Acanthocephala) from Sperm Whales (Physeter Macrocephalus) Stranded on Prince Edward Island, Canada

Home , Acanthocephala, Bolbosoma, Polymorphidae

J. Helminthol. Soc. Wash. 60(2), 1993, pp. 205-210

Bolbosoma capitatum and Bolbosoma sp. (Acanthocephala) from Sperm Whales (Physeter macrocephalus) Stranded on Prince Edward Island, Canada

ERIC P. HOBERG,' PIERRE-YVES DAOusx,2 AND SCOTT McBuRNEY2 1 United States Department of Agriculture, Agricultural Research Service, Biosystematic Parasitology Laboratory, BARC East, Building 1180, 10300 Baltimore Avenue, Beltsville, Maryland 20705 and 2 Department of Pathology and Microbiology, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, Prince Edward Island, Canada CIA 4P3

ABSTRACT: Specimens of Bolbosoma capitatum (von Linstow, 1880) and Bolbosoma sp. were recovered from 2 male sperm whales (Physeter macrocephalus L.) that died following a mass stranding on Prince Edward Island, Canada. Some aspects of previous descriptions of B. capitatum have been incomplete, particularly with char- acteristics of the hooks of the proboscis being poorly denned. Females of B. capitatum were found to have 16- 18 longitudinal rows of hooks with either 7-8 or 8-9 hooks in each row. The largest hooks with strongly curved blades were apical to median (overall range 69-122 mm long), whereas the basal hooks were spinelike (68-91 /j.m long). The basal hooks had a unique transverse orientation of the roots, an attribute apparently shared only with B. physeteris Gubanov, 1952, among the 14 species of Bolbosoma from cetaceans and pinnipeds. Although Bolbosoma capitatum had apparently been reported from Physeter macrocephalus in the eastern Atlantic Ocean, none of these records could be substantiated. The current report constitutes a new geographic record (Gulf of St. Lawrence, Canada) and the first account of this parasite in sperm whales from North American waters. KEY WORDS: Bolbosoma capitatum, Physeter macrocephalus, acanthocephalans, cetaceans, stranding.

Acanthocephalans have seldom been reported examined for parasites. The first animal, an adult, 13.6 from large cetaceans in North American waters m long (males reach sexual maturity near 12.5-12.8 m [Best et al., 1984; Whitehead and Waters, 1990]), died (Van Cleave, 1953; Margolis and Dailey, 1972; on the afternoon of 1 October, and a necropsy was Margolis and Aral, 1989; Measures, 1992), al- performed on the morning of 4 October. All internal though some species ofCorynosoma Liihe, 1905, organs, except those of the head, but including the and Bolbosoma Porta, 1908, are considered typ- entire gastrointestinal tract, were examined. The sec- ical of whales and dolphins (Van Cleave, 1953; ond animal, 11.4m long, was towed offshore, with the 4 remaining whales, in the early evening of 1 October Deliamure, 1955). Additionally, relatively little but died shortly afterward. It was found beached, ap- is known about the helminth faunas of sperm proximately 50 km west of Covehead Harbor, 4 days whales (Physeter macrocephalus L.; Physeteri- later and examined at necropsy on the morning of 7 dae) in either the eastern North Pacific or the October. It was in an advanced state of postmortem decomposition, and only portions of the small intestine western North Atlantic oceans (Margolis and were examined for the presence of parasites. No disease Dailey, 1972; Margolis and Aral, 1989), and re- process was identified in either whale, and mishap was cent studies have suggested that acanthocephalan considered a plausible cause of the stranding. parasites may be useful in the definition of ce- Acanthocephalans were fixed in 10% formalin, stained tacean populations (Dailey and Vogelbein, 1991). with Semichon's acetic carmine, dehydrated, and mounted entire. The proboscises from 2 specimens In the current study, we present new records for were dissected for examination of the structure of the species of Bolbosoma from sperm whales in the hooks. Measurements are in micrometers unless spec- southern region of the Gulf of St. Lawrence, Can- ified otherwise; sample sizes (AO are followed by the ada. Additionally, new details of the morphology range with the mean and standard deviation in brack- ets. of Bolbosoma capitatum (von Linstow, 1880) are described. Results Materials and Methods Acanthocephalans of the genus Bolbosoma On the morning of 1 October 1989, 6 sperm whales were the only helminthic parasites recovered from stranded near Covehead Harbor on the northern shore either whale. Only 9 female specimens of Bol- of Prince Edward Island, Canada (46°24'N, 63°10'W), approximately 200 m from a bridge under repair. Two bosoma capitatum were found in the small in- of these whales, both male, subsequently died and were testine of the first whale (deposited in the U.S.

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VII

VIII

Figures 1-3. Bolbosoma capitatum (von Linstow, 1880). Scale bars = 100 /«n; same scale in Figures 1 and 2. 1. Armature of proboscis in lateral view showing structure and distribution of hooks in a row of 8 (numbered from the anterior, I-VIII). Note typical apical to median hooks (I-IV) with strongly curved blades and elongate

National Parasite Collection, U.S. Department anterior to posterior; 35-85 in length. The pos- of Agriculture, Beltsville, Maryland, No. 82700, terior field of spines was situated across the and in the New Brunswick Museum, St. John, broadest region of the bulb, also arranged in ap- New Brunswick, Canada, No. 10211). Three proximately 10 transverse rows and with an ir- specimens of a small Bolbosoma sp. were recov- regular gradient in length from the anterior to ered from the second whale but could not be the posterior ([TV = 30] 80-165 [115 ± 20.30]) definitively identified because the proboscis was (Fig. 3). The proboscis receptacle was 2,100-2,150 not extended in any of these immature females x 405-520 and extended beyond the posterior (U.S. National Parasite Collection, No. 82701). margin of the bulb. Lemnisci were broad, con- The short descriptions presented below augment voluted, and relatively short, not exceeding 3.4 current knowledge of species of the genus Bol- mm, and not extending into the narrow con- bosoma in cetaceans. stricted region. The uterine bell was located in Among 5 specimens of B. capitatum examined the far posterior; combined length of the vagina, in detail, all were females, measuring 51.5-69.0 uterus, and uterine bell was 5.3-7.7 mm. mm long by 2.0-2.3 mm in maximum width in Three immature female specimens of Bolbo- the trunk and showing early development of soma from the second whale measured 18.7-28.0 ovarian balls. The forebody was distinctly sep- x 1.0-1.07 mm. The cephalic bulb was 1.0-1.25 arated from the trunk by a narrow constricted mm in width; a prominent constriction separat- region up to 5.0 mm in length. The proboscis ing the forebody from the trunk was lacking. The was cylindrical and rounded, measuring (N = 3) proboscis receptacle was 1,580-2,100 x 390 and 575-760 (662 ± 92.99) x 380-475 (428 ± 47.52) the lemnisci were 750 in length; neither extended and armed with 16-18 longitudinal rows of 7-8 beyond the base of the bulb. The combined length (2 specimens) or 8-9 (1 specimen) hooks (usually of the vagina, uterus, and uterine bell was 3.05- 8). Hooks, apical to median in position, had 4.45 mm. It could not be determined whether prominent curved blades, were 4 in number, with these specimens were immature B. capitatum or the 4th hook being the largest in each row (num- referable to another species. bered from the anterior hooks measured: \[N = 6] 68-88 [78 ± 8.16], II [TV = 13] 78-101 [91 ± Discussion 7.28], III [N= 13) 91-114 [103 ± 6.98], IV [TV Bolbosoma capitatum was described briefly by = 16] 96-122 [112 ± 8.61]); these hooks had von Linstow (1880) from false killer whales strongly developed elongate roots (I [TV = 5] 52- (Pseudorca crassidens (Owen)). It was subse- 55 [53 ± 1.64], II [7V= 12] 70-96 [81 ± 7.56], quently redescribed by Porta (1906, 1908, 1909) III [N = 10] 88-104 [97 ± 8.49], IV [N = 16] with this information being perpetuated rela- 91-122 [110 ± 10.32]) (Fig. 1). Basal hooks tively unaltered by Meyer (1932), Deliamure numbered from the anterior, began with the 5th (1955), Petrochenko (1958), and Yamaguti hook, were 3-4 or 4-5 in number and spinelike (1963). Edmonds (1957, 1987) and Machado (V [TV = 1] 78, VI [TV = 1] 81, VII [TV = 4] 70- Filho (1964) have augmented this redescription, 81 [77 ± 5.32], VIII [TV= 9] 78-91 [82 ± 3.88], but some pertinent information is lacking for the IX [TV = 1] 68]) and with prominent roots ori- structure of the armature on the proboscis and ented transverse to the longitudinal axis of the bulb. proboscis (V [N = 6] 55-57 [57 ± 0.82], VI [TV In contrast to some keys (Meyer, 1932; Delia- = 6] 44-55 [50 ± 4.22], VII [TV = 6] 39-52 [46 mure, 1955; Petrochenko, 1958), B. capitatum ± 4.46], VIII [TV= 6] 31-40 [37 ± 3.14], IX [TV is similar to other species of Bolbosoma in having = 1 ] 34) (Figs. 1, 2). The enlarged cephalic bulb a distinct armature on the proboscis (spinelike was 2.22-2.35 mm wide and armed with 2 prom- basal hooks with reduced or transversely ex- inent fields of spines that were not confluent ven- panded roots and strongly curved apical to me- trally. In the anterior field, there were about 10 dian hooks with more typical elongate roots) and transverse rows with a gradient in length from the cephalic bulb (simple spines) (in agreement

roots and spinelike basal hooks (V-VIII) with reduced roots. 2. Armature of proboscis showing structure of roots on the largest median hook (IV) and spinelike basal hooks (V-VIII). Note that roots of the basal hooks are transversely elongate with respect to the longitudinal axis of the proboscis. 3. Armature of forebody showing pattern and structure of spines in the midregion of the posterior field of the inflated cephalic bulb.

Copyright © 2011, The Helminthological Society of Washington 208 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY with Porta, 1906, 1908, 1909; see Van Cleave, guish adequately between B. capitatum and B. 1953) (Figs. 1-3). The range for numbers of hooks physeteris, and apparent differences in the bulb and hooks per row on the proboscis in the current armature require confirmation (numbers of specimens was in general agreement, particularly transverse rows of spines and spine length) (De- with more recent detailed reports (14-16 longi- liamure, 1955). tudinal of 8 hooks [Edmonds, 1957], 18 longi- Among the 14 species of Bolbosoma listed by tudinal of 8 [Machado Filho, 1964], and 15-17 Amin (1985), 4 have been reported from sperm longitudinal of 6-8 [Edmonds, 1987]). whales: B. brevicolle (Malm, 1867), B. physeteris, Although the length and distribution of spines B. tuberculata Skrjabin, 1970, and B. capitatum on the cephalic bulb agreed with those depicted (from the eastern Atlantic basin, Mediterranean by Machado Filho (1964), von Linstow (1880) Sea, southern Australia; primarily from delphi- and Porta (1906, 1909) have described 2 fields nids and ziphiids). Although many of these spe- of spines that were confluent ventrally on the cies have apparently broad host and geographic bulb of B. capitatum. Voucher specimens of B. ranges (Shipley, 1899; Porta, 1909; Baylis, 1929, capitatum examined during the current study 1932; Meyer, 1932; Deliamure, 1955; Edmonds, (collected by C. Parona from Globicephalus svi- 1957, 1987; Yamaguti, 1963; Skrjabin, 1970; neval = G. malaena (Traill) in the Mediterranean Dailey and Vogelbein, 1991), records of species Sea; confirmed by H. J. Van Cleave [USNM of Bolbosoma from the northwestern Atlantic and 6299]) were found to have 2 distinct fields of the Gulf of St. Lawrence are limited (Van Cleave, spines, similar to specimens from the Canadian 1953; Measures, 1992). Cowan (1967) provided sperm whale. Thus, it is possible that the distri- the only report of B. capitatum in this region (in bution of spines on the bulb is variable or that Globicephalus melaena on the coast of New- B. capitatum represents a complex of at least 2 foundland), but it has apparently not been found poorly defined species. in the Gulf of St. Lawrence and appears to be The dimensions and structure of the hooks and rare in North American waters. roots of B. capitatum have not previously been Records of B. capitatum from P. macrocepha- determined accurately. Machado Filho (1964) lus could not be substantiated. Baylis (1932), in measured hooks on a proboscis that was not fully a review of cetacean helminths, apparently was extended and apparently obscured (I = 65 /im, the first to specify sperm whales as a host. How- II = 70, III = 70, IV = 72, V = 60, VI = 56, VII ever, accounts cited by Baylis (1932) did not refer = 40) and indicated that the largest hooks were to B. capitatum from P. macrocephalus (see von median in position. Although the lengths of Linstow, 1880; Shipley, 1899; Porta, 1906, 1908, hooks found in the current study exceeded those 1909; Hamilton, 1916; Meyer, 1931) and there reported by Machado Filho (1964), the general is no indication that new material was examined. distribution was similar. The transverse orien- Although commonly listed as a parasite from tation of the roots of basal hooks, depicted by sperm whales (Deliamure, 1955; Petrochenko, Porta (1906, 1909), appears to be rare among 1958; Dailey and Brownell, 1972), none of these species of the genus Bolbosoma. appear to constitute an original record. Notably, Two species, B. capitatum and B. physeteris neither Meyer (1932) nor Yamaguti (1963) rec- Gubanov, 1952, are the only members of the ognized P. macrocephalus as a host. Thus, our genus where a transverse orientation of the roots discovery of B. capitatum may represent a new of basal hooks of the proboscis has been recog- host record; otherwise, it suggests that this hel- nized (Porta, 1906;Deliamure, 1955). These spe- minth is a rare or an incidental parasite of sperm cies are similar in overall dimensions (females whales. of B. physeteris are 47-87 mm in length) and The occurrence of immature females, lacking most mensural characters overlap. They may dif- copulatory caps, further indicates that P. macro- fer in the number of longitudinal rows of hooks cephalus may be an atypical host for B. capita- but there are conflicting data for this attribute tum. Typically, in early infections of other poly- with respect to B. physeteris (original description: morphids (e.g., Corynosoma spp.), the sex ratio 18-20 rows of 6-8 hooks [Deliamure, 1955; also is close to 1:1 and males are rapidly passed from in Yamaguti, 1963], 18-20 of 6-8 or 20-24 of the host following copulation (Van Cleave, 1953; 7-8 [Petrochenko, 1958], 20-24 of 7-8 [Skrjabin, Valtonen and Helle, 1982; Adams, 1988). 1970]). Relatively few characters exist to distin- There is only a single, wide-ranging stock of

Copyright © 2011, The Helminthological Society of Washington OF WASHINGTON, VOLUME 60, NUMBER 2, JULY 1993 209 sperm whales recognized in the North Atlantic Literature Cited (Mitchell, 1975), with males usually found at lat- Adams, A. M. 1988. Taxonomy, systematics and itudes above 40°S and 45°N, either singly or in ecology of helminth parasites of the ringed seal, small bachelor pods (Reeves et al., 1986; Rice, Phoca hispida Schreber, in Alaskan waters. Ph.D. 1989). Generally highly pelagic and found over Dissertation, University of Washington, Seattle. 203 pp. deep water, they regularly occur in areas less than Amin, O. M. 1985. Classification. Pages 27-72 in D. 200 m in depth on the Scotian Shelf (Whitehead W. T. Crompton and B. B. Nickol, eds. Biology et al., 1992), but in the shallow region of the Gulf of the Acanthocephala. Cambridge University of St. Lawrence (100 m or less, except for the Press, Cambridge. Laurentian Channel) they appear relatively un- Baylis, H. A. 1929. Parasitic Nematoda and Acan- thocephala collected in 1925-1927. Discovery Re- common (other strandings of P. macrocephalus ports 1:541-560. involved a whale on the northern shore of Prince . 1932. A list of worms parasitic in Cetacea. Edward Island in December 1988 and 3 whales Discovery Reports 6:393-418. in December 1991 [Daoust, pers. obs.]). Thus, it Best, P. B., P. A. S. Canham, and N. Macleod. 1984. is likely that the mass stranding at Covehead Patterns of reproduction in sperm whales, Physeter macrocephalus. Report of the International Whal- Harbor involved a bachelor group that included ing Commission Special Issue 6:51-79. at least some adults. Buron, I., and Y. J. Golvan. 1986. Les holes des Life cycles for species of Bolbosoma are con- acanlhocephales I. Les holes intermediaries. An- sidered to involve pelagic marine zooplankton nales Parasilologie Humaine el Comparee 61:581- (euphausiids and copepods) as intermediate hosts 592. and a taxonomically broad array of fishes as par- Cowan, D. F. 1967. Helminlh parasites of Ihe pilot whale Globicephala melaena (Traill 1809). Journal atenic hosts (Buron and Golvan, 1986; Ed- of Parasitology 53:166-167. monds, 1987; reviewed in Measures, 1992). Dailey, M. D., and R. L. Brownell, Jr. 1972. A check- Among male sperm whales, demersal fishes such lisl of marine mammal parasites. Pages 544-561 as gadids and scorpaenids (known paratenic hosts in S. H. Ridgway, ed. Mammals of Ihe Sea: Biology for species of Bolbosoma) are a frequent but in- and Medicine. Charles Thomas, Springfield, Illi- nois. substantial component of the diet (Rice, 1989). , and W. K. Vogelbein. 1991. Parasite fauna Additionally, monkfish (Lophius americanus of Ihree species of anlarclic whales wilh reference Valenciennes) (Lophiidae), a demersal predator lo Iheir use as polenlial slock indicators. Fishery in the western North Atlantic and the Gulf of St. Bullelin 89:355-365. Lawrence (Leim and Scott, 1966), has been found Deliamure, S. L. 1955. Helminlhofauna of Marine Mammals (Ecology and Phylogeny). Akademiia commonly in the stomach contents of sperm Nauk SSSR, Gel'minlologicheskaya Laboraloriia, whales off Nova Scotia (Mullins et al., 1988). Moscow. (English Iranslalion, Israel Program for The wide range of piscine prey (including gadids, Scienlific Translalions, Jerusalem, 1968). 522 pp. scorpaenids, cottids, osmerids, and others) and Edmonds, S. J. 1957. Auslralian Acanlhocephala 10. Transaclions of Ihe Royal Sociely of Soulh Aus- invertebrates exploited by monkfish indicate its tralia 80:76-80. potential as a paratenic host. Thus, the occa- . 1987. A note on Ihe occurrence of Bolbosoma sional exploitation of marine fishes could ac- capitatum from a false killer whale slranded on count for sporadic infections by species of Bol- Ihe coasl of western Auslralia. Records Wesl Aus- bosoma in sperm whales. Although mesopelagic lralian Museum 13:317-318. Hamilton, J. E. 1916. Biological problems incidental squids of medium to large size are the primary lo Ihe Belmullet Whaling Slalion. Pages 124-146 prey of sperm whales throughout the world (Rice, in Reports of Ihe Brilish Associalion, London. 1989), they apparently have not been implicated Hochberg, F. G. 1990. Diseases of Mollusca: Cepha- in transmission of these acanthocephalans lopoda, diseases caused by prolislans and mela- (Hochberg, 1990). zoans. Pages 47-202 in O. Kinne, ed. Diseases of Marine Animals. Vol. 3. Biologische Anslall Hel- goland, Hamburg, Germany. Acknowledgments Leim, A. H., and W. B. Scott. 1966. Fishes of Ihe The cooperation of Friend Herring, Prince Ed- Allanlic coasl of Canada. Bullelin 155. Fisheries ward Island Department of Fisheries, was essen- Research Board of Canada. Queens Printer, Ol- tial in obtaining access to the 2 sperm whales. lawa. 485 pp. Linstow, O. von. 1880. Helminlhologische Unler- The authors thank A. M. Adams and L. S. Mans- suchungen. Archiv fur Nalurgeschichle 46:41-54. field for providing helpful comments in review- Machado Filho, D. A. 1964. Conlribuicao para o ing an early version of the manuscript. conhecimenlo do genero "Bolbosoma" Porta, 1908

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