GRAY WHALE BARNACLES CRYPTOLEPAS RHACHIANECTI INFEST WHITE WHALES, DELPHINAPTERUS LEUCAS, HOUSED IN SAN DIEGO BAY
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1 BULLETIN OF MARINE SCIENCE, 61(2): , 1997 GRAY WHALE BARNACLES CRYPTOLEPAS RHACHIANECTI INFEST WHITE WHALES, DELPHINAPTERUS LEUCAS, HOUSED IN SAN DIEGO BAY Sam H. Ridgway, Elek Lindner, Kerry A. Mahoney and William A. Newman ABSTRACT A whale barnacle, Cryptolepas rhachianecti (Dall), previously considered an obligate commensal for the gray whale, Eschrichtius robustus (Lilljeborg), infested white whales, Delphinapterus leucas (Pallas), housed in San Diego Bay. The infestation occurred annually between January and April in concert with the northward migration of the gray whale, and did not occur during years when the white whales were housed elsewhere during these months. Although initial infestation elicited no apparent skin response, after successive years of exposure, massive cellular proliferation in the adjacent epidermis resulted in ejection of barnacles from the whales within a few weeks. This increasing epidermal response and the invasion of inflammatory cells at the juncture of skin and barnacle shell is suggestive of an immune reaction to the barnacles. Barnacles are marine crustaceans that attach to a variety of inanimate and animate objects including the skin of whales. Although whale barnacles are often referred to as parasites, they strain food from the sea and, other than to increase drag, are generally thought not to adversely affect their cetacean hosts (Slijper, 1962). The life cycle of a barnacle begins with a series of six free-swimming planktonic stages progressing to a molt into a cyprid which seeks a place for permanent settlement. In the case of Cryptolepas rhachianecti (Dall), the site of attachment is the skin of the gray whale, Eschrichtius robustus (Lilljeborg), for which it is generally considered to be host-specific (Newman and Ross, 1976; Newman and Abbott, 1980; Wolman, 1985; Scarff, 1986). Observations of C. rhachianecti suggest that they spawn on the whales winter grounds following the southern breeding migration. No small (newly attached) barnacles are found on southbound whales as they pass by San Francisco; however, all northbound whales carry numerous small barnacles (Rice and Wolman, 1971). Therefore, attachment must occur in the warmer waters of the breeding grounds and/or during their return north. Although other barnacles are found on other whale species, there are no published reports of barnacles occurring on beluga or white whales, Delphinapterus leucas, (Pallas). MATERIALS AND METHODS At various times between 1977 and 1980, two male and two female white whales taken off Churchill, Canada, were brought to live in netted ocean enclosures at the mouth of San Diego Bay (Fig. 1) at the Naval Command Control and Ocean Surveillance System (NCCOSC), RDT&E DIV. The males were identified as NOC and CHU; the females as MUK and RUB. Over the next 8 yrs, some were also kept in land-based pools in San Diego, and/or in netted ocean enclosures in Kaneohe Bay, ; Puget Sound, Washington; or Vancouver Island, Canada (Table 1). 377
2 378 BULLETIN OF MARINE SCIENCE, 61(2): , 1997 Figure 1. Three of the four white whales (Delphinapterus leucas) in this study: left to right, MUK, NOC, RUB in the bay pen complex. The entrance to San Diego Bay is about 1 km away in the upper right of this photograph. The water for the land-based pools in San Diego was collected from the Pacific Ocean at a depth of about 20 m and pumped through sand and gravel filters into the pool at a rate sufficient to allow for complete water exchange every 2-4 h. For laboratory examination, excised barnacles were fixed in 70% alcohol. Under a dissecting microscope, the whale epidermis was removed from the barnacle so that it could be identified. Portions of proliferated epidermis containing barnacles were decalcified, processed for histology, and sectioned on a microtome prior to mounting on a glass slide for staining with hematoxylin-eosin. RESULTS In late January, and early February 1978, trainers noticed small dark specks on the skin of the whales. By late February they had grown to about 1 mm in diameter, and appeared over much of the whales body surface. By March cirral-like appendages, were seen protruding from many of the black spots. A few of these dark areas were excised to reveal barnacles with a calcareous shell. Despite the absence of overt signs of inflammation, purulence, or discomfort manifested by the whales, we eliminated most of the barnacles from the whales skin by apply-
3 RIDGWAY ET AL.: GRAY WHALE BARNACLES ON WHITE WHALES 379 Table 1. Location of white whales, NOC, MUK, CHU, and RUB, , and incidences of barnacle infestations. Animal Date Location Barnacles NOC 8/1977 Canada to SD pool 12/1977 Barnacles 1/ /30/79 San Clemente Is., CA 10/1980 Wash. and Canada 1981 Wash. and Canada 3/ / / Reinfested, marked skin response 1987 to 1995 Reinfested each Jan/Mar, marked skin response CHU 8/1977 Canada to SD pool 12/1977 Barnacles 1/ Reinfested, no skin 5/1980 SD pool 5/1981 3/ /1984 2/1985 Reinfested, no (5/95 died) response noted skin response noted MUK 8/1977 Canada to SD pool 12/1977 Barnacles 1/ /30/79 San Clemente Is., CA 10/1980 Wash. and Canada 1981 Wash. and Canada 3/ to 1995 Reinfested each Jan/Mar, marked skin response RUB 7/1980 Canada to SD pool 10/80 Barnacles 1/ to 1995 Reinfested each Jan/Mar, marked skin response
4 380 BULLETIN OF MARINE SCIENCE, 61(2): , 1997 Figure 2. A. Exterior view of shells of three different size barnacles are shown in the upper series. Below these barnacles three comparable ones are displayed with wall plates separated. B. Side views of the shells of two immature barnacles. C. High-magnification basal view of one wall plate cusp showing the complex lace-like pattern by which the shell anchors to the whale skin. D. Highmagnification of the exterior of a wall plate cusp showing the complex arrangement for anchoring to the skin of the whale. ing an ointment containing zinc oxide and copper sulfate. This treatment rapidly stopped cirral movement and killed the barnacle. Treatment was withheld from a few of the barnacles to allow them to grow to a size that would enable us to confirm their identity. In March 1978, a specimen with a 3 mm high and 3 mm diameter shell was removed for examination. The slightly conical shell had no vertical ridges on either of the six compartments and had no calcareous basis, but it was clearly a balanomorph or sessile barnacle. Because the specimen was immature, it lacked some of the characteristics of the coronuline barnacle, Cryptolepas; however, it was tentatively identified as such. For more positive identification, a few barnacles were allowed to grow; periodically some of these specimens were removed for examination. Growth rates of the attached barnacles
5 RIDGWAY ET AL.: GRAY WHALE BARNACLES ON WHITE WHALES 381 Figure 3. A. Ventral body skin of RUB showing barnacles of various sizes from about 2 to 20 mm in diameter. The photograph was taken in early June 1981 during RUB s first year in San Diego Bay. Small scratches, creases, or depressions in the whale skin appeared to be favorite attachment points for barnacles. B. Photograph taken in March 1985 showing the massive skin proliferation around a barnacle. C. Photograph showing a pit remaining in the epidermis after the barnacle was ejected. In most cases, pits filled in and the skin was smooth within about 6 wks.
6 382 BULLETIN OF MARINE SCIENCE, 61(2): , 1997 Figure 4a. A. 40 X photomicrograph of a section through whale skin with embedded barnacle. B. Enlargement (250X) of the area of i and s indicated on A. C. Enlargement (250X) of an area between i-s and b indicated on A. appeared to be in the range of 3 to 4 mm per month. The complexity of the shell (Fig. 2) could be one explanation for the relatively slow growth rate (Hirano and Okushi, 1952). Two more specimens, one 16 mm and one 20 mm were collected from MUK and RUB during the month of June. Although a mature C. rhachianecti may reach 55 mm in diameter, these barnacles were sufficiently large to positively identify them as Cryptolepas rhachianecti (Dall). MUK, NOC, and CHU acquired their first barnacle infestations in 1978; RUB was first infested in During these initial infestations there was no apparent skin response (Fig. 3A); however, with several successive years of exposure, a marked response developed (Fig. 3B). Infestation did not occur during the years when these whales were kept at other locations during the months of January, February, or March - even if the whale was returned to San Diego after these months. In whales that spent successive years in San
7 RIDGWAY ET AL.: GRAY WHALE BARNACLES ON WHITE WHALES 383 Figure 4b. D. 500 X photomicrograph of a section through whale skin with embedded barnacle: b, barnacle tissue; i, layer of inflammatory cells; e, whale epidermis proliferated around barnacle; s, barnacle shell. Diego Bay and were likewise infested, a marked response of the epidermis adjacent to the barnacles was noted which caused the barnacles to be ejected within several weeks of attachment (Fig. 3C). Microscopic examination of stained sections of portions of skin with attached barnacles revealed that there was a massive proliferation of epidermis surrounding the barnacle. Micro-abscesses developed at the juncture between the barnacle shell and the epidermis. Within these micro-abscesses were numerous white blood cells including neutrophils, eosinophils, and lymphocytes (Fig. 4). No scarring was observed on the skin of the whales after shedding the barnacles. This was surprising because when barnacles are removed or shed from E. robustus or Megaptera novaeangliae (Borowski), the remaining pit eventually becomes a tissue scar (Wolman, 1985; Geraci and St. Aubin, 1987). DISCUSSION Whenever white whales were kept in San Diego Bay during the season of the northward migration of the gray whales past San Diego Bay, barnacles appeared on their skin. When whales were in land-based pools in San Diego, or in bay enclosures in or in open ocean enclosures in the Pacific Northwest, their skin remained clear of barnacles. Whales kept in the land-based pools in San Diego during the northward migration of gray whales were not infested by barnacles despite the fact that the pools were filled with sea water pumped from an area closer to the path of the migrating gray whales than the enclosures in the bay. This water source is in a mixed layer during the late fall and winter (Dayton et al., 1992) and passes through sand and gravel filters before it enters the whale pools. It is possible that filtration removed any barnacle larvae that may have been in this water, thus preventing infestation of the whales in the land-based pool.
8 384 BULLETIN OF MARINE SCIENCE, 61(2): , 1997 The southward migration of gray whales passes San Diego as early as the end of November; however, we never saw any sign of barnacles until the middle to end of January, after the northward migration had begun. Of course, some gray whales are still migrating south in January and we cannot be certain that all infestations were from northward migrating whales. However, the observations of Rice and Wolman (1971), mentioned earlier, suggest that infestation by southward migrating gray whales is unlikely. Because white whales do a good deal of rubbing and scratching on one another and objects within their enclosures, it is difficult to tell whether or not barnacle infestation causes irritation. We have not noticed quantifiable signs that the barnacles cause skin irritation to the whale. We question if there might be some secretion from the barnacle that may have an anesthetic effect on whale skin, for it is known that barnacles may influence the growth of surrounding tissue when established on other animals (Anderson, 1994). It is interesting that no barnacles were ever found on any of the numerous bottlenose dolphins, Tursiops truncatus (Montagu), that occupied San Diego Bay alongside the white whales. Perhaps physiological or anatomical differences in the skin covering of the two species (Brown et al., 1983; Hicks et al., 1985; St. Aubin et al., 1990; Shoemaker and Ridgway, 1991) explain the barnacles selective affinity for, or ability to, infest white whales. The proliferation of skin and the invasion of inflammatory cells at the juncture between skin and barnacle shell suggests that with successive exposure over a period of 3-4 yrs, an immunity developed in response to the barnacle. We have not looked for barnacle antibodies in whales; however, this should be the next step in defining the proliferative skin response we observed. In their summer feeding areas off Alaska and Siberia, gray whales are sympatric with white whales, yet barnacle infestations have never been reported in white whales in the North Pacific. Atlantic gray whales probably became extinct at least two centuries ago. Likely, the Atlantic gray whales were coastal migrators and may well have been sympatric with the Hudson Bay populations (Reeves and Mitchell, 1988) from which our animals were taken at Churchill, Canada. It seems reasonable to question whether the North Pacific white whales are already sensitized, or more easily sensitized to the barnacle, than our North Atlantic white whales. In view of the aforementioned observations of Rice and Wolman (1971), however, it appears more likely that C. rhachianecti do not produce larvae in the cooler northern waters that their gray whale hosts share with white whales. ACKNOWLEDGMENTS We thank C. Bowers and D. Ewing for help in the initial discovery of barnacles on the white whales, M. Reddy for help with manuscript preparation, and R. Tarpley for taking the photomicrographs. The whales were collected in 1977 and 1980 under Canadian and U.S. federal permits. Since collection, the whales have been maintained in accordance with regulations promulgated under the Animal Welfare Act and Marine Mammal Protection Act.
9 RIDGWAY ET AL.: GRAY WHALE BARNACLES ON WHITE WHALES 385 LITERATURE CITED Anderson, D. T Barnacles. Chapman and Hall, London. 357 p. Brown, W. R., J. R. Geraci, D. B. Hicks, D. J. St. Aubin, and J. P. Schroeder Epidermal proliferation in the bottlenose dolphin (Tursiops truncatus) Can. J. Zool. 61: Dayton, P. K., M. J. Tegner, P. E. Parnell, and P. B. Edwards Temporal and spatial patterns of disturbance and recovery in a kelp forest community. Ecol. Monogr. 62: Geraci, J. R. and D. J. St. Aubin Effects of parasites on marine mammals. Int. J. Parasitology 17: Hicks, B. D., D. J. St. Aubin, J. R. Geraci and W. R. Brown Epidermal growth in the bottlenose dolphin, Tursiops truncatus. J. Invest. Dermatol. 85: Hirano, R. and J. Okushi Studies on sedentary marine organisms - I. Seasonal variations in the attachment and growth rates of barnacle cyprids in Aburatsubo Bay, near Misaki. Bull. Jap. Soc. Scient. Fish. 18: Newman, W. A. and D. P. Abbott Cirripedia. Pages in R. H. Morris, D. P. Abbott, E. C. Haderlie, eds. Intertidal Invertebrates of California. Stanford University Press. and A. Ross Revision of the balanomorph barnacles; including a catalogue of the species. San Diego Soc. Nat. Hist. Memoir 9: Reeves, R. R. and E. Mitchell Current status of the gray whale Eschrichtius robustus. Canad. Field Natu. 102: Rice, D. W., and A. A. Wolman The life history and ecology of the gray whale (Eschrichtius robustus). Spec. Publ. Am. Soc. Mammal. 3: Scarff, J. E Occurrence of the barnacles Coronula diadema, C. reginae and Cetopirus complanatus (Cirripedia) on right whales. Sci. Rep. Whales Res. Inst. 37: Shoemaker, P.A. and S. H. and Ridgway Cutaneous ridges in odontocetes. Mar. Mam. Sci. 7: Slijper, E. J Whales. Basic Books, New York. St. Aubin, D. J., T. G. Smith and J. R. Geraci Seasonal epidermal molt in beluga whales, Delphinapterus leucas. Can. J. Zool. 68: Wolman, A. A Gray Whale Eschrichtius robustus (Lilljeborg, 1861). Pages in S. H. Ridgway and R. J. Harrison, eds. Handbook of marine mammals: Volume III The Sirenians and Baleen Whales. Academic Press, London. DATE ACCEPTED: September 25, 1995 ADDRESSES: (S. H. R. and E. L.) Naval Command, Control, and Ocean Surveillance Center, RDTE DIV D3503, San Diego, CA ; (K. A. M.) Office of the San Diego County Veterinarian, 5555 Overland Ave., Bldg. 4, M.S San Diego, CA 92123; (W. A. N.) Scripps Institution of Oceanography, La Jolla, CA
-Cl No. of baleen plates. ..c KASUYA AND RICE E ~20 Q. 10. Sci. Rep. Whales Res. Inst., No. 22, 1970.
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