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Monroe and Limpus (1979) described a new species of turtle barnacle which they assigned to the genus Tubicinella Lamarck, a genus previously known to occur only on cetaceans. Our analysis of the situation confirms our suspicion that they misinterpreted certain characteristics and relationships concerning their new species, as detailed below. Monroe & Limpus (1979) expressed reservations about including their new species, Tubicinella cheloniae, within the whale barnacle clade (Coronulidae) because it would not “ ... adequately reflect the relationship of this species to other members of the family.” Nonetheless, Monroe (1981) elected to redefine the higher taxa and resurrect one other familial level taxon that in effect destroyed the unity of the whale barnacles on one hand and the turtle barnacles on the other, a unity which was so clearly expounded by Pilsbry (1916) and carried forward in later studies (Newman & Ross 1976). Below we re-establish this unity by incorporating Tubicinella cheloniae (here renamed Chelolepas cheloniae) into the Platylepadidae and we assign a new genus to this unique form of turtle barnacle. We also trace the history of this species through the literature from its original description as a life stage variation of another platylepadid, Stephanolepas muricata, to subsequent studies that, as a result of its original misidentification, have improperly catalogued this species as S. muricata when encountering it upon marine turtles (i.e. Hendrickson 1958).

The whale barnacle Tubicinella Lamarck, 1802 (Figures 1A, 2B)

Lamarck (1802) described two species of Tubicinella based on specimens taken from a whale in the south Atlantic Ocean. Among the species he described only one, T. major, is presently recognized and it occurs solely on the southern right whale, Eubalaena australis (DesMoulins). According to Pilsbry (1916), Olas Worm reported a tubicinellid on the head of a stranded whale from the coast of Syderoe, one of the Faroe Islands, and there is one unconfirmed record on a stranded bottlenose whale (Hyperoodon ampullatus) in Nova Scotia (Mitchell & Kozicki 1975).

Tubicinella is a relatively large barnacle, often exceeding 50 mm in height. The wall is cylindrical, bilamellar, and ornamented externally by simple, relatively wide-spaced ridges, and it lives wholly embedded to its orifice in the tissues of its host. The external ridges comprise swellings in the parietes rather than discrete structures added to the wall.

Darwin (1854) devoted considerable space to his description of Tubicinella. Among other aspects of its morphology he analyzed the manner of growth and he interpreted the development of the parietal ridges as a means of forestalling the rejection of the barnacle from the tissues of the host.

The turtle barnacle Stephanolepas Fischer, 1886 (Figure 1B&C)

Fischer’s (1886) description of Stephanolepas muricata from Pulo Condor, Condor Is., Cochin China (= Viet Nam) was based on specimens taken from the carapace and plastron of the hawksbill turtle Eretmochelys imbricata (Linnaeus). Nilsson-Cantell (1932) mistakenly described and illustrated specimens from Bentota, Ceylon, also from a hawksbill, that he attributed to Stephanolepas, believing his specimens were adult whereas those described by Fischer were juveniles. He also suggested that his specimens revealed that the species in question was closest in form to that of Tubicinella, but quite distinct from this genus. Hendrickson (1958) described and illustrated the same species taken from growths on the carapace of the green turtle Chelonia mydas (Linnaeus) taken at Talang Talang, Besar Island, Sarawak - presumably basing his identification on the work of Nilsson-Cantell and, as a result, called his specimens S. muricata. However, Monroe & Limpus (1979) clearly recognized that what Nilsson-Cantell and Hendrickson had described was not S. muricata but rather a wholly different species for which they proposed the epithet Tubicinella cheloniae.

The basally tapering, or deep bowl-shaped wall of Stephanolepas also has external ridges extending completely across the parietes. However, as we shall demonstrate these are special structures added to the wall and they develop in part from the suture where they form small knobs, the whole reminiscent of a dog bone or bow tie (Figure 1 B-C). These similarly serve to anchor the barnacle in the host.

The turtle barnacle Tubicinella cheloniae Monroe & Limpus, 1979
Monroe & Limpus (1979) included “... this species in Tubicinella because of the strong affinity shown by the general facies of the shell and the mode of invasion of the host”. However, Cylindrolepas, a platylepadid turtle barnacle, also has a tall cylindrical wall and has never been considered a feature warranting its designation to the coronulid whale barnacles.

The wall in T. cheloniae is relatively small, attaining a height of about 20-25 mm and a diameter of 10 mm. The most outstanding feature is the development of horizontally flattened, upward curving flanges that project from the lateral edges of the parietes and extend well beyond the circumference of the wall (Figure 1D).

DEFINITION. Wall with six plates, deciduous; parietes commonly with pronounced medial tooth or sulcus; wall elaborations, when present, emanating from both sides of suture concomitant with diametric growth; opercular plates wider than high; embedded in tissues of sea turtles and other marine animals.

REMARKS. Monroe (1981) was confronted with an ambiguous definition of the platylepadids largely stemming from the work of Pilsbry (1916). Newman & Ross (1976) in recognizing the familial level status of the platylepadids unfortunately did not provide a definition. For the most part Monroe (1981) was unable to adequately define the platylepadid clade which accounts for his unusual reassignment of genera to one or another family.

TYPE SPECIES. Tubicinella cheloniae Monroe and Limpus, 1979; Recent, Mon Repos, southeast Queensland, Australia; on Caretta caretta.
ETYMOLOGY. Derived from Greek, Chelo-, turtle, and -lepas, barnacle; gender feminine.

DEFINITION. Wall tall, cylindrical, tubiferous; parietes with flat upturned, flanges arising from each side of suture, enlarging during diametric growth and extending well beyond circumference of wall; articulation of wall plates complex.

Figure 1. Technical representations of cirripeds: A. Tubicinella major, scale bar = 10 mm, B. Stephanolepas muricata (side view), C. S. muricata (ventral view), scale bar between B and C = 6 mm, D. Chelolepas cheloniae (formerly Tubicinella cheloniae) (side view), scale bar = 10 mm, E. dorsal schematic of external, upturned flange in Chelolepas consisting of two juxtaposed components, each contributed from opposite sides of the suture – representing the key diagnostic character of this new genus. Figure adapted from Pilsbry (1916), Fischer (1886) & Nilsson-Cantell (1932). A, B & D depict the barnacles in an upright position (aperture or opening face up). When embedded in turtles the entire barnacle is located subcutaneously and only the opening (aperture) and the top edge of the barnacle shell is exposed.

Figure 2. Photographs of cirripeds: A. Chelolepas cheloniae (formerly Tubicinella cheloniae) (side view) and B. Tubicinella major (side view). Units on the middle scale bar = 1 mm.

REMARKS. The two part nature of the flanges, with a portion contributed from each side of the suture, clearly separate Chelolepas from all other known platylepadids. These flanges obviously serve to anchor the barnacle in the tissues of the host, where they are commonly entwined with fibrous connective tissue (Monroe 1981).
Chelolepas cheloniae (Monroe & Limpus 1979) (Figures 1D&E, 2A)
Stephanolepas muricata: Nilsson-Cantell 1932: 258 (wall morphology, Ceylon); Hendrickson 1958: 524 (effect on host, Sarawak).
Tubicinella cheloniae Monroe & Limpus 1979: 199 (morphology, Queensland); Monroe 1981: 241 (growth and phylogeny, Queensland); Jones et al. 1990 (Australian distribution); Limpus et al. 1994: 147 (Queensland).

Figure 3. A subadult loggerhead turtle from Baja California, Mexico hosting numerous platylepadid barnacles embedded into the flippers and an eyelid. These insitu specimens appear to be Chelolepas cheloniae but collections from dead turtles would be necessary to confirm the species in question.

MATERIAL: Scripps Inst Oceanography, Benthic Invertebrates C- 5813; 4 spec. alcohol, Talang Talang, Besar Is., Sarawak; on Chelonia mydas; J. R. Hendrickson coll., Sept. 1952. California Acad Sci 153163, same as SIO C-5813. Queensland Museum W7473; Wynnum, Moreton Bay, SE Queensland; on Chelonia mydas; P. Davie coll., October 1, 1978.

REMARKS. This species is only known to occur on three species of turtle in Australasian waters (Dobbs & Landry 2004). Its presence has not been detected in the central or eastern Pacific regions based on material available to us. However, photographic evidence from Baja California, Mexico suggests that this species is present in the eastern Pacific (see Figure 3) but no specimens have been collected to verify this possibility. Thus, researchers in this area should conduct detailed analyses of the platylepadid, skin barnacles from dead or dying chelonians. Hendrickson (1958) described the deleterious effects it has on the green turtle in Sarawak. However, we are not convinced it is the causative agent in the development of the tumors that Hendrickson described.

DISCUSSION Tubicinella and Chelolepas live fully embedded in the tissues of their host, the former on whales the latter on sea turtles (see Figure 3 for an example of C. cheloniae colonization). Both have a relatively thin or flimsy cylindrical wall and both rely on a combination of factors, including modest diametric growth, to increase the size and volume of the body chamber as well as to maintain the apex of the wall at the surface of the host. For the most part Tubicinella relies on abrasion and breakage to maintain its position whereas Chelolepas depends upon corrosion and delamination, something that is abundantly evident when cleaning any platylepadids in household bleach, especially individuals of Stomatolepas Pilsbry. This pronounced difference clearly sets them apart. The tissue surrounding the aperture or scuto-tergal flaps are a characteristic of all sessile barnacles. However, in the whale barnacles they reach their greatest development by forming a tall apertural shroud that likely functions to prevent over extension and expansion of the cirral net when deployed. Monroe & Limpus (1979) did not report its presence in C. cheloniae. Nonetheless, in this species it does not attain the prominence displayed in whale barnacles, and we have not detected its presence in other platylepadids. The opercular plates in whale and turtle barnacles, unlike those found in balanids, are clearly a laminate of cuticular and calcareous material. It is likely that corrosion of the cuticular lamina at each major growth increment results in delamination, thus periodically exposing a fresh surface to the vagaries of an abrasive environment. In both families the opercular membrane, comprised of several layers (Darwin 1854), has one or two layers extending to the base of the wall. Noteworthy is that the opercular plates in Tubicinella are higher than wide, but wider than high in Chelolepas as in all platylepadids. The large, conspicuous, longitudinal parietal tubes in Tubicinella are numerous and surprisingly uniform in size except for one or two larger ones adjoining the radius (Figures 1A & 2B). These develop externally by deepening and closing over external striae (Darwin 1854; Pilsbry 1916), as they do in certain species of Platylepas. In contrast, those in Chelolepas are cryptic, ovate to circular in outline, few in number and apparently secondarily filled, but develop in the same manner. The longitudinal tubes are directly involved in the formation of the transverse ridges of Tubicinella, but they are not involved in the construction of the flanges in Chelolepas.

The circumferential transverse ridges of Tubicinella reflect a swelling or slight bulge of the exterior lamina, and they are low, simple, evenly rounded and they are not involved in diametric growth. The flanges in Chelolepas consist of two juxtaposed components each contributed from opposite sides of the suture (Figure 1E & 2A). In addition, although initially hollow, the flanges become multiseptate and some appear to be secondarily filled. Their growth is concomitant with diametric growth. The delicate and intricate lace-like fimbriations in Stomatolepas are similar in that they arise from each side of the suture. In both of these genera the wall elaborations forestall their rejection by the host.

The tubiferous radii in Tubicinella which extend from the apex to the base consist of an inner and outer lamina connected by transverse septa. Near the outer lamina they bifurcate or trifurcate, thereby resulting in a square primary tube and irregular secondary or tertiary tubes all of which connect with the large proximal longitudinal tubes of the parietes (Darwin 1854). The radius in Chelolepas is an open channel bordered on one surface by strong denticles. The radius in Platylepas and Stomatolepas is also an open channel.

The paired branchiae or gills in Tubicinella are “enormously developed” - their combined size equaling about two-thirds of the area of the mantle cavity. Each consists of two folds, both deeply plicated (Darwin 1854). In Chelolepas they are relatively small and simple and they lack any plications. The difference between the two genera may reflect physiological or ecological differences relating to swimming speed, diving depth, or rate of descent of the host.

In comparing sperm ultrastructure Healy & Anderson (1990) discovered that the sperm of Chelolepas is most closely related to the platylepadid Cylindrolepas. In differing significantly from the whale barnacle Coronula, they summarily dismissed the notion of Monroe & Limpus (1979) and Monroe (1981) to include C. cheloniae within the whale barnacle lineage.

Monroe’s (1981) reassessment of the whale and turtle barnacles resulted in an unnatural alliance of diverse taxa, and did not recognize the convergent evolution of wall structures that are an adaptation for living in the soft tissues of a mobile host. Based on the foregoing comparisons we view the resemblance of Chelolepas to the whale barnacle Tubicinella as an excellent example of convergent evolution; in all other regards it is a platylepadid turtle barnacle. Furthermore, we subscribe to the alignment of taxa so lucidly promulgated by Pilsbry (1916).

Acknowledgments: We thank Peter Davie, Queensland Museum, Australia, Robert J. Van Syoc, California Academy of Sciences, San Francisco and William Newman, Scripps Institution of Oceanography for the loan of specimens. This study was supported, in part, by contract number 40JJNF100200 (to AR) from NOAA, National Marine Fisheries Service, Honolulu Laboratory and funding from the Caretta Research Project. We thank Eric A. Lazo-Wasem from the Peabody Museum of Natural History, Yale University for the picture of T. major, Hoyt Peckham for the photo in Fig. 3 and Kirsten Dobbs for the picture of C. cheloniae. Dana Biasatti and an anonymous reviewer provided helpful comments that improved the manuscript. Barnacle collections made by George Balazs inspired our research into the Coronuloidea. This paper is dedicated to the memory of Crawford Jackson and John Hendrickson and to the continually exceptional cirriped research conducted by William A. Newman.

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