A New Flagellate Protozoan Living as a Commensal or Opportunist in the Blow Hole of a Stranded Pygmy Sperm Whale (Kogia breviceps)
IAAAM Archive
Sarah L. Poynton1,2; Brent Whitaker1; James H. Sniezek3
1Animal Health, National Aquarium in Baltimore, Baltimore, MD; 2Marine Pathology Group, Department of Fisheries Biology, Institute fur Meereskunde an der Universitat Kiel, Kiel, Germany; 3Smithsonian Environmental Research Center, Edgewater, MD

Introduction

Pygmy sperm whales, Kogia breviceps (Physeter idae) have a wide geographical range in the warmer waters of the world, where they live beyond the edge of the continental shelf, usually individually, or in small schools of up to six animals. Much of our knowledge of them comes from individuals that are taken in fisheries, or that strand.

Although numerous helminths and crustaceans have frequently been reported from cetaceans, including Kogia spp., very little is known of protozoan infections (Dailey 1985). To the best of our knowledge, reports are confined to ciliates from the blow hole and skin of dolphins (Woodard et al., 1969, Sniezek et al., in press, and Howard et al, 1983 respectively), and the apicomplexan Sarcocystis from muscles of dolphins and whales (Cowan, 1966, Dailey & Stroud, 1978; Owen Kakulas, 1967).

The paucity of information on protozoan infections in cetaceans can be attributed to the following: cetaceans are not readily accessible in the wild, most stranded animal are dead or in poor condition, protozoa are delicate and do not survive long after the host has died, infections may not be grossly visible, and specialized knowledge and facilities for studying protozoa may not be available at the stranding site.

However, between November 1993 and May 1994, a stranded juvenile pygmy sperm whale was successfully rehabilitated at the National Aquarium in Baltimore. During this time, intensive medical care and effort afforded us a unique opportunity to study aspects of her biology, including observing flagellates in her blowhole.

Materials and Methods

The juvenile female whale stranded in New Jersey in November 1993 and was transported to the National Aquarium in Baltimore, where she remained for care until her rehabilitation and release of l the coast of Florida in May 1994. Although she was in poor condition on arrival at the National Aquarium, she was successfully treated for dehydration, bacterial pneumonia, and gastroenteritis. Following the removal of plastic from her stomach using endoscopy, she made a full recovery.

Routine health monitoring included the periodic collection of blood and blow hole samples. The latter were collected when the whale was out of the water for a physical examination or transport. Mucus from the respiratory tract was collected in a clean plastic petri dish, held approximately 6 ems above the blow hole, when the whale exhaled. Five to eight exhalations together yielded enough material for examination (care was taken to prevent the sample from drying out). The fresh material was examined microscopically, and then two different types of stained preparations were made. Some samples were fixed in Bouins fixative and stained with silver protein (protargol) to demonstrate the flagella and nuclear membranes. The protargol staining procedure followed the filter method of Lynn ( 1992) and Montagnes & Lynn (1987). Other samples were air dried, fixed in methanol and stained by Wrights Giemsa.

Results

Flagellates were routinely detected in fresh wet mounts of mucus, immediately after the whales' arrival in Baltimore, throughout the rehabilitation period, and until release. The flagellates were elongate, with an undulating membrane, and one anterior flagellum and one posterior flagellum. They moved very actively through the mucus. Flagellates were frequently associated with epithelial cells in the mucus, and were attached to clumps of epithelial cells by one of their two flagella. We have tentatively identified these flagellates as belonging to the flagellate Order Kinetoplastida.

Discussion

Although kinetoplastids have not been previously reported from cetaceans, flagellates with similar relationships to their hosts are known from fishes. Members of the genus cryptobia with two unequal flagella and sometimes also with a narrow undulating membrane, occur as both endo zoic and ectozoic commensals of invertebrates and fish (Lom & Dykova, 1992). Those species that are ectozoic are transmitted by direct contact. Although the life cycle of endo zoic species is not known, it is known that they can be regurgitated, and can survive in the water for up to 72 hours, (presumably then to be swallowed again). Our knowledge of kinetoplastids from fishes thus suggests that the flagellates from the pygmy sperm whales could be transmitted to other whales directly, i.e. a vector may not be needed. We suggest that transmission could take place between the mother and the calves, and when these usually solitary animal gather in schools.

The attachment of the flagellates to the epithelial cells in the blow hole mucus, is also reminiscent of the attachment of c. brancizialis (a species from the gills of many species of fish). The C .branchialis flagellates adhere to the substratum with their recurrent flagellum while feeding on bacteria and detritus particles According to Lom (198()), there is no evidence of any pathogenic action of crypto bias, and the adherence of the recurrent flagellum inflicts no damage to the hosts epithelial cells.

The presence of the epithelial cells in the blow and the attachment of the flagellates to them, suggest that the protozoa inhabit the upper respiratory tract of the whale, such as the trachea, rather than the lower parenhymous tissue or the sinuses. The continuous presence of the flagellates, even when the whale returned to good health, suggest to us that they are probably normal components of the fauna of the whale, and are harmless commensals.

It is also possible, though we believe less likely, that the flagellate from the pygmy sperm whale is an opportunistic symbiont, the infection perhaps having been acquired from fish or squid, the latter being the whales primary food. As mentioned above, Cryptobiu spp. have been reported from fish, and several ectoparasitic flagellates, tentatively identified as members of the blastidinid and bodonid groups, can infect octopus (Hochberg, 1990).

We would like to encourage other aquatic animal health specialists to examine the mucus from the blow hole of cetaceans, to determine which protozoa arc present. In this way we can build up host symbiont-geographic distribution records, and thus better understand the relationships between the leg plates and their hosts.

Acknowledgements

We extend our sincere thanks to the Marine Animal Rescue Program at the National Aquarium in Baltimore, and to the dedicated team of staff and volunteers who made it possible for us to work with this whale. In particular we would like to thank David Schofield, Christine Steinert, Jill Arnold, Jenni Jenkins, Jennifer Fasick and Or. Andrew Stamper for their conscientious and enthusiastic observations of the whale and her flagellates.

References

1.  Cowan, D.F. 1966 Pathology of the pilot whale. Arch.Path. 82: 178 - 189.

2.  Dailey, M.D. 19X5. Disease of Mammalia: Cetacea. In Kinne, O. (ed.) Disease of Marine Animals. Vol. IV, Part 2, Introduction, Reptilia, Aves, Mammalia. Biologische Anstalt Helgoland, Hamburg. pp. 8()5 - 847.

3.  Dailey, M.D. & Stroud, R.K. 1978. Parasites and associated pathology observed in cetaceans stranded along the Oregon coast. Journal of Wildlife Diseases 14: 503 - 511.

4.  Hochberg, F.G. 1900. Diseases of Mollusca: Cephalopoda. 1.2. Diseases caused by Protistans and Metazoans. In Kinne, O. (ed.) Diseases of Marine Animals, Vol III, Biologische Anstalt Helgoland. pp. 47 - 202.

5.  Howard, E.B., Britt, J.O.,Matsumoto, G.K., Itahara, R., & Nagano, C.N. 1983. Bacterial Diseases. In Howard, E.B. (ed.). Pathobiology of Marine Mammal Diseases. Vol. I. CRC Press, Boca Raton Florida, pp. 70 - 117.

6.  Lom, J. 1980. Cryptobia branchialis Nie from fish gills: ultrastructural evidence of ectocommensal function. Journal of Fish Diseases 3: 427 - 436.

7.  Lom,J. & Dykova, I. 1992. Protozoan Parasites of Fishes. Developments in Aquaculture and Fisheries Scienee 26. Elsevier Press.

8.  Lynn, D.H. 1992. Protargol staining. In Lee, J.J.and Saldo, A.T. Protocols in Protozoology, Society of Protozoologists, Lawrence, Kansas, C4.1 - C4.8.

9.  Montagnes , D .J. S . & Lynn, D. H. 1 987 . A quantitative protargol stain (QPS) for ciliates : method description and test of its quantitative nature. Marine Microbial Food Webs 2: 83 - 93.

10. Owen, C.C. & Kakulas,R.A. 1967. Sarcosporidiosis in the sperm whale. Australian Journal Science 31: 46 - 47.

11. Sniezek, J.H., Small, E.B. & Coats, D.W. in press. Kyariokeus cetis N.G., N.Sp.: a holotrichously ciliated phyllopharyngian associated with odonticete cetaceans. Journal of Eukaryotic Microbiology.

12. Woodard, J.C., Zam, S.G., Caldwell, D.K. & Caldwell, M.C.1969. Some parasites of dolphins. Path Vet6 257-272.

Speaker Information
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Sarah L. Poynton, BSc, PhD
Division of Comparative Medicine
Johns Hopkins University School of Medicine
Baltimore, MD, USA


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