Gray Whale Barnacles <I>Cryptolepas Rhachianecti</I

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Gray Whale Barnacles <I>Cryptolepas Rhachianecti</I BULLETIN OF MARINE SCIENCE, 61(2): 377–385, 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 an- nually 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 epider- mis 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 south- bound whales as they pass by San Francisco; however, all northbound whales carry nu- merous 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 bar- nacles 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, Hawaii; Puget Sound, Wash- ington; or Vancouver Island, Canada (Table 1). 377 378 BULLETIN OF MARINE SCIENCE, 61(2): 377–385, 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 decal- cified, 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 mani- fested by the whales, we eliminated most of the barnacles from the whales’ skin by apply- RIDGWAY ET AL.: GRAY WHALE BARNACLES ON WHITE WHALES 379 fosecnedicnidna,5991-7791,BURdna,UHC,KUM,CON,selahwetihwfonoitacoL.1elbaT .snoitatsefnielcanrab Aelamin Dnat LsocatioBarnacle N7OC8l/197CsanadatoSDpooNobarnacle 1D2/1977O8penwaterSBarnacles1/7 1D979OdpenwaterSReinfested,noskinresponsenote 0A4/30/79SanClementeIs.,C 1a0/1980Wsash.andCanadNobarnacle 1a981Wsash.andCanadNobarnacle 3D/1982OdpenwaterSReinfested,noskinresponsenote 1i1/1982HsawaiNobarnacle 1i983HsawaiNobarnacle 4D/1984OspenwaterSNobarnacle 1D985OdpenwaterSReinfested,noskinresponsenote 1D986OepenwaterSReinfested,markedskinrespons 1D987to1995OnpenwaterSReinfestedeachJan/Mar,markedski response C7HU8l/197CsanadatoSDpooNobarnacle 1D2/1977O8penwaterSBarnacles1/7 1D979OdpenwaterSReinfested,noskinresponsenote 5l/1980SsDpooNobarnacle 5i/1981HsawaiNobarnacle 3i/1982HsawaiNobarnacle 1i983HsawaiNobarnacle 1D0/1984OspenwaterSNobarnacle 2D/1985OdpenwaterSReinfested,noskinresponsenote (5/95died) M7UK8l/197CsanadatoSDpooNobarnacle 1D2/1977O8penwaterSBarnacles1/7 1D979OdpenwaterSReinfested,noskinresponsenote 0A4/30/79SanClementeIs.,C 1a0/1980Wsash.andCanadNobarnacle 1a981Wsash.andCanadNobarnacle 3D/1982OdpenwaterSReinfested,noskinresponsenote 1D983OdpenwaterSReinfested,noskinresponsenote 1D984OdpenwaterSReinfested,noskinresponsenote 1D985to1995OnpenwaterSReinfestedeachJan/Mar,markedski response R0UB7l/198CsanadatoSDpooNobarnacle 1D0/80O1penwaterSBarnacles1/8 1D982OdpenwaterSReinfested,noskinresponsenote 1D983OdpenwaterSReinfested,noskinresponsenote 1D984OdpenwaterSReinfested,noskinresponsenote 1D985to1995OnpenwaterSReinfestedeachJan/Mar,markedski response 380 BULLETIN OF MARINE SCIENCE, 61(2): 377–385, 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. High- magnification 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 com- partments and had no calcareous basis, but it was clearly a balanomorph or sessile bar- nacle. 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 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. 382 BULLETIN OF MARINE SCIENCE, 61(2): 377–385, 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 diam- eter, 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 1981. During these initial infestations there was no apparent skin response (Fig. 3A); however, with several successive years of exposure, a marked response devel- oped (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 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;
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