Abstract

Few reports of commensal or parasitic protozoa in marine mammals exist. However, consideration of the wealth of protozoans infecting terrestrial mammals strongly suggests that marine mammals should also be infected by a diversity of protozoa, and this possibility is further supported by the diversity of symbiotic protozoa that are known from other marine hosts. Thus, the apparent paucity of protozoa in cetaceans is not necessarily an indication of the rarity of their occurrence, but rather of the rarity of reporting; the latter reflects the challenges of working with small and delicate organisms infecting large hosts typically living in relatively inaccessible environments. However, when suitable protozoan material from cetaceans is available, it is very amenable to examination by a wide range of standard protozoological techniques, which can yield valuable information about identification of the protozoa, providing useful insight into their possible life cycles and clinical significance.

Woodcock and Lodge⁷ published the first accounts of ciliates in cetaceans when they described an ectoparasite, Haematophagus megapterae, attached to the baleen plates of humpback whales (Megaptera novaeangliae). It was later described from two other species of mysticetes². Woodward et al.⁶ reported the first internal parasitic ciliate from nasal swabs of bottlenose dolphins (Tursiops truncatus) captured off the northeast coast of Florida. This spindle-shaped organism was associated with pulmonary parenchymal inflammation. Howard et al.³ described an unidentified oval ciliate in the skin lesion of a bottlenose dolphin from Florida and reported an unidentified elongate ciliate in the alveoli of lung of T. truncatus. Subsequently, Dailey1 reported an oval ciliate from the skin of a bottlenose dolphin in Florida that closely resembled that described by Howard et al.³ Recently, Sniezek et al.⁵ isolated a large, spindle-shaped ciliate (fixed, unstained organisms: length =107.7-225.5 mm, width = 29.0-38.⁵ mm) identified as Kyaroikeus cetarius, from the blowholes of live captive bottlenose dolphins from Florida and from nasal orifices of dead hosts stranded at Virginia Beach, Virginia, and confirmed the presence of this ciliate in killer whales (Orca orca), false killer whales (Pseudorca crassidens), and beluga whales (Delphinapterus leucas) held in captivity in Florida. In gross morphology this organism closes resembles the ciliate previously described by Woodward et al.⁶

We report here on the detection of the ciliated protozoan, Kyaroikeus cetarius, in the respiratory tract of apparently healthy bottlenose dolphins held at the Space and Naval Warfare Systems Center San Diego facility at San Diego Bay. The organism is frequently collected by introducing a swab into the spiracular cavity, vestibular sac(s), or nasal passage(s) of the dolphins during routine physical examination. Light microscopic examination of mucus samples revealed large numbers of the spindle-shaped, holotrichously ciliated organism, moving freely and actively. To further determine the identity of the ciliates, fresh material was preserved in Bouins fixative and then stained by protargol (silver protein) impregnation in order to reveal the rows of ciliature (kineties), and macro- and micronucleus⁴. Stained ciliates had features consistent with Kyaroikeus cetarius as first described by Sniezek et al.⁵, namely a broad terminal podite (conical foot-like appendage); deep oral cavity containing a preoral kinety, two circumoral kineties, and cytostome (cell mouth); a prominent cytopharynx (cell "throat"); somatic kinetome with both right and left ciliary fields; and a heteromeric (not uniformly staining) nucleus. In addition, these ciliates were comparable in size to K. cetarius as previously described⁵.

An organism similar to Kyaroikeus sp. also infected the lymph nodes of a geriatric male bottlenose dolphin that was maintained at the San Diego facility since August of 1993. The animal had been transferred from the Hawaii facilities where it had been treated several times for reduced or erratic appetite and weight loss. After arrival in San Diego, the dolphin experienced several episodes of weight loss, poor healing of superficial lacerations and erratic appetite. At each episode the dolphin was treated with systemic antimicrobials and supportive care, recovering to normal clinical status. Beginning in April of 1996, the animal's condition began to deteriorate, and euthanasia was elected in July of 1996. Primary problems identified by clinical pathology included refractory hypernatremia, hyperchloremia, and azotemia, marked leukocytosis progressing to a pronounced left shift, developing delayed healing and multiple bulbous eruptive lesions along the fluke insertion and fluke blades progressing to necrotic open wounds. The primary cause of death was bronchointerstitial pneumonia. However, among several other pathological findings, lymphadenitis with intralesional ciliated protozoa was reported. Protozoa associated with focal dermal abscessation and ulceration were also noted. The ciliated protozoan, Kyaroikeus cetarius has been previously reported from both the skin and the upper respiratory tract of odonticete cetacea⁵. In dermal lesions, it is unclear whether this ciliate is the primary cause of dermatitis or is an opportunistic invader. However, it has been suggested as the cause of irritation and pulmonary inflammation⁶.

We believe this to be the first confirmed report of Kyaroikeus cetarius from a cetacean from the Pacific Coast of the United States; K. cetarius has previously been reported from both stranded and captive cetaceans from the Atlantic Coast of the USA. Additionally, identification of ciliates in the somatic lymph nodes (tentatively identified as Kyaroikeus sp.) is a rare finding and one of potential clinical significance. We believe that the greatly weakened condition of the animal, particularly the bronchointerstitial pneumonia, allowed the ciliates to migrate through the compromised tissues, from the respiratory tract, through the lungs and ultimately to the lymph nodes. This possible mechanism of infection is supported by a previous report of unidentified ciliates from the alveoli of a T. truncatus with pneumonia³. Moreover, one case of ciliate lymphadenitis and one case of bronchopneumonia with rare intrabronchiolar ciliates have been described from dolphins that died during the 1987-88 Atlantic bottlenose dolphin morbillivirus epizootic (T.P. Lipscomb, personal communication). Routine isolation of the ciliated protozoan from healthy captive bottlenose dolphins in California suggest that Kyaroikeus cetarius is a normal constituent of the flora of the upper respiratory tract of animals, but when their health is compromised, the ciliates can become endoparasites, migrating to other tissues.

Acknowledgements

Dr. D. Wayne Coats (Smithsonian Environmental Research Center, Edgewater, MD) graciously assisted with specimen identification.

References

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