DISEASES OF AQUATIC ORGANISMS Published April 3 Dis Aquat Org

Macroparasites in cetaceans stranded on the northwestern Spanish Atlantic coast

E. ~bollol, A. ~opez2, C. ~estall, P. ~enavente~,S. Pascual 'P*

'Laboratorio de Parasitologia, Facultad de Ciencias del Mar, Universidad de Vigo, Apdo. 874, E-36200 Vigo, Spain 'c.E.M.MA. Anxeriz, 19, SOD. Milladoiro, E-15895 Ames, A Coruna, Spain 3C.E.S. Apto. 100, 0 Grove. E-36980 Pontevedra, Spain

ABSTRACT: An extensive parasitological survey was carried out during autopsy of 80 cetaceans representing 8 species within 4 families (Delphinus delphis, Stenella coeruleoalba, Tursiops truncatus, Grampus griseus, Globicephala melas, Kogia breviceps, Phocoena phocoena and Megaptera novaean - glide) collected on the northwestern Spanish Atlantic coast from February 1991 to October 1996. Two species of tetraphyllidean cestodes (Phyllobothnum delphjni and Monorygnla grimaldii), 2 ascaridoid (Anisakis simplex and A. physeteris), a single spirurid (Crassicauda magna), 4 rhabditidiform nematodes (Halocercus delphini, H. invaginatus, Halocercus spp. and Stenurus glob)- cephalae), a single polymorphynae acanthocephalan (Bolboson~asp.), and 2 amphipods (Isocyamus delphini and Cyamus boopis) were found. This paper presents 6 new geographic records of macro- parasites from cetaceans in temperate Atlanto-Iber~anwaters. A total of 11 component parasite spec~es were found, mainly parasitizing the blubber, mesentery and stomach of cetaceans. Cetaceans har- boured a suite of 4 generalist and 8 specialist species.

KEYWORDS: Macroparasites Stranded cetaceans . NW Spain

INTRODUCTION During the period 1990 to 1996, the Galician Co- ordinating Body for the Study of Marine Mammals Several unusual mass mortalities of marine mam- (C.E.M.MA.) compiled a total of 776 references to mals around the world have been linked to environ- marine mammals found stranded or accidentally caught mental deterioration involving bioaccumulation of in the northwestern Spanish Atlantic waters (Lopez pollutants (trace metals and organo-halogenated com- et al. 1996). This data represents 75 % of total stranded pounds) (Wageman & Muir 1984, Tanabe et al. 1994, marine mammals found on 2750 km of the North Iber- Viale 1994, Aguilar et al. 1995) and virus-induced epi- ian Peninsula coast (from the Bidasoa river, French zootics (Geraci et al. 1982, Domingo et al. 1990).A high border, to the Mirio Estuary, Potuguese border). De- intake of xenobiotics could cause, directly or indirectly, spite this, no attention has been given to their parasite- impairment of immune responses to other common fauna composition. pathogens (bacteria, fungi and parasites), causing Although the Galician coast is probably an important severe intercurrent disease outbreaks in wild popula- area for cetacean strandings, comparative data on par- tions. Nevertheless, in many instances it has been asitic disease prevalence has not been reported. This difficult to establish the link between morbidity and study provides the first information on host-parasite mortality of individuals and populations and exposure data for marine mammals off the NW Iberian Peninsula to parasites (Geraci & St. Aubin 1987). coast. This paper thus provides new data for monitor- ing transfers and bioaccumulation of parasites in wild marine organisms and for studying the adjustment of 'Addressee for correspondence. heteroxenous parasite life-cycles to the Galician food E-mail: [email protected] web.

O Inter-Research 1998 Resale of full article not permitted 228 Dis Aquat Org 32: 227-231. 1998

MATERIALS AND METHODS

During the period February 1991 to Octo- ber 1996, a total of 80 toothed and baleen ICES division IXa whale specimens (Table 1) which were stranded on the shores of the Galician coa.st (NW Spain), either floating in the water or entangled in fishing nets, were systemati- cally surveyed for ectoparasites or epizoics and endoparasites. Cetaceans were sampled at 6 localities (Fig. 1). Sex and standard body length (BL, to the nearest cm) of each host were recorded in the field. When possible, ani- mals were taken to the laboratory and weighed (total body weight, BW, to the nearest kg). The investigation was restricted to the macroparasite (platyhelminths, nematodes, acanthocephalans and crustaceans) fauna of cetaceans according to Rohde (1993). Blubber layer, mesenteries, kidneys and air sinuses were examined during necropsy in the field. Digestive systems and lungs were Fig. 1. Sampling subareas on the shores of Galicia, Spain collected and immediately frozen. The in- testines, stomach compartments, bile and pancreatic stricted in distribution to their host cetacean species. ducts, bronchi and bronchioles were split open and Generalists are species that are regularly found in examined and processed by parasitological tech- several genera or families of cetaceans (Kennedy niques, according to the recommendations by Borg- 1995). Ecological terms referring to the parasites follow steede (1991). Margolis et al. (1982) and Bush et al. (1997). Based on Species were assigned to the categories of specialist prevalence values, parasitic metazoa were also classi- or generalist. Specialists were defined as species re- fied into component (p > 10%) and secondary species

Table 1. Host species, sampling date and reference codes for hosts and sampling locations. The number of host individuals (N), standard body length (BL:mean * SD) and total body weight (BW:mean +SD) are also provided : no data

Host Host Area Sampling N BL BW species reference reference date code code (cm) (kg)

Delphinus delphis DD 1 1 V, V Jan 1991-0ct 1996 50 189.5 i 21 6 74.3 2 28.9 (common dolphin) (135-230) (36.3 - 150) Stenella coeruleoalba SC 111. V, V1 Dec 1992-Sep 1996 t 194.3 * 31.1 - (striped dolphin) (154-225) Tursiops fruncatus TT 11, 111, IV, V Nov 1992-0ct 1996 10 279.5 i 25.7 (bottle-nosed dolphin) (240-310) Grampus grjseus GG 111, V1 Dec 1994-Ju1 1996 299.5 * 7 8 (Risso's dolphin) (294-305) Globicephala rnelas GM I, V1 Apr 1993-Dec 1995 384.2 A 82.2 (long-finned pilot whale) (286-469)

Kog~abreviceps KB I1 Oct 1995 L 258 (pigmy sperm whale) Phocoena phocoena PP IV, V1 Nov 1992-Dec 1994 4 182.7 * 16.1 (harbour ) (168-202) Megaptera novaeangliae MN 111 Mar 1993 l 4 90 (humpback whale) Abollo et al.: Macroparasites in cetaceans 229

(10"/0 2 p 1 l%)(Bush et al. 1990).Frequency distribu- 54.2 % in other Delphinidae and 71.4 O/oin other ceta- tions of parasitized organs were calculated within and ceans) with a mean of 1.2 parasitic species (range: 1 to between host groups. Representative specimens of 3) per host. Nematodes comprised 61.5%1of the total each parasite species have been deposited in the parasitic sample. The sibling species complex Anisakis Department of Parasitology at the University of Vigo simplex (Nascetti et al. 1986) was the most frequent (Spain). nematode, comprising 12.5% of all nematode species.

Table 2. Taxonomic information, host and site location, and prevalence (P) RESULTS of infestation of the macroparasites found in cetaceans from NW Spain. Host-reference codes defined in Table 1. Sites: as, air sinuses; bb, blubber; The taxonomic and systematic studies have lu, lungs; mm, mesentery; na, neck area; oe, oesophagous; ph, pharynx; enabled the identification of 12 metazoan sk, skin: st, stomach endo- or ectoparasitic species (Table 2). Larval phylobothriid worms were the most Parasite Host Site P (X) common tissue parasites found in cetaceans. Cestoda (tapeworms) Host range varied from 6 (Phyllobothrium Phyllobothriidae delphini) to 4 odontocetes (Monorygma gri- Phyllobothriurn delphinid DDC bb 70 (Bosc, 1802) (plerocercoid) SCc bb 87.5 maldii). A total of 14.4 (range: 1 to 47) indi- TT' bb 50 viduals of P. delphini were usually found in GG' bb 50 the subcutaneous fat (mainly in the urogeni- GM' bb 25 tal zone), which comprised 18.2 to 33.6% of KBc bb 100 Monorygmagrimaldii" DDc mm 4 2 the infested organs (Fig. 2). Cysts of M. gri- (Moniez, 1889) (plerocercoid) SC' mm 7 5 maldii were found singly or in groups with TTC mm 50 13.5 (range: 2 to 32) cysts on the outer sur- KB' mm 100 faces of mesentery membranes in the body Nernatoda (roundworms) cavity (26.7 to 27% of the infested organs). Anisakidae Anisakis simplex" (Rudolphi, 1809) DDr st 64 Nematodes of the family infested (larvae and adults) SCC st 37.5 lungs and air sinuses of the Delphinidae. All TTc ph, oe, st 60 nematodes found in the pharynx, oesophagus GMr st 75 and stomach belonged to the Anisakidae. KBc ph, oe, st 100 PPC st 75 Within the genus Anisakis (Dujardin 1845), Anisak~sphyseter~s KBc ph, oe, st 100 2 common species were found: A. simplex (Bayl~s,1923) (larvae and adults) (which had the highest prevalence) and A. Crassicaudidae physeteris; these parasitized 6 and 1 host Crassicaudamagna KB C." na 100 species, respectively. A single species of cras- (Dollfus, 1966) (adult) sicaudid nematode (Crassicauda magna) was Pseudahldae Halocercus delphinia DD'.~ lu 18 found infesting the musculature in the neck (Baylis & Daubney. 1925) (adults) TTe lu 10 area of Kogia breviceps. Among the crusta- Halocercus invaginatus" PP' lu 25 cean species, 2 amphipods, Isocyamus del- (Quekett, 1841) (adults) phini and Cyamus boopis, were identified in Halocercus ~pp.~ natural openings and wounds of the skin, (Baylis & Daubney. 1925) (adults) sCc-" lu 25 mainly parasitizing the genital slit of the Stenurus globicephalae" GMC as 50 (Baylis & Daubney. 1925) (adults) Risso's dolphin and humpback whale, respec- Acanthocephala (thorny-headed worms) tively. Polymorphidae Two common dolphins were free of para- Bolbosorna ~p.~ 1 sitic metazoa, while 97.5 % of cetaceans were (Porta, 1908) (adults) infested with 1 to 4 parasite species (mean Crustacea (whale-lice) 2.04 to 2.2 in Delphinidae and 1.67 for other Cyarmdae Isocyarnus delphini 50 cetaceans). Sixty-eight percent of the ceta- (Guerin-Meneville. 1837) (adults) ceans were infested with cestodes (74% in Cyarnus boopis 50 Delphinus delphis, 66.7 % in other Del- (Liitken, 1870) (larvae and adults) phinidae and 28.6% in other cetaceans). This aGeneralist species; bspecialist species; Ccomponent species; "first comprised 15.4 % of all parasitic metazoan record of this parasite on this host in temperate water of the NE parasites. Nematode infestations occurred in Atlantic Ocean; esecondary species 65.4 % of the cetaceans (70% in D. delphis, 230 Dis Aquat Org 32: 227-231, 1998

FREQUENCY (%) on appropriate intermediate hosts) (Kennedy et al. 3.5, 1986, Balbuena & Raga 1993) are likely. A comparison of common dolphin and other Del- phinidae parasite-faunas indicated that their respec- tive parasite component communities were, to some extent, similar (67%) with a high overlap of parasitic metazoan species. In Galician waters, available data suggests that dolphins are primarily fish-eaters (mostly blue-whiting Micromesistius poutassou) which take prey they encounter rather than selecting particular prey items (Gonzalez et al. 1994). Similarity in trophic specialization of small cetaceans in the sampling area may lead to their helminthofauna similarity. Major dif- ferences in patterns of community richness and less SITE ,m parasite-fauna similarity were found between dolphins W and other cetaceans, which probably shows the inter- Fig. 2. Frequency distribution of parasitized organs in ceta- acting influence of host ecology and host evolution in ceans from NW Spaln. S~tes:sk, skin; bb, blubber; mm, determining community richness, as previously pro- mesentery; na, neck area; ph, pharynx; oe, oesophagous; st, posed for other cetacean species (Balbuena & Raga stomach; lu, lungs; as, air sinuses. DD: Delphinus delphis; 1993, Aznar et al. 1994). OD: other Delphinidae; OC: other cetaceans

Acknowledgements. The authors are very grateful to many Acanthocephalan infestations occurred in 3.7% of people who reported stranded and those who helped the cetaceans, comprising 7.7 % of the total parasitic by storing or transporting specimens, particularly the staff of sample. Cyamids of the species Isocyamus delphini the C.E.M.MA. Thanks are also due to Xunta de Galicia for financial support under Project XUGA301 lOA97. and Cyarnus boopis occurred in 2 (2.5%) cetacean individuals. Prevalences varied from 0% in D. delphis to 4.2 % in other Delphinidae and to 14.3 % in the other LITERATURE CITED cetaceans. Nematoda was clearly the most prevalent Aguilar A, Borell A, Pastor T (1995) Factors affecting vari- taxonomic group: 7 species within the Anisakidae, ability of persistent pollutants levels in cetaceans. Bergen, Crassicaudidae and Pseudaliidae were found in both 27-29 March 1995. Working paper. SC/M95/P6 cetacean suborders. Aznar FJ, Balbuena JA, Raga JA (1994) Helminth communi- ties of Pontopona blainvillei (: Pontoporiidae) in Argentinian waters. Can J Zoo1 72:702-706 Balbuena JA, Raga JA (1993)Intestinal helminth commun~ties DISCUSSION of the long-finned pilot whale (Globicephala melas) off the Faroe Islands Parasitol 106:327-333 Many of the parasites recovered in this study have Borgsteede F (1991) Parasitological examination. In: Kuiken been reported previously. However, the nematodes T,Garcia Hartmann M (eds] Proceedings of the first ECS Crassicauda magna, Halocercus delphini, and Halo- workshop on cetacean pathology: dissection techniques and tissue sampling. European Cetacean Society News- cercus spp., the acanthocephalan of the genus Bolbo- letter No. 17, Special issue. Leiden, p 11-16 soma and the cyamids Isocyamus delphini and Cya- Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasito- mus boopis are reported for the first time from 5 logy meets ecology on its own terms. Margolis et al. revis- cetacean species from temperate waters off the north- ited. J Parasitol 83:575-583 Bush AO, Aho JM. Kennedy CR (1990) Ecological versus phy- ea4tern Atlantic coast. logenetic determinants of helminth parasite community Parasites species richness is well within the ranges richness. Evol Ecol 4:1-20 given for endothermic vertebrates (Kennedy et al. Domingo JV, Ferrer L, Pumarola M, Marco A. Plana J, 1986, Pence 1990). Cetaceans harboured the same Kennedy S. McALiskey M, Rima BK (1990) Morbilhvirus number of component helminth parasite species as in dolphins. Nature 336:21 Geraci JR, St. Aubin DJ (1987) Effects of parasites on marine those found by Bush et al. (1990) in an analysis of pat- mammals. Int J Parasitol 17:407-414 terns of community richness among parasitic helminth Geraci JR, St. Aubin DJ, Barker IK,Webster RG, Hinshaw VS, communities in aquatic mammals. The common dol- Bean WJ, Ruhnke HL, Prescott JH. Early G, Baker SS, phin harbours a similar number of parasite species, as Madoff S, Schooley RT (1982) Mass mortality of harbour seals: pneumonia associated with influenza A virus do other Delphinidae, since no marked differences in Science 215:1129-1131 host factors (complexity of the digestive tract, vagility, Gonzalez AF, Lopez A, Guerra A, Barreiro A (1994) Diets of diet complexity, selective versus-non selective feeding marine mammals on the northwestern Spanish Atlantic Abollo et al.: Macroparasites in cetaceans 23 1

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Editorial responsibility: iMurray Dailey, Submitted: May 23, 1997; Accepted: December 12, 1997 Gunnison, Colorado, USA Proofs received from authorls): February 26, 1998