|Constancea 83, 2002|
University and Jepson Herbaria
P.C. Silva Festschrift
The complex nomenclatural relationship of the Hawaiian species Cladophora tildeniae Brand in Tilden, Cladophora tildeniae Brand, and Cladophora hawaiiana Tilden is evaluated, with the latter deemed the appropriate name. Microdictyon japonicum var. laxum Gilbert is regarded as a synonym.
The marine benthic algal flora of the Hawaiian Islands has, historically and recently, received a great deal of attention, both from indigenous Hawaiians as a source of food, and from phycologists as a source of interesting and novel taxa. One outcome of this attention has been the publication of the Marine Red Algae of the Hawaiian Islands (Abbott 1999), the first major algal flora for the Central Pacific. This volume is intended to be the first of a series that will eventually also include the brown algae and the green algae.
During the preparatory research for the future volumes, some nomenclatural and taxonomic problems arose that could not be dealt with in detail in the flora proper. These include a new combination and clarification of some nomenclatural matters; one of the latter will be dealt with herein.
The name Cladophora tildeniae Brand (as tildenii) first appeared in Tilden's American Algae, no. 541 (1902). Brand, who had received dried and liquid-preserved specimens of Pacific Cladophoraceae from Tilden, published a complete description of the species (Brand 1904, p. 186). He included the following three features that he considered characteristic of the species: (1) a fan-shaped thallus; (2) conspicuous rhizoids that are not produced laterally from the axis but as basipetal projections from lower cells of the main axis; (3) scattered apical fusions of ultimate laterals to cells of lower-order laterals, as occur in Microdictyon.
Unfortunately none of these features are evident in the specimens that were circulated (as no. 541) in Tilden's American Algae exsiccatae under the name of Cladophora tildenii Brand. In fact, this number represents a freshwater species of Cladophora collected from Pearl City, Oahu, that was designated by Brand (1904) as Cladophora (Spongomorpha) longiarticulata Nordstedt var. valida Brand, but later identified by Tilden as C. canalicularis (Roth) Kützing, a species that is presently considered to be a synonym of C. glomerata (L.) Kützing (Guiry and Nic Dhonncha 2002). A specimen of this entity from Tilden's collection (no. 541) is preserved in the Bishop Museum (#531869), Honolulu, and has been examined. It is a sparsely branched plant, with subdichotomies every 1-9 cells. Cells are 270-540µm long by 135-160µm diam., tapering to 45µm diam. near the apex. The morphology of this specimen is clearly not the same as that described by Brand for Cladophora tildeniae (1904) and it is probably correctly identified as C. glomerata, a species that is common in Hawaiian streams (Sherwood, pers. comm.). Cladophora tildeniae Brand in Tilden (1902) is therefore not the same as Cladophora tildeniae Brand (1904). Moreover, as Cladophora tildeniae Brand (1904) is a later homonym of Cladophora tildeniae Brand in Tilden (1902), it has to be rejected.
Tilden realized that an error had been made, and in Fascicle 7 of the American Algae (1909) she placed C. tildeniae Brand (1904, p. 186, referred to as in manuscript by Tilden; non C. tildeniae Brand in Tilden 1902) in synonymy with her new Cladophora hawaiiana Tilden, nos. 615-616. Tilden's treatment of this species suggests, without specifically stating, that she was proposing a substitute name for C. tildeniae sensu Brand. The type of this species would therefore be the Brand specimens, which unfortunately appear to be lost. Herein we lectotypify the species on Brand's figures (1904, figs. 24-27, reproduced as our Fig. 1), which are sufficiently detailed to characterize the species.
To further complicate matters, the specimens distributed by Tilden as C. hawaiiana (no. 615) apparently do not agree with Brand's description (Silva, pers. comm.), and their actual identity is yet to be ascertained. We have not examined these specimens, which were collected at Lâie, Oahu Island, a marine locality.
Two additional taxa need to be considered in relation to C. hawaiiana, the first being Microdictyon japonicum var. laxum Gilbert (1962, p. 139, figs. 5:C, D; 6:C) from Maui, Hawaiian Islands. Gilbert's variety displays the defining characteristics of C. hawaiiana and, based on his description, is considered by us to represent that species. The second entity is Rhipidophyllon reticulatum (Askenasy) Heydrich (type locality: Dirk Hartog Island, Western Australia), which Børgesen's (1924) description from Easter Island populations indicates have lateral filaments that are distinctly gathered at the apices of the subtending cells and are always upwardly directed, unlike the spreading laterals of Cladophora hawaiiana. In addition, the lateral branches of Rhipidophyllon reticulatum apparently always arise and stay in one plane (Børgesen 1924, p. 252), whereas occasional branches of C. hawaiiana do not.
Cladophora hawaiiana also displays many of the features of the widespread Willeella ordinata Børgesen 1930 (see Itono, 1970; Hoek and Rios 1972). Willeella was reduced to a (possibly monospecific) section of Cladophora by Hoek (1982), but recently Silva et al. (1996) have supported its recognition. Similarities between the two species include their branching pattern and the production of closely adpressed, descending rhizoids from the bases of lower lateral branches. However, while Cladophora hawaiiana does produce several laterals of equal length from each node, these do not arise synchronously (as do those of Willeella) and are therefore more Cladophora-like. Kraft and Millar (in Kraft 2000, p. 548) have recently described a species of Cladophora (C. willeelloides), that has characteristics similar to C. hawaiiana, and we follow their interpretation that such plants should be maintained in Cladophora. In addition to the non-synchronous production of laterals, those authors highlighted several additional characters of C. willeelloides that differed from Willeella ordinata, including paired, non-rostrate ostioles in zooidangia. Zooidangia in Cladophora hawaiiana, like C. willeelloides, produce raised pores, further reinforcing the distinction between the two species and Willeella. Cladophora hawaiiana differs from C. willeelloides in the presence of occasional anastomoses between branches and absence of long internodes. Intercalary divisions in C. hawaiiana are rapidly followed by the initiation of lateral branches, such that internodes are generally only one-celled (rarely up to four cells long), in contrast, internodes in C. willeelloides can be up to 14 cells long (Kraft 2000).
The distinctions between several of the cladophoralean genera are not clearly drawn. Cladophora includes species with free branches but also several with secondary anastomoses (e.g., sections Boodleoides van den Hoek and Repentes Kützing, see Hoek and Chihara 2000). Secondary anastomoses are also present in genera such as Microdictyon, Phyllodictyon, and Boodlea, and their occasional presence in C. hawaiiana no doubt led Gilbert to recognize the entity as a Microdictyon. Of those genera, Boodlea has branches in three dimensions, resulting in a spongiose thallus, whereas branching in Phyllodictyon is planar. The two genera can be distinguished from Cladophora by the presence of regular anastomoses and the occasional presence of specialized tenaculae at the junctions between anastomosing cells (Kraft and Wynne 1996). Microdictyon is primarily distinguished from Cladophora by its planar thallus with secondary anastomoses, but both features are also found in Cladophora to some degree, although apparently not in combination. Hoek and Chihara (2000, fig. 4) illustrated the phylogenetic relationships of the genera of the Cladophorales (based on gene sequence studies of Bakker et al. 1994) and, indeed, Microdictyon was shown to be closely related to Cladophora section Boodleoides, leading to the hypothesis (earlier proposed by Hoek 1982, 1984) that Microdictyon evolved by the flattening of an ancestor with a morphology similar to Cladophora liebetruthii Grunow (i.e., with secondary anastomoses and branching in three dimensions). Hoek and Chihara (2000, p. 19) also regard Cladophora as paraphyletic, but a reorganization of the genus was postponed until further sequence data became available. Thus the distinction between Cladophora and Microdictyon is possibly arbitrary. Where, then, should C. hawaiiana be placed? At present the distinction between Microdictyon and Cladophora appears to be one of degree; if the thallus is planar with regular secondary anastomoses then the plant is a Microdictyon; if the thallus is planar without anastomoses, or spongiose with anastomoses, it is a Cladophora. We propose to retain C. hawaiiana in Cladophora based on the thallus architecture and scarcity of lateral fusions. Until genetic analyses demonstrate clear generic boundaries it would seem prudent to maintain the current placement. Further study is clearly warranted to clarify the relationships of these genera.
The stipe-like lower cells with descending rhizoids and lateral branches with steeply inclined cross-walls at nodes suggest that Cladophora hawaiiana should be placed in Cladophora section Rugulosae Sakai. Of the species included in that section, none are described as having secondary anastomoses (Hoek and Chihara 2000; Hoek 1963, as section Longi-articulatae Hamel p.p.). While there are sections of Cladophora for which secondary anastomoses have been recorded (e.g., Boodleoides and Repentes), none have branching architectures like that of C. hawaiiana. Based on gene sequence data (Bakker et al. 1994), Cladophora sections Rugulosae, Boodleoides, and Repentes, and Microdictyon are closely related (Hoek and Chihara 2000, fig. 4). The alignment of section Rugulosae (represented by Cladophora prolifera (Roth) Kützing) with these morphologically seemingly distant taxa was unexpected (Hoek and Chihara 2000, p. 19), but the secondary anastomoses in C. hawaiiana would appear to provide a link between them.
Based on our observations we present the following characterization of Cladophora hawaiiana Brand.
Cladophora hawaiiana Tilden, American Algae 7, nos. 615, 616, 1909.
Lectotype: Brand 1904, plate VI, figures 24-27 (reproduced as our Fig. 1) (type locality: "ad litora arenosa ins. sandwicens." [sandy shore, Hawaiian Islands]).
Cladophora tildeniae Brand, Beih. Centralbl. 18, pp. 186-187, pl. 6, figs. 24-27, 1904; nom. inval., non C. tildeniae Brand in Tilden, Tilden American Algae 6, no. 541, 1902. [=C. glomerata (L.) Kützing, fide Tilden 1909, as C. canalicularis (Roth) Kützing].
Microdictyon japonicum var. laxum Gilbert, Pacific Science 16, p. 139, figs. 5: C, D; 6. (1962).
Specimens examined: Oahu: (1). Kaena Pt, J. Newhouse, WJN 2103, BISH 651438. (2). Ke-awa-ula (Yokohama Bay) Magruder, WHM 605, BISH 653055. (3). Lanai lookout, Halona, HMA 425, BISH 648526. Hawaii: (4). Liliuokalani Gardens Pond, Hoyle 812, BISH 636077. Molokai: (5). Kalaekapu Point, HMA 500, BISH 628824. (6). Moku Islet Site LVII, HMA 1773, BISH 625020. (7) Kalaupapa, north of lighthouse, Magruder, WHM 814, BISH 653276.
Habit and Vegetative Structure: Plants 1.5-3 cm tall, dark green, with several fan-like fronds arising from a common rhizoidal holdfast; each frond with lower cells bearing strong, non-septate, uniseriate rhizoids (Fig. 3) from the basal poles, these coiling around each other downward for 3-4 mm; lower cells of axes cylindrical, 80-200 µm diam, 2-6 times longer, with apical ends frequently widening and becoming clavate ('club-shaped') (Fig. 1); upper cells of axes 50-80 µm diam.; apical cells with rounded ends. Branching opposite or flabellate, with most nodes initially bearing 2 or 4 opposite lateral branches (Figs. 1, 2), these eventually becoming indistinguishable from primary axes and appearing flabellate with five branches per node; lateral branches bearing l-4-celled branchlets either adaxially or abaxially, with each of the penultimate orders bearing 1-2-celled branchlets, either opposite or occasionally secund. Intercalary divisions in primary axes present, resulting in internodes 2 cells in length, but these obscured by rapid initiation of adventitious laterals. Adventitious laterals often remaining short, 1-2 cells in length, those in the inner, lower portions of some plants occasionally forming terminal attachments to a cell of an adjacent branch (Fig. 4).
Reproduction: Brand (1904, reproduced in Fig. 1) illustrated empty zooidangia, each with a raised, distal pore. Identical reproductive structures were observed in several specimens (e.g., BISH 653276, BISH 648426) from recent collections.
We would like to thank Dr. Paul Silva (University of California Berkeley) for nomenclatural guidance and the David and Lucile Packard Foundation for support of this and other algal studies.