall length (N = 15) 118-236 (191) by distribution of rostellar hooks (in A. campyla- 413-719 (612) in width. Vitelline gland (N = 12) cantha every third hook is in the anterior row); lobed, 58-94 (82) long by 131-247 (192) wide. a flat, coarse reticular uterus; a strongly muscular Mehlis gland (N = 10) 58-93 (70) in diameter, genital atrium; mature eggs that lack polar fila- situated dorsal to vitelline gland. Uterine stem ments; and apparent ecological and phylogenetic arising from dorsal surface of Mehlis gland, pass- specialization of the host-group. The genus Ris- ing to ventral surface of ovary. Uterus initially sotaenia Spasskaia and Kolitolova, 1972 was es- develops as a flat, coarse, highly lobed reticulum tablished for two species of dilepidids from Lar- that has extended beyond osmoregulatory canals idae, viz., R. larina (Krabbe, 1869) (type) and when first ova appear; eventually assuming a sac- R. dominicanus (Railliet and Henry, 1912) culate form when fully gravid. Eggs numerous, [Odening (1982) would also include R. micran- ovoid, elongate, outer envelope (7V= 6) 69-87 tha (Krabbe, 1869)] (Spasskaia and Kolitolova, (74) long by 46-56 (52); embryophore (N = 50) 1972). It was distinguished from Alcataenia on 44-56 (49) long by 22-28 (24), containing ovoid the basis of the uterus, a reticulum composed of oncosphere (N = 50) 23-28 (25) long by 17-22 a series of large loops, and from Anomotaenia (20). Walls of embryophore 1.0-2.5 thick. Em- by having eggs without filaments; a muscular bryonic hooks (N = 35) 12.7-13.9 (13.2) for lat- genital atrium; and ecological and phylogenetic eral pairs; 11.6 for median groups. relationships of the host-group. The genus Ano- TYPE HOST: Aethia pygmaea (Gmelin), whisk- motaenia in charadriiform birds was thought to ered auklet (Charadriiformes: Alcidae). represent cestodes that had a reticulate uterus of LOCALITY: Buldir Island, Alaska (lat. 52°21'N; a form different from that reported for either long. 175°56'E). Alcataenia or Rissotaenia; a weakly developed HABITAT: Duodenum, deeply embedded in the genital atrium; and eggs with polar filaments mucosa. (Spasskaia and Spasskii, 1978). SPECIMENS: Holotype: USNM Helm. Coll. No. Based on recent studies of cestodes from alcids 77546, collected by D. J. Forsell, July 1982. and larids in the North Pacific Ocean and Bering Paratype 1: No. 77547, an early mature specimen Sea, and on a reexamination of Krabbe's (1869) collected July 1982. Paratypes 2 and 3: No. 77548, type series of A. campylacantha, A. socialis (a collected July 1974. A supplementary specimen, synonym of A. armillaris), R. larina, and R. mi- also listed under No. 77548, is a single worm cracantha, Baer's (1956) types of A. meinertz- sectioned in situ. hageni and additional specimens of A. armillar- ETYMOLOGY: The species name pygmaeus is is, A. campylacantha, R. larina, and R. derived from the Latin "pygmaea" for "dwarf- micracantha redescribed by Baer (1956) it was ish" indicating the small size of members of this apparent that the uterus was identical in structure species. In addition pygmaea is the specific name in those taxa that represent Alcataenia and Ris- of the type and only known host for this species sotaenia. As the distribution of hooks on the of cestode. rostellum of A. campylacantha has taxonomic

Figures 1-5. Alcataenia pygmaeus sp. n. 1. Scolex. 2. Rostellar hooks. 3. Ventral view of mature segment. 4. Early development of the uterus showing reticular structure. 5. Oncosphere contained within thick-walled embryophore. All scales in micrometers.

Copyright © 2011, The Helminthological Society of Washington 318 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY significance only at the specific level, there are the western North Pacific (Krabbe, 1869; Baer, no morphological differences that can be used to 1956; Spasskaia and Kolitolova, 1971). A. pyg- differentiate these two genera. Supposed ecolog- maeus is also clearly distinguished from the re- ical isolation of the primary host-groups, al- maining species ofAlcataenia in which the max- though not an acceptable taxonomic character, imum number of hooks in representatives of any is also not constant because at least two species, taxon is 30. A. armillaris and R. larina have the same species of euphausiid crustacean as an intermediate host Pathology (Shimazu, 1975). Consequently Rissotaenia is The scolex of specimens of A. pygmaeus is suppressed as a synonym ofAlcataenia. Odening characteristically deeply embedded in the mu- (1982) already pointed out the similarity of A. cosal tissue of the duodenum of its host. Among meinertzhageni to species placed in the genus pelagic seabirds, this situation has been reported Rissotaenia. for three other species of cestodes, viz., A. ar- The genus Alcataenia contains seven nominal millaris and A. meinertzhageni in Uria spp. taxa: A. campylacantha (type), A. armillaris, A. (Krabbe, 1869;Baer, 1956)and Parorchites zederi meinertzhageni, and A. pygmaeus sp. n. from (Baird, 1853) in penguins, Aptenodytes forsteri, alcids, and A. larina comb, n., A. micracantha Pygoscelis adeliae, P. papua, and P. antarctica comb. n. sensu Odening (1982), and A. domin- (Fuhrmann, 1921; Ippen et al., 1981). In infec- icanus comb. n. sensu Odening (1982) from lar- tions with A. pygmaeus, the cestodes are embed- ids. Alcataenia is considered valid pending com- ded individually rather than occurring in groups pletion of a more detailed analysis of this genus as has been reported in other avian species. The and its relationships to Anomotaenia (Hoberg, lesions associated with A. pygmaeus are also not in prep.). Morphological characteristics defined as extensive. Lesions associated with infections by Spasskaia and Spasskii (1978) for Anomo- of other species ofAlcataenia or Parorchites are taenia indicate that it is probably distinct from often massive and may cause a noticeable swell- Alcataenia. ing on the serosal surface of the intestine. With Alcataenia pygmaeus sp. n. is clearly distin- infections of Parorchites, the intestine may be guished from all other species of Alcataenia by perforated and adhesions may develop (Hoberg, its small size (16 mm), consistently smaller or- pers. obs.). On the mucosal surface there is often gans, and relatively few segments (76) when grav- a fibrous collar that surrounds the neck of the id. Representatives of species of Alcataenia are cestode or group of cestodes at the point of in- generally large, with several hundred segments, sertion. In A. pygmaeus, there was no evidence and range in length from 40-80 mm for A. larina, of infection on the serosal surface, and the ces- 47-65 mm for A. dominicanus, 80-120 mm for todes were never surrounded by a fibrous collar A. micracantha, about 80 mm for A. meinertz- at the point of insertion. The scolex was enclosed hageni, 50-60 mm for A. campylacantha, and in a deep cavity lined with a thin wall of fibrous greater than 42 mm for A. armillaris (Schiller, connective tissue. The scolex sometimes extend- 1951; Baer, 1956; Odening, 1982). The cirrus ed to the depth of the muscularis mucosae. The sac, 101-174 /j.m in length, is shorter than that surrounding tissue was densely infiltrated with in A. armillaris (204-274), A. meinertzhageni lymphoid cells, predominately lymphocytes and (160-182), A. micracantha (up to 216), A. plasma cells. Heterophils and histiocytes were dominicanus (155-266), and A. larina (>240). occasionally present. The lesions were extensive; The number of testes (36-50) is greater than that infiltration and fibrosis extended through the reported for A. micracantha (13-18), A. cam- muscularis mucosae into the muscularis externa pylacantha (15-20), and A. dominicanus (up to and was accompanied by some erosion of the 28); about equal to that reported for A. armillaris intestinal epithelium. The lesions appear to be (33-40) and A. larina (up to 40); and less than of a chronic nature and were similar to those the number reported for A. meinertzhageni (53- reported by Baer (1956) for A. meinertzhageni. 56). The rostellar hooks are similar in form to those of other species in the genus. However, A. Discussion pygmaeus has 34-38 hooks that measure 41-49 This is the second record of cestodes from the yum. In this respect it is most similar to A. ar- whiskered auklet. It is of interest that A. pyg- millaris that has 20-25 hooks 35-46 ^m in length maeus was not found in a sample of 19 crested in specimens from the North Atlantic, and 20- auklets, Aethia cristatella collected from locali- 22 hooks 40-45 /urn in length for specimens from ties in the western Aleutian Islands where the

two avian species are sympatric. Additional Fuhrmann, O. 1921. Die Cestoden der Deutschen specimens of this ecologically similar auklet were Sudpolar Expedition 1901-1903. Deutsche Siid- polar Expedition 1901-1903. 16, Zool. 8:461-524. examined from St. Lawrence (20 birds) and St. Hoberg, E. P. 1982. Diorchis pelagicus sp. nov. (Ces- Matthew Islands (11) in the Bering Sea where toda: Hymenolepididae) from the whiskered auk- whiskered auklets do not occur. Of the 50 crested let, Aethia pygmaea, and the crested auklet, A. auklets examined from all localities, seven were cristatella in the western Aleutian Islands, Alaska. infected with two other species ofAlcataenia but Can. J. Zool. 60:2198-2202. Ippen, R., K. Odening, and D. Henne. 1981. Cesto- not A. pygmaeus. Specimens of least auklets, Ae- den (Parorchites zederi) und Sarkosporidienbcfall thia pusilla from St. Lawrence (26) and St. Mat- (Sarcocystis sp.) bei Penguinen der Siid-Shetland thew Islands (24) were not infected with any Inseln. Verhandl. des XXIII. Int. Symp. Erkran- species of dilepidid cestode. However, Smetan- kungen Zootiere Halle/Saale 1981. Akademischer Verlag Berlin, pp. 203-210. ina (1979) found specimens of Alcataenia ar- Krabbe, H. 1869. Bidrag til Kundskab om Fugelenes millaris infecting least auklets near Vladivostok, Baendelorme. Dansk Vidensk Sels. Skr., naturvid, USSR. Previous studies indicated that whiskered math. Afd. 8:251-368. and crested auklets share the hymenolepidid ces- Odening, K. 1982. Cestoden aus Flugvogeln der Siid- tode Diorchispelagicus Hoberg, 1982 only where shetlands (Antarktis) und der Falklandinseln (Malwinen). Angew Parasitol. 23:202-223. they co-occur in the western Aleutian Islands. Schiller, E. L. 1951. Studies on the helminth fauna This suggests that A. pygmaeus has a limited of Alaska VIII. Some cestode parasites of the Pa- geographic distribution, and is probably a host- cific kittiwake, (Rissa tridactyla Ridgway) with the specific parasite of the whiskered auklet. description of Haploparaxis rissae n. sp. Proc. Helminthol. Soc. Wash. 18:122-125. Shimazu, T. 1975. Some cestode and acanthoceph- Acknowledgments alan larvae from euphausiid crustaceans collected I should like to thank G. V. Byrd and C. P. in the northern North Pacific Ocean. Bull. Jap. Dau formerly of the Aleutian Islands National Soc. Sci. Fish. 41:813-821. (In Japanese, with En- glish summary.) Wildlife Refuge, Adak, Alaska and D. J. Forsell, Smetanina, Z. B. 1979. Tsestody rybiadnykh ptits U.S. Fish and Wildlife Service, Anchorage, Alas- primorskogo kraia. Materialy nauchnoii Konfer- ka for providing specimens of auklets and their entsii vsesoyznogo obshchestva gel'mintologov parasites from the western Aleutian Islands. Type Vypusk 31. Tsestody i tsestodozy. Akad Nauk specimens of other species of Alcataenia were SSSR, Lab. Gel'mint. Moskva, 120-128. Spasskaia, L. P. 1971. Alcataenia gen. n. (Cestoda: kindly made available by C. Vaucher, Museum Dilepididae). Parazity zhivotnykh i rastenii. 6:12- d'Histoire Naturelle, Geneve. W. E. Giddens 14. confirmed some histological details in lesions as- , and E. M. Kolitolova. 1971. Alcataenia ar- sociated with infections of A. pygmaeus. I should millaris (Cestoda: Dilepididae) ot tikhookean- skikh chistikov. Izvest. Akad Nauk Moldavskoi also like to thank R. L. Rausch for helpful dis- SSR, Seriia biolog. i khimi. nauk. 3:83-85. cussions and for critically reviewing the manu- , and . 1972. Novyi rod tsepnei Risso- script. taenia gen. n. (Cestoda: Dilepididae) parasiti- ruiushchikh u chaek. Parazity zhivotnykh i ras- Literature Cited tenii. 8:51-58. , and A. A. Spasskii. 1978. Tsestody ptits Baer, J. G. 1956. Parasitic helminths collected in SSSR. Dilepididy limnofil'nykh ptits. Akad Nauk West Greenland. Medd. om Granland Bd. 124. SSSR Moldavskoi SSR. Inst. Zool. i fiziol. Izda- No. 10. 55 pp. tel'stvo nauka, Moskva. 315 pp.