MORPHOLOGICAL VARIATION (PHENOTYPIC PLASTICITY) IN BARNACLES

An underlying theme present throughout Hayashi (Reference Hayashi2011) regards the ‘plasticity’ or morphological variation that occurs in the way coronuloid barnacles produce the shell that surrounds them. By all accounts, and given the number of studies that document shell variation in a number of balanomorph barnacle species, Hayashi (Reference Hayashi2011) is correct in pointing out the occurrence of morphological variation in the Coronuloidea (also discussed by Darwin (Reference Darwin1854) and Pilsbry (Reference Pilsbry1916)). However, through the analysis of numerous specimens, it is possible to recognize consistent characters that represent specific or interspecific morphological variation in barnacles (see Pilsbry's (1916) comments on the coronuloid Platylepas hexastylos (Fabricius, 1798)).

External morphological characters are generally used to define taxonomic relationships in the Coronuloidea (see Darwin, Reference Darwin1854; Pilsbry, Reference Pilsbry1916; Ross & Newman, Reference Ross and Newman1967; Monroe & Limpus, Reference Monroe and Limpus1979; Monroe Reference Monroe1981; Young, Reference Young1991). Hayashi (Reference Hayashi2011) emphasizes that descriptions and comparisons of the morphology of the barnacle's ‘soft parts’ (cirri, penis, etc.) are just as important in establishing an accurate classification of the coronuloid barnacles. It should be noted, however, that a number of studies report interspecific morphological variation in the cirral and penis morphology of barnacles occurring under different environmental conditions (see Arsenault et al., Reference Arsenault, Marchinko and Palmer2001; Marchinko, Reference Marchinko2003; Marchinko & Palmer, Reference Marchinko and Palmer2003; Hoch, Reference Hoch2008; and references within these papers). And, in most cases, this type of interspecific morphological variation exceeds that observed in shell morphology (López et al., Reference López, Ramírez, Guaitro and López2010). Such ‘soft part’ variation often occurs as a result of wave exposure and other environmental factors associated with attachment location (ecophenotypic response); and to a lesser degree, through genetic inheritance (genotypic reponse). Additionally, Marchinko (Reference Marchinko2003) indicates that the cirral morphology of an individual balanomorph barnacle can change significantly within a period of 18 days or less (~2 molts).

Moreover, the external surfaces of sea turtles are by no means a uniform attachment environment. Some attachment surfaces on host turtles are curvaceous and highly flexible, while others are planar and rigid. Additionally, some attachment sites on host turtles are highly movable (i.e. flippers, skin, head and tail), while other attachment sites are fixed (carapace and plastron). Most chelonophilic barnacle species will occur on all external surfaces of host turtles (Frick et al., Reference Frick, Zardus and Lazo-Wasem2010a). For instance, Stephanolepas muricata Fischer, 1886 is documented to attach to the head, skin, flippers, carapace and plastron of cheloniid turtles (Frick et al., Reference Frick, Zardus, Ross, Senko, Montano-Valdez, Bucio-Pacheco and Sosa-Cornejo2011). Given the variety of environmental conditions that undoubtedly occur in association with these disparate attachment sites, one would expect that the ‘soft part’ morphology of a coronuloid—like S. muricata—to vary with respect to the conditions associated with a particular attachment location (an aspect of coronuloid biology illustrated for the first time by Hayashi (Reference Hayashi2011) but neither discussed nor acknowledged).

Hayashi (Reference Hayashi2011) points out differences in shell morphology observed in S. muricata in relation to specimens that attach to different regions of a host turtle (a morphological aspect originally presented by Frick et al. (Reference Frick, Zardus, Ross, Senko, Montano-Valdez, Bucio-Pacheco and Sosa-Cornejo2011) for eastern Pacific S. muricata). Yet, he does not include a similar comparison of the ‘soft parts’ between these two ‘types’ of S. muricata in the descriptions provided. Instead, he clearly illustrates these differences (Plate 4 therein) but makes no mention of them in the text. Had Hayashi (Reference Hayashi2011) acknowledged this facet of barnacle biology occurring within the Coronuloidea he would have no cause to disagree with the current taxonomic placement of the following species:

TUBICINELLA CHELONIAE MONROE & LIMPUS, 1979 OR CHELOLEPAS CHELONIAE (MONROE & LIMPUS, 1979)

The tubular, coronuloid genus Tubicinella was erected by Lamarck (Reference Lamarck1802). It is currently known only from right whales, Eubalaena australis (Desmoulins, 1822) and Eubalaena japonica (Lacépède, 1818). Tubicinella appears to have occurred at one time in the North Atlantic Ocean, as indicated by illustrations provided by Worm (1655; in Pilsbry (Reference Pilsbry1916)) of specimens collected from a balaenid whale that was landed in the Faroe Islands (between Scotland and Iceland). Worm's (1655) account of this whale barnacle was unknown to Darwin (Reference Darwin1854), but it was later widely-disseminated by Pilsbry (Reference Pilsbry1916), who identified the specimens illustrated by Worm (1655) as belonging to the genus Tubicinella. Since Worm's (1655) publication, no Tubicinella specimens have ever been observed on any North Atlantic cetacean species. The only balaenid whale species documented from the Faroe Islands is the northern right whale, Eubalaena glacialis (Müller, 1776), but contemporary analyses of numerous E. glacialis have failed to detect any whale barnacle species from present day populations (Rolland et al., Reference Rolland, Hamilton, Marx, Pettis, Angell, Moore, Kraus and Rolland2007). It is possible that the near decimation of northern right whales during the 19th and early 20th Centuries (Reeves et al., Reference Reeves, Smith, Josephson, Kraus and Rolland2007) eventually led to the extirpation of Tubicinella from the North Atlantic, or that Tubicinella still inhabits the North Atlantic via E. glacialis, and that the contemporary rarity of this barnacle's host has made its detection difficult.

Lamarck (Reference Lamarck1802) originally described two Tubicinella species: Tubicinella major and Tubicinella minor. Detailed analyses by Darwin (Reference Darwin1854) revealed that these two species are synonymous and any differences between the two ‘species’ noted by Lamarck are purely ontogenetic. Given that Lamarck had dubbed his two new species as ‘major’ and ‘minor’, and because Darwin (Reference Darwin1854) demonstrated that both species were actually one in the same, Darwin (Reference Darwin1854) thought it bad nomenclature to retain the name ‘major’ when there was actually no ‘minor’. So Darwin decided to reject Lamarck's species and gave priority to the name Tubicinella trachaealis (Shaw, 1806)—defying the normal and accepted avenues established for naming and renaming species observed at the time (prior to the publication of the International Code of Zoological Nomenclature (the Code) by the International Commission on Zoological Nomenclature (ICZN) on 9 November 1961). Noting Darwin's (Reference Darwin1854) deviation from proper nomenclatural protocol, Pilsbry (Reference Pilsbry1916) reinstated Lamarck's nomenclatural priority and, as a result, T. major is the correct epithet recognized today.

Nilsson-Cantell (Reference Nilsson-Cantell1932) examined specimens of another tubular barnacle collected from hawksbill turtles, Eretmochelys imbricata (Linnaeus, 1776), nesting at what is known today as the island of Sri Lanka. Erroneously, he concluded that these specimens represented large individuals of S. muricata. Noting that Nilsson-Cantell's (1932) observations were incorrect, Monroe & Limpus (Reference Monroe and Limpus1979) formally named the species in question Tubicinella cheloniae—basing their placement of this species into the genus Tubicinella on the tubular form of the shell and its similar invasion into the host tissue to that observed in T. major.

Ross & Frick (Reference Ross and Frick2007)—examining Australian specimens collected by Monroe & Limpus (Reference Monroe and Limpus1979), specimens collected from Malaysia and Sarawak by Hendrickson (Reference Hendrickson1958) and additional material in the collections of the California Academy of Sciences—describe marked differences in how T. cheloniae and T. major produce their tubular shells and retain their position within the host tissue. These differences, exhaustively and clearly described by Ross & Frick (Reference Ross and Frick2007), warranted erecting a new genus, Chelolepas Ross & Frick, Reference Ross and Frick2007, to include this species. Nevertheless, Hayashi (Reference Hayashi2011) dismisses this taxonomic assignment in the following statement: ‘Ross & Frick (Reference Ross and Frick2007) established the genus Chelolepas as new for Tubicinella cheloniae, however, there is no description and comparison on soft parts between Tubicinella major and T. cheloniae.’ As a result, Hayashi (Reference Hayashi2011) retains the epithet T. cheloniae therein. Yet, the studies of Darwin (Reference Darwin1854), Nilsson-Cantell (Reference Nilsson-Cantell1932) and Monroe & Limpus (Reference Monroe and Limpus1979) describe, illustrate and allow for the comparison of the ‘soft parts’ of C. cheloniae and T. major.

A perusal of these descriptions and illustrations reveals differences in the ‘soft part’ morphology between these two coronuloids, particularly in the morphology of the mandibles. The mandibles in T. major bear four distinct primary teeth, where all teeth, excepting the first tooth, possess a double point. Smaller, intermediate teeth are present between the second, third and fourth primary teeth. The inferior angle on each intermediate tooth is irregularly pectinated (Darwin, Reference Darwin1854). The mandibles of C. cheloniae bear five distinct primary teeth, where teeth four and five are smaller with an irregularly pectinated inferior angle. An intermediate tooth is present between primary teeth two and three. Primary teeth two and three often bear double points (Nilsson-Cantell, Reference Nilsson-Cantell1932).

A more contemporary analysis by Monroe & Limpus (Reference Monroe and Limpus1979) indicates that the mandibles of Australian C. cheloniae differ from those reported for Sri-Lankan specimens by Nilsson-Cantell (Reference Nilsson-Cantell1932). Specimens from Queensland bear four primary mandible teeth, where teeth two and three possess a double point. Intermediate teeth are present between primary teeth two, three and four. These observations seemingly amalgamate the descriptions of T. major and C. cheloniae mandibles presented by Darwin (Reference Darwin1854) and Nilsson-Cantell (Reference Nilsson-Cantell1932), bringing into question the efficacy of soft-part analyses in ascertaining broader evolutionary relationships within the Coronuloidea. Or, the same observations could have been used by Hayashi (Reference Hayashi2011), despite marked differences in shell morphology between the two species, to support his inclusion of C. cheloniae into the genus Tubicinella.

Differences in soft part morphology between regional C. cheloniae populations, those that approximate characters seen from the mandibles of T. major, may also point to co-evolutionary adaptations amongst the Coronuloidea as discussed by Ross & Frick (Reference Ross and Frick2007), or that an undescribed Chelolepas sp. occurs on Indo-Pacific hawksbill turtles. The observed soft part differences noted above between C. cheloniae populations may also simply represent ecophenotypic responses to the barnacle's surrounding environment as documented in S. muricata (Frick et al., Reference Frick, Zardus, Ross, Senko, Montano-Valdez, Bucio-Pacheco and Sosa-Cornejo2011; Hayashi, Reference Hayashi2011). Currently, observations on shell morphology and production reported by Ross & Frick (Reference Ross and Frick2007) are the most comprehensive comparisons of C. cheloniae and T. major. Their results clearly support the current placement of these two species into two different genera, and, more importantly, within two different families—families that taxonomically distinguish chelonophilic barnacles (Platylepadidae) from cetophilic barnacles (Coronulidae), and families that clarify evolutionary relationships within the Coronuloidea (Ross & Newman, Reference Ross and Newman1967; Ross & Frick, Reference Ross and Frick2007).

It should be emphasized that most cirripedologists, including the current author, recognize that analyses of ‘soft part’ morphology, when combined with analyses of shell morphology (see Chan et al., Reference Chan, Tsang and Chu2007), provide useful characters in ascertaining taxonomic affinities. However, shell morphology, when viewed from a Darwinian perspective that yields speciation to the likelihood of variation or convergent evolution, is currently the most reliable tool taxonomists have in illuminating the classification of barnacles, especially with respect to fossilized species (Ross & Newman, Reference Ross and Newman1967). Even molecular data must be accompanied by rigorous analyses of shell morphology in order to properly classify barnacle species (Chan et al. Reference Chan, Tsang and Chu2007). Yet, despite his emphasis on ‘soft part’ morphology, Hayashi (Reference Hayashi2011) provides no comparisons between animal and shell morphology of the barnacles he examined. Such an analysis is necessary for Hayashi (Reference Hayashi2011) to substantiate the importance he places on the use of ‘soft parts’ over shell morphology in ascertaining taxonomic relationships within the Coronuloidea (as demonstrated by his dismissal of the validity of the genus Chelolepas).

It should also be noted that Hayashi (Reference Hayashi2011) describes the horizontal projections of C. cheloniae as simply emanating from the lateral ‘edges’ of the shell plates. More specifically, and as illustrated in the same paper (Figure 5 therein), these projections emanate from either side of the sutures between plates. These projections or ‘flanges’ articulate with those of the neighbouring plate to form a two-part flange, where a portion of each flange is actually contributed by two separate plates—a characteristic that, by itself, clearly separates Chelolepas from Tubicinella (Ross & Frick, Reference Ross and Frick2007).

CYLINDROLEPAS DARWINIANA PILSBRY, 1916, CYLINDROLEPAS SINICA REN, 1980 AND PLATYLEPAS DECORATA DARWIN, 1854

The most notable omission in Hayashi (Reference Hayashi2011) is that of a study by Frick & Zardus (Reference Frick and Zardus2010) on the first authentic report of C. darwiniana since its description by Pilsbry (Reference Pilsbry1916). Frick & Zardus (Reference Frick and Zardus2010) provide the most detailed analysis of C. darwiniana to date, and report that past accounts of C. darwiniana actually represent reports of the morphologically-similar Platylepas decorata Darwin, Reference Darwin1854. The same study also reports preliminary findings that indicate that Cylindrolepas sinica Ren, 1980 is synonymous with P. decorata. Moreover, Frick & Zardus (Reference Frick and Zardus2010) and Frick et al. (Reference Frick, Zardus and Lazo-Wasem2010b) provide analyses and discussions noting morphological similarities between C. darwiniana and P. decorata that, after further analyses, may necessitate placing P. decorata into a new genus, and may necessitate placing both P. decorata and C. darwiniana together under a new subfamily and away from the Platylepadinae, where P. decorata and C. darwiniana currently reside, taxonomically.

Given that Hayashi (Reference Hayashi2011) reports all three of these species from Japanese waters, it is curious as to why he failed to mention the most up-to-date information available on these species and compare his observations to those made by Frick & Zardus (Reference Frick and Zardus2010). The illustrations provided by Hayashi (Reference Hayashi2011) of these three species (Figures 8, 9 and 10 therein) clearly demonstrate their similarity; to the point where the shells of P. decorata and C. sinica appear to represent the same species (the material descriptions provided by Hayashi (Reference Hayashi2011) are insufficient for comparisons or species identification throughout his paper). However, Hayashi's (2011) illustrations of the ‘soft parts’ of these two species vary markedly, and could have provided the author an opportunity to refute or expand upon the observations made by Frick & Zardus (Reference Frick and Zardus2010).

Additionally, within the material descriptions provided by Hayashi (Reference Hayashi2011) the author omits integral characteristics that unequivocally characterize both P. decorata and C. darwiniana (see Zardus & Balazs, Reference Zardus and Balazs2007 and Frick & Zardus, Reference Frick and Zardus2010 for more detailed descriptions of these species, respectively). With respect to C. darwiniana, it is difficult to determine from the photographs in Hayashi (Reference Hayashi2011) whether these diagnostic characteristics are present on the specimens he examined, and, as mentioned above, they are not noted in the material description provided. It is clear to the present author, however, that the photographs of C. darwiniana presented by Hayashi (Reference Hayashi2011) do not represent C. darwiniana sensu stricto as described by Pilsbry (Reference Pilsbry1916) and Frick & Zardus (Reference Frick and Zardus2010). It is possible that these specimens represent an undescribed Cylindrolepas species. Comparisons of the Okinawa material to C. darwiniana collected and examined by Frick & Zardus (Reference Frick and Zardus2010) would clarify the identity of this barnacle from Japanese loggerhead turtles, Caretta caretta (Linnaeus, 1758).

STOMATOLEPAS DERMOCHELYS MONROE & LIMPUS, 1979, STOMATOLEPAS ELEGANS (COSTA, Reference Costa1840) AND STOMATOLEPAS PRAEGUSTATOR PILSBRY, 1910

There has been much confusion over the identities of Stomatolepas dermochelys Monroe & Limpus, Reference Monroe and Limpus1979, Stomatolepas elegans (Costa, Reference Costa1840) and Stomatolepas praegustator Pilsbry, 1910. An extensive analysis by Frick et al. (Reference Frick, Zardus and Lazo-Wasem2010a) rectified this confusion by examining numerous specimens and by outlining the nomenclatural history of these species that ultimately lead to the aforementioned taxonomic misunderstandings. Hayashi (Reference Hayashi2011), however, promulgates the confusion surrounding the identities of these species that existed prior to the publication of Frick et al. (Reference Frick, Zardus and Lazo-Wasem2010a) despite citing the same study within his publication.

Hayashi's (2011) treatment of the genus Stomatolepas begs to question whether or not the author gave more than a cursory examination of the works of Pilsbry (Reference Pilsbry1916), Monroe (Reference Monroe1981) and Frick et al. (Reference Frick, Zardus and Lazo-Wasem2010a). For instance, Hayashi states that ‘Monroe (Reference Monroe1981) regarded S. elegans as a junior synonym of S. praegustator’. First, nowhere in Monroe (Reference Monroe1981) does the author suggest or provide data that indicates that S. elegans is a junior synonym of S. praegustator. Second, because S. elegans was described before S. praegustator, it would be impossible for S. elegans to become a junior synonym (Pilsbry, Reference Pilsbry1916). The species S. elegans takes nomenclatural priority over S. praegustator.

Hayashi (Reference Hayashi2011) states that Frick et al. (Reference Frick, Zardus and Lazo-Wasem2010a) ‘described the neotype specimens of S. praegustator and S. elegans’; Hayashi's statement is incorrect. Frick et al. (Reference Frick, Zardus and Lazo-Wasem2010a) designate and describe a neotype specimen only for S. elegans. This was done because, in opposition to the Code instated by the ICZN, Monroe & Limpus (Reference Monroe and Limpus1979) declared S. elegans a nomen dubium, and renamed the species S. dermochelys. Frick et al. (Reference Frick, Zardus and Lazo-Wasem2010a) clearly demonstrated this error and rectified the situation by correctly declaring S. dermochelys a nomen dubium and reinstating the epithet S. elegans in accordance to the rules of the Code. Such was clearly stated within Frick et al. (Reference Frick, Zardus and Lazo-Wasem2010a), yet, Hayashi (Reference Hayashi2011) (within his discussion on page 18 therein) refers to S. dermochelys as a ‘special parasite’ of leatherback turtles, Dermochelys coriacea (there are no parasitic coronuloids).

Because Hayashi (Reference Hayashi2011) recognizes both S. elegans and S. dermochelys as two distinct species belonging to the genus Stomatolepas, it is clear that he does not understand that these are simply two names for the same species. Again, S. elegans is the correct name for the species in question, and it is not confined solely to leatherback turtles (Frick et al., Reference Frick, Zardus and Lazo-Wasem2010a). Molecular analyses would undoubtedly aid in clarifying evolutionary relationships within the genus Stomatolepas, and some species may, in fact, be synonymous, or new species may await discovery, but as to the identities of S. elegans and S. dermochelys, Monroe & Limpus (Reference Monroe and Limpus1979) simply changed the name provided by Costa (Reference Costa1840) from ‘elegans’ to ‘dermochelys’. The confusion is purely nomenclatural and the epithet Stomatolepas dermochelys Monroe & Limpus, Reference Monroe and Limpus1979 is inarguably a junior synonym of Stomatolepas elegans (Costa, Reference Costa1840). It is also possible, as stated above, that the type species for the genus Stomatolepas, S. praegustator, is a junior synonym of S. elegans. Furthermore, it should also be noted that while Hayashi (Reference Hayashi2011) cites Frick et al. (Reference Frick, Zardus and Lazo-Wasem2010a), the study is missing from the ‘References’ section of his paper.

CORONULOID FAMILY—GROUP NAMES

Hayashi's (2011) statement that the subfamilies Cylindrolepadinae, Stomatolepadinae, Chelolepadinae, Cryptolepadinae and Tubicinellinae (all erected and described by Ross & Frick, Reference Ross and Frick2007) are invalid according to Article 9 of the Code is correct. These family-group names have been amended and they now represent valid taxa within the Coronuloidea (Ross & Frick, Reference Ross and Frick2011). Additionally, a recent study by Harzhauser et al. (Reference Harzhauser, Newman and Grunert2011) reports and describes a new coronuloid genus, Protochelonibia Harzhauser & Newman, 2011, and subfamily, Protochelonibiinae Harzhauser & Newman, 2011 under the family Chelonibiidae Pilsbry, Reference Pilsbry1916.