BULLETIN OF MARINE SCIENCE, 74(2): 401–421, 2004 NEW TAXA PAPER
TAXONOMY, CIRCUMSCRIPTION, AND USAGE IN ANTHOPLEURA (CNIDARIA: ANTHOZOA: ACTINIARIA) FROM THE GULF OF MEXICO AND CARIBBEAN
Marymegan Daly and J. C. den Hartog
ABSTRACT Inadequate descriptions and diagnoses of representatives of the sea anemone ge- nus Anthopleura from the Gulf of Mexico and Caribbean have led to confusion about species identity. Multiple names have been applied to a single species, and the same name has been used for multiple species, obscuring the distinction between species and confusing accounts of anatomy, life history, and ecology. Because Anthopleura krebsi Duchassaing and Michelotti, 1860, the type species of the genus, is among these spe- cies, reconciling taxonomy, anatomy, and biology is essential. We conclude from our investigation of live specimens, museum collections, and published records that the sea anemones in the Gulf of Mexico and Caribbean that have been considered members of Anthopleura belong to four valid species: A. krebsi, Anthopleura pallida Duchassa- ing and Michelotti, 1864, Anthopleura texaensis (Carlgren and Hedgpeth, 1952), and Isoaulactinia stelloides (McMurrich, 1889). We redescribe these species, providing differential diagnoses that use characters visible in the field and those evident after preservation; we also identify synonyms and reconcile published records of these spe- cies with our circumscriptions. Although all of the features that have been proposed as defining or diagnosing Anthopleura are seen in A. krebsi, a comprehensive study of spe- cies in Anthopleura, Aulactinia, Bunodactis, Bunodosoma, and Gyractis is necessary to evaluate the systematic value of currently used characters.
Accurate accounts of the biology of an organism or of the biodiversity of a region de- pend on correct and consistent taxonomy. Discrepancies between the attributes of speci- mens to which a name is applied, and the definition of that name can lead to confusion about the variability of a species. Inaccurate or inappropriate application of names con- founds attempts to assemble information about these species and thwarts assessments of knowledge of an animalʼs biology. In the sea anemone genus Anthopleura, changes in nomenclature and circumscription have led to confusion about the identity of many species, including the type species of the genus, Anthopleura krebsi Duchassaing and Michelotti, 1860. Because A. krebsi is the type species of Anthopleura, clarifying usage and accurately documenting the histology, anatomy, and nematocyst signature of this species is essen- tial for resolving genus-level taxonomic problems. The definition and composition of Anthopleura have changed over time as the anatomy and variability of its constituent species have become known in greater detail (e.g., Verrill, 1869; McMurrich, 1889, 1901; Carlgren, 1949; England, 1987). In his catalog of the Actiniaria, Corallimorpharia, and Ptychodactiaria, Carlgren (1949) cited 29 species as belonging to Anthopleura; seven species have since been transferred from other genera, based on more complete informa- tion about anatomy and cnidom (e.g., Parry, 1951; Hand, 1955; Mathew, 1967; Schmidt, 1972; England, 1987). Anthopleura has been confused with and is in partial synonymy with Aulactinia Verrill, 1864, Gyractis Boveri, 1893, Bunodactis Verrill, 1899, and Bu- nodosoma Verrill, 1899 (e.g., Carlgren, 1949; Hand, 1955; Dunn et al., 1980; England, 1987; den Hartog, 1987); amendments to the definition of Anthopleura have been tar- geted towards more clearly differentiating it from these genera (e.g., Carlgren, 1949;
Bulletin of Marine Science 401 © 2004 Rosenstiel School of Marine and Atmospheric Science of the University of Miami 402 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 2, 2004
England, 1987; Belém and Pinto, 1990). We reexamine criteria proposed as diagnostic for Anthopleura in light of our redescription of A. krebsi and discuss how well these criteria distinguish Anthopleura from its allies. The implications of inappropriate application of species names for specimens of An- thopleura from the Gulf of Mexico and Caribbean extend beyond taxonomy. Specimens attributed to these species have been used in studies of phylogeny and biogeography (e.g., McCommas, 1983, 1991; Geller and Walton, 2001), anatomy (e.g., Bigger, 1976, 1982; Belém and Pinto, 1990; Belém et al., 1996), and behavior (e.g., Bigger 1976, 1980). These studies are compromised because the specimens used may not belong to the species whose name was applied to them. GenBank contains sequences for 16S and cytochrome c oxidase subunit III genes from A. carneola (AF375806 and AF375791, respectively); unless the name associated with molecular sequence data is accurate, the results of sequence studies cannot be corroborated or used to interpret the evolution of life history or anatomy. Five species epithets have commonly been used for species of Anthopleura from the Gulf of Mexico and Caribbean: A. krebsi; A. carneola (Verrill, 1905); A. catenulata (Verrill, 1905); A. pallida Duchassaing and Michelotti, 1864; and A. varioarmata Watzl, 1922. Two other species that belong to genera often confused with Anthopleura, Buno- dactis texaensis Carlgren and Hedgpeth, 1952, and Isoaulactinia stelloides (McMur- rich, 1889), are also found in this region. In fact, two species originally described as subspecies of the species now called I. stelloides, Bunodactis stelloides catenulata Ver- rill, 1905, and Bunodactis stelloides carneola Verrill, 1905, are considered species of Anthopleura (e.g., Cairns et al., 1986). In addition, the name Aulactinia stella (Verrill, 1864), which belongs to a species considered a member of Anthopleura by some authors (e.g., Uchida, 1938, 1941), was applied to sea anemone specimens from the Caribbean (Duerden, 1897), although Verrill (1899) considered Duerdenʼs use of the name a misap- plication. McCommas (1983, 1991) used the name Anthopleura stellula (Hemprich and Ehrenberg, 1834), which refers to a Red Sea and tropical Indo-Pacific species, for speci- mens collected in Puerto Rico. In this paper, we attempt to disentangle circumscription, name usage, and taxonomy of the species of Anthopleura from the Gulf of Mexico and Caribbean. To accomplish this, we determine the number of species, identify the valid name for each species, and reconcile published records with the appropriate name. We find that the nine names used for members of Anthopleura from the Gulf of Mexico and Caribbean can be attributed to four species: A. krebsi, A. pallida, A. texaensis, and I. stelloides. We redescribe these species, synthesizing published information for senior and junior synonyms. Because the internal anatomy and histology of A. pallida has never been de- scribed in detail, we furnish additional details about this species. Anthopleura krebsi, A. pallida, A. texaensis, and I. stelloides can be distinguished from one another based on field characteristics like color and posture, and anatomical characteristics like tentacle number, arrangement of verrucae, and the size and distribution of cnidae (Table 1). Be- cause A. krebsi, A. pallida, A. texaensis, and I. stelloides have overlapping ranges and have been confused, we attempt to identify the species to which particular specimens mentioned in previous reports belong; unfortunately, some publications contain insuf- ficient information to determine the identity of the specimens studied. DALY AND DEN HARTOG: TAXONOMY AND USAGE OF ANTHOPLEURA 403 -mastigophores and basitrichs p Holotrichs and basitrichs Cnidae marginal of structures Macrobasic Holotrichs and basitrichs Holotrichs and basitrichs In rows, toIn mid-column rows, Verrucae arrangement In rows, toIn limbus rows, In rows, toIn limbus rows, In rows, toIn limbus rows, Elongate Column shape Stout Stout Stout Pale green to white Column color Cream to light brown Gray to pale pink Pale pink to wine, with red spots 48 96 100 – – – 48 24–48 24 80 Number of tentacles Anthopleura texaensis Table 1. Key to the Key species 1. Anthopleura of Table from the Gulf Mexico and of Caribbean. Species Anthopleura krebsi Anthopleura pallida Isoaulactinia stelloides 404 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 2, 2004
METHODS
We examined preserved museum specimens and newly collected material. We corresponded with collectors and field workers to augment the information on museum labels or in published records because differences in microhabitat, life history, and behavior have proven essential to solving species-level problems in sea anemones (e.g., Fautin and Chia, 1986; Pearse and Francis, 2000). Living specimens of A. krebsi and A. pallida were collected in Sarasota, Florida. A chunk of rock bearing many specimens of both species was removed from just below mean low water at Point of Rocks, Siesta Beach (27º15ʹ45ʺ N, 82º32ʹ59ʺ W; coordinates taken from the National Oceanographic and Atmospheric Administration website
SYSTEMATIC ACCOUNT
Anthopleura Duchassaing and Michelotti, 1860
Actiniidae with well-developed pedal disc. Column with adhesive verrucae arranged in longitudinal rows. Simple, endocoelic marginal spherules containing basitrichs and holotrichs (= acrorhagi) encircle column; spherules may sit inside fosse or atop marginal projections. Fosse deep. Tentacles simple, conical, hexamerously or irregularly arranged, with ectodermal longitudinal muscles. At least two well-developed siphonoglyphs. Mar- ginal sphincter muscle diffuse to circumscript; retractor muscles diffuse or restricted. In adults, numerous or all mesenteries perfect and fertile. Mesenteries more numerous proximally than distally in some specimens. Cnidom: spirocysts, basitrichs, microbasic DALY AND DEN HARTOG: TAXONOMY AND USAGE OF ANTHOPLEURA 405
Figure 1. Anatomy of Anthopleura krebsi. A) External anatomy, contracted live specimen. Dark spots in column cover adhesive verrucae. Scale = 5.0 mm. B) External anatomy, preserved spec- imen. Scale = 5.0 mm. C) Longitudinal section through relaxed specimen, showing marginal projections (Mp) and verrucae (arrow). Scale = 2.5 mm. D) Longitudinal section through distal column, showing marginal sphincter (arrow) and dense pad of holotrichs (H) on oral surface. Scale = 50 μm. b-mastigophores, microbasic p-mastigophores, holotrichs. (Synthesis of Carlgren, 1949; England, 1987; Belém and Pinto, 1990.) Type Material.—Anthopleura krebsi Duchassaing and Michelotti, 1860, St. Thomas, Jamaica; by monotypy.
Anthopleura krebsi Duchassaing and Michelotti, 1860 Figures 1,2
Anthopleura Krebsi Duchassaing and Michelotti, 1860; Carlgren, 1949 Anthopleura Krebsii Duchassaing and Michelotti, 1864; Verrill, 1869, 1871; Andres, 1883 Bunodes krebsii Duerden, 1897 Bunodactis stelloides var. carneola Verrill, 1905 406 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 2, 2004
Figure 2. Representative cnidae from Anthopleura and Isoaulactinia species from the Gulf of Mexico. Source taxon for each illustrated cnida indicated in parentheses; morphology of cnidae differs little among species. Scale = 20 µm, refer to Tables 2–5 for sizes and location of each type. A) Holotrich (A. texaensis). B) Basitrich (A. pallida). C) Spirocyst (A. krebsi). D) Micro- basic b-mastigophore (A. krebsi). The shaft of this type of cnida is slightly flared but lacks the v-shaped notch characteristic of an undischarged microbasic p-mastigophore. E) Small basitrich (I. stelloides). F) Basitrich (A. krebsi). G) Microbasic p-mastigophore (A. pallida). H) Holotrich (A. texaensis). I) Holotrich (A. pallida). J) Long, thin basitrich (I. stelloides). K) Microbasic b- mastigophore (A. texaensis). L) Macrobasic p-mastigophore (I. stelloides).
Anthopleura varioarmata Watzl, 1922 Anthopleura krebsi Carlgren and Hedgpeth, 1952; Hedgpeth, 1954; Bigger, 1976, 1980, 1982; Hererra Moreno, 1981; Belém and Pinto, 1990; Pires et al., 1992; Gomes et al., 1998; Zamponi et al., 1998 Anthopleura carneola McCommas, 1983, 1991; Ruppert and Fox, 1988; Cairns et al., 1986; den Hartog, 1994 non Anthopleura varioarmata Carlgren, 1952; Belém and Monteiro, 1981
Diagnosis.—Anthopleura with 24–48 tentacles; pale pink to red column with darker red spots atop verrucae to limbus. Type Material.—None known. Duchassaing and Michelotti (1860) did not name type specimens, and we have been unable to locate museum material from the type local- ity of St. Thomas, Jamaica with a date of collection appropriate to Duchassaing and Michelottiʼs (1860) original description. Material Examined.—Caribbean Sea: Galatea Reef (NNM 11270); Playa Boca Canoa (NNM 11290, 11300), Aruba: Colorado Point (NNM 11278); Kudarebe (NNM 10997); North Coast (NNM 11269) Bermuda: Hamilton, Shelly Bay (NNM 10993, 11292, 11293); St. George (NNM 11271); Smithʼs Bay (NNM 11301) Bonaire: Lac (NNM 255); Little Bonaire (NNM 10998) Curaçao: (NNM 11267); Awa Blancu (NNM 268); Playa Kalkie (NNM JCdH 236); Oostpunt (NNM 10999, 11307; JCdH 261) Florida: Sarasota (KUMNH 1622) Saba: Cove Bay (NNM 11305) External Anatomy.—Column cylindrical, generally taller than wide, pedal disc diam- eter 5.0–12.5 mm, column height 5.0–15.0 mm (Fig. 1A,B); pale pink to wine-colored in life, paler after preservation. Column flecked with darker red spots (Fig. 1A); spots DALY AND DEN HARTOG: TAXONOMY AND USAGE OF ANTHOPLEURA 407 3.2–6.2 4–7.6 3.2–5.6 3.2–4.8 1.6–4 × × × × × 1.6–4 1.6–4 1.6–3.2 2.4–7.2 2–4.8 3–4.2 1.6–4.2 1.2–2.8 × × × × × × × × Belém & Pinto, 1990 12–22.4 12.8–22 10.4–16 30–44.8 15.2–21.7 16.8–23.2 8–15.6 19.2–48 18.2–21.6 20.8–28.8 14–20.8 11.2–19.2 11.2–19.2 11–25.6 4.2-5.6 1.5-2.5 2.2-2.8 4.5-5 4.2-4.5 × × × × × 2.5-2.8 3-3.5 5 5-5.6 × × × × Carlgren & Hedgpeth, 1952 15.5-18.3 12.7-15.5 32.4-43.7 16.5-19.7 17-19.7 21-25.4 19.7-21 17-19.7 18.3 –28.2 p -mastigophore by Belém and Pinto (1990). Letters 2.0–4.4 2.1–5.7 × (1.7) 2.0–3.8 × × 1.7–4.2 (4.7) 4.6–6.9 2.6–4.2 (5.9) 2.8–5.5 3.7–5.7 (6.5) 2.3–3.8 1.8–2.6 (2.3) 3.9–5.1 3.6–4.7 2.2–4.1 1.5–3.6 1.8–3.7 × × × × × × × × × × 2.9–4.7 × × × 11.7–21.4 (28.2) 11.7–21.4 (9.9) 11.4–21.1 Present study 10.5–29.8 7.3–16.8 32.2–59.7 20.0–39.9 (7.0)12.3–20.0 12.8–19.6 8.0–18.2 19.1–25 16.5–20.4 10.3–16.4 28.9–44.3 14.4–21.0 17.7–26.8 12.3–18.9 b -mastigophore II” was called a microbasic . Length krebsi by width measurements (in µm) are presented as ranges, with exceptionally small or large
-mastigophore (G) -mastigophore (G) -mastigophore (K) -mastigophore II (D) p p b b Anthopleura Cnidae type Spirocyst (C) Basitrich (F) Basitrich (F) Holotrich I (H) Holotrich II (I) Basitrich (F) Holotrich III (A) Basitrich (F) Holotrich III Basitrich (B) Microbasic Small basitrich (A) Long, curved basitrich (J) Microbasic Microbasic Microbasic measurements given in parentheses. Cnidae of the same general that differ in size or morphology are designated by roman numerals. The nematocyst we identify as “microbasic Table 2. Cnidae of Table refer to Figure 2. Tissue Spherule Upper column Limbus Actinopharynx Filament Tentacle 408 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 2, 2004
irregularly placed proximally, correspond to verrucae distally. Verrucae simple, cup- shaped, endocoelic, in 18–24 rows to limbus; those of distal column larger, denser, more prominent, red or dark pink in life, typically colorless after preservation. Verrucae of distal column margin atop conical projections (Fig. 1C); oral surface of marginal projec- tion bears swollen acrorhagus (Fig. 1D). In living specimens, acrorhagus opaque white, tinged with pink; in preserved specimens, acrorhagus opaque, same color as column. Oral disc pinkish tan, with irregularly spaced white lines radiating from mouth. Tentacle pinkish tan, with small, opaque white cross marks on oral side. Adoral base of tentacle may be marked with opaque white streak, streak may extend onto upper column. Ten- tacles 24–48, in three cycles, innermost cycle longest. Internal Anatomy.—Marginal sphincter endodermal, diffuse to circumscript-diffuse (Fig. 1D). Actinopharynx long, deeply sulcated, with two aborally prolonged siphong- lyphs, each attached to a pair of directive mesenteries. Mesenteries hexamerously ar- ranged in three cycles, those of third cycle more developed proximally than distally (arrangement may be obscured by longitudinal fission). Mesenteries of first two cycles perfect, with large oral and marginal stomata; mesenteries of third cycle imperfect. Gonochoric; all mesenteries of first two cycles fertile; directives may be sterile in small specimens. Both retractor and parietobasilar muscles diffuse; on larger mesenteries, ac- cessory muscles lie between retractor and parietal muscles. Basilar muscles strong. Cnidom.—Gracile spirocysts, basitrichs, holotrichs, microbasic b-mastigophores, mi- crobasic p-mastigophores (Fig. 2). See Table 2 for size and distribution. Natural History.—Zooxanthellate, intertidal to shallow subtidal. Undergoes longitu- dinal fission. Shell debris and pebbles adhere to verrucae, giving A. krebsi its common name “the armored anemone” (Ruppert and Fox, 1988). Taxonomic Remarks.—Cairns et al. (1986) were the first to recognize that the speci- mens described by Watzl (1922) as Anthopleura varioarmata belong to A. krebsi. Carlgren (1952) and Belém and Monteiro (1981) applied the name A. varioarmata to specimens of Anthopleura with 96 tentacles. We provisionally refer these specimens to A. texaensis (see below).
Anthopleura pallida Duchassaing and Michelotti, 1864 Figures 2,3
Anthopleura pallida Duchassaing and Michelotti, 1864; Verrill, 1869; Andres, 1883; Carlgren, 1949; McCommas, 1983, 1991 Actinioides pallida Duerden, 1897; Verrill, 1900, 1907; Pax, 1907 Aulactinia stelloides var. catenulata Verrill 1905 Anthopleura catenulata Cairns et al., 1986 non Anthopleura pallida (Boveri, 1893) Carlgren, 1949
Diagnosis.—Anthopleura with 24–48 tentacles, elongate, pale-green to white column, with white verrucae extending halfway down the column. Oral side of tentacle with lon- gitudinal opaque stripe and opaque white crossbars. Type Material.—None known. Duchassaing and Michelotti (1864) did not specifically name type specimens, and we have been unable to locate any material from the type locality of St. Thomas, Jamaica with a date of collection appropriate to Duchassaing and Michelottiʼs (1864) original description. Material Examined.—Florida: Cross Key (NNM 32304); Sarasota (KUNHM 1623) External Anatomy.—Column cylindrical, generally taller than wide, pedal disc diam- DALY AND DEN HARTOG: TAXONOMY AND USAGE OF ANTHOPLEURA 409
Figure 3. Anatomy of Anthopleura pallida. A) External anatomy, live specimen. Note markings on tentacles and white marginal projections just proximal to tentacle crown. Scale = 3.0 mm. B) External anatomy, preserved specimen. Scale = 3.0 mm. C) Longitudinal section through distal column, showing marginal sphincter muscle (arrow). Scale = 50 μ. D) Cross section through marginal projection. Note dense pad of holotrichs (H) on oral surface. Scale = 70 μm. E) Basilar muscles. Scale = 40 μm. F) Longitudinal section through verruca. Scale= 200 μm. G) Cross-sec- tion of a mesentery, showing retractor (R) and parietal (P) muscles; pennon of parietal muscle indicated with an arrow. Scale = 0.5 mm. 410 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 2, 2004
eter 5.0–10.0 mm, column height 5.0–15.0 mm; pale gray to greenish in life, paler after preservation (Fig. 3A,B). Marginal exocoelic spaces marked with small, opaque white patches. Verrucae simple, cup-shaped, endocoelic, extend halfway to limbus in 12–24 rows, 6–12 verrucae per row. Verrucae (Fig. 3F) relatively narrow in diameter compared to those of A. texaensis of A. krebsi; same color as column, central depression opaque white, colorless after preservation; those of distal column larger, denser, more promi- nent, atop conical projections at distal margin. Marginal projection bears approximately three verrucae on adoral surface; oral surface bears swollen, opaque acrorhagus (Fig. 3A,D) that contains holotrichs. Oral disc pale green or white to dark gray. Oral side of tentacle typically marked with single longitudinal opaque white stripe and several opaque white crossbars or chevrons; adoral side typically unmarked (Fig. 3A). Tentacles filiform, 24–48, in three cycles, tentacles of innermost cycle longest. Internal Anatomy.—Marginal sphincter endodermal, small, circumscript-diffuse (Fig. 3C). Actinopharynx long, deeply folded and grooved, with two aborally prolonged si- phonoglyphs each attached to a pair of directive mesenteries. Mesenteries hexamerously arranged, in three cycles. Mesenteries of first two cycles perfect, with large oral and mar- ginal stomata. Retractor muscle restricted, nearly reniform, without accessory muscles (Fig. 3G). Parietobasilar muscle diffuse; tall and narrow, of approximately equal width along its length, with short free flap (= pennon; Fig. 3G). Basilar muscle small, with few, short branches (Fig. 3E). Gonochoric, mesenteries of first two cycles except directives perfect and fertile. Cnidom.—Spirocysts, basitrichs, holotrichs, microbasic b-mastigophores, microbasic p-mastigophores (Fig. 2). See Table 3 for size and distribution. Natural History.—Azooxanthellate, intertidal to shallow subtidal, in crevices; pedal disc attaches to sides and bottom of crevices. Broadcast spawns. No evidence of asexual reproduction: specimens do not live in dense aggregations and all examined specimens lack fission scars or internal anatomical irregularities. Taxonomic Remarks.—Cairns et al. (1986) recognized A. catenulata and A. pallida as synonyms but chose to call the species A. catenulata, possibly to avoid confusion with Anthopleura pallida (Boveri, 1893), a subjective junior homonym of A. pallida Duchas- saing and Michelotti, 1864 (see Carlgren, 1949). However, A. pallida Duchassaing and Michelotti, 1864 has priority over A. catenulata (Verrill, 1905), and is thus the valid name (Art. 23: International Commission on Zoological Nomenclature, 1999). Hom- onymy between A. pallida Duchassaing and Michelotti 1864, and A. pallida (Boveri, 1893) has been eliminated, as England (1987) synonymized A. pallida (Boveri, 1893) with Gyractis excavata Boveri, 1893.
Anthopleura texaensis (Carlgren and Hedgpeth, 1952), new combination Figures 2,4
Bunodactis texaensis Carlgren and Hedgpeth, 1952; Hedgpeth, 1954; McCommas, 1983, 1991 ?Anthopleura varioarmata Carlgren, 1952; Belém and Monteiro, 1981
Diagnosis.—Anthopleura with 80–100 tentacles, gray to pink column with pale ver- rucae extending from distal margin to limbus. Type Material.—Holotype, Port Aransas, Texas (USNM 49988). DALY AND DEN HARTOG: TAXONOMY AND USAGE OF ANTHOPLEURA 411
Table 3. Cnidae of Anthopleura pallida. Length by width measurements (in µm) are presented as ranges, with exceptionally small or large measurements given in parentheses. Cnidae of the same general that differ in size or morphology are designated by roman numerals. Letters refer to Figure 2. Tissue Cnidae type Present study Tentacle Spirocyst (C) 10.2–22.3 × 1.4–4.4 Basitrich (F) 10.2–20.1 × 2.0–3.8 Spherule Small basitrich (E) 10.5–14.4 × 1.9–3.3 Basitrich (F) 13.5–25.1 × 2.5–3.6 Holotrich I (H) 32.4–68.6 × 4.0–7.5 Holotrich II (I) 30.4–53.1 × 3.6–5.2 Upper column Basitrich (F) 12.2–25.1 × 1.7–3.6 Small basitrich (E) 5.0–12.4 × 1.1–2.4 Holotrich III (A) 13.8–22.4 × 2.7–5.0 Limbus Basitrich (F) 14.9–22.4 × 3.1–3.9 Long, curved basitrich (J) 26.1–42.8 × 1.7–3 Holotrich III (A) 13.2–22.4 × 3.1–5.4 Actinopharynx Basitrich (B) 16.6–26.2 × 2.3–3.6 Small basitrich (E) 9.1–13.1 × 2.1–2.4 Microbasic p-mastigophore (G) 15.4–26.3 × 3.3–5.6 Microbasic b-mastigophore (K) 21.4–27.5 × 3.1–5.4 Microbasic b-mastigophore II (D) 13.8–17.6 × 2.7–3.6 Filament Basitrich (B) 9.4–17.7 × 1.9–3.4 ong, curved basitrich (J) 27.0–46.1 × 1.9–2.5 Microbasic p-mastigophore (G) 14.3–24.7 × 3.0–5.4 Microbasic b-mastigophore (K) 22.4–30.1 × 3.9–5.0 (6.2) Microbasic b-mastigophore II (D) 14.0–19.5 × 2.4–3.9
Material Examined.—Colombia: Cartagena (NNM 10925) Jamaica: (AMNH 586) Puerto Rico: Mayaguëz (NNM 10927); Quebrada Honda (NNM 10926) Texas: Port Aransas (USMN 49988, 50010) Virgin Islands: St. Thomas (USNM 54235) External Anatomy.—Column cylindrical, oral disc generally greater than or equal to pedal disc in diameter, pedal disc diameter 10.0–30.0 mm, column height 7.5–25.0 mm (Fig. 4A); column gray to pink (Carlgren and Hedgpeth, 1952), paler after preservation. Column with approximately 48 rows of simple, cup-shaped endocoelic verrucae; most rows extend to limbus. Verrucae translucent, paler than column, those of distal column larger, denser, more prominent, atop conical projections at margin (Figs. 4A,C). Oral surface of marginal projection bears opaque acrorhagus (Fig. 4B). Oral disc unmarked in preserved specimens. In many preserved specimens, oral side of tentacle darker than adoral side, with pigmented chevrons and crossbars. Tentacles 80–100, in four cycles, tentacles of innermost cycle longest. Internal Anatomy.—Marginal sphincter endodermal, circumscript, palmate (Fig. 4D). Actinopharynx long, deeply folded and grooved, with two aborally prolonged sipho- noglyphs each attached to a pair of directive mesenteries. Mesenteries hexamerously arranged, in four cycles (Fig. 4E; but see Belém and Monteiro, 1981 for discussion of anatomical irregularities resulting from longitudinal fission). Mesenteries of first three cycles perfect, with large oral and marginal stomata. Retractor muscle diffuse, with branches of nearly equal height; retractors of larger mesenteries have short free flap on side of muscle closer to body wall. Parietal muscle strong, narrowest at junction with 412 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 2, 2004
Figure 4. Anatomy of Anthopleura texaensis. A) External anatomy, preserved specimen. Scale = 5.0 mm. B) Longitudinal section through marginal projection, showing holotrichs (H) on oral surface of projection. Scale = 70 μ. C) Detail of column margin, showing verrucae (V) atop projection. Scale = 1.0 mm. D) Longitudinal section through distal column, showing strong, pal- mate marginal sphincter muscle. Scale = 150 μm. E) Cross section through column proximal to actinopharynx, showing arrangement of mesenteries. Roman numerals indicate cycle. Fourth cycle mesenteries small, not labeled; lie between those of cycles I and III, and cycles II and III. Scale = 3.0 mm. body wall, becoming broader along its length; both pennon and main lamella of mes- entery opposite it bear secondary branches. Gonochoric, all mesenteries of first three cycles except directives fertile. Cnidom.—Spirocysts, basitrichs, holotrichs, microbasic b-mastigophores, microbasic p-mastigophores (Fig. 2). See Table 4 for size and distribution. Natural History.—Azooxanthellate, intertidal to shallow subtidal. Undergoes longi- tudinal fission. Taxonomic Remarks.—Members of this species have adhesive verrucae and true ac- rorhagi with holotrichs, and thus belong in Anthopleura rather than in Bunodactis. Mem- bers of Bunodactis never have holotrichs in the marginal structures (Carlgren, 1949) or in the column (England, 1987). DALY AND DEN HARTOG: TAXONOMY AND USAGE OF ANTHOPLEURA 413 2–3.3 2.8–5 1.7–2.9 1.7–2.1 2.0–3.3 4.2–5.0 2.5–4.2 × 4.2–5 × 3.5–4.5 2.5–2.8 2.8–3.0 3.6–6.0 × × × × × × × × × × × 1.5–2.8 1981 12.8–17.7 12.8–17.7 24.2 –40 14.4–23.3 14.2–19 28–36.6 15–23.3 13.3–20 7.1–21.4 7.1–21.4 Belém & Monteiro, 17.5–25.7 13.5–15.7 14.4–23.3 12.8–17.7 12.8–23.3 1952 10–14 × 1.5–2 19–26 × 3–3.5 8.5–17 × 1.5–2.5 12.7–21 × 2.2–2.8 17–19.7 × 4.2–5.6 22.6–39.5 × 3.5–5.6 Carlgren & Hedgpeth, 4.8–7.4 3.5–6.0 1.8–3.4 2.0–3.1 2.1–3.4 1.8–3.0 3.2–5.6 2.4–3.8 3.6–6.6 4.2–6.7 1.5–3.4 2.2–3.6 1.2–2.5 1.3–2.9 × 1.7–3.0 × × × × × × × × × × × × 1.6–3.0 × × (1.8) 2.7–5.2 × × Present Study 6–13.8 14–23.6 7.3–14.5 11.6–18.5 11.6–18.5 12.9–24.0 17.0–26.0 40.9–54.1 12.1–21.2 16.2–25.8 16.2–33.3 19.8–26.1 28.8–40.3 8.1–19.21 17.0–25.8 15.0–21.5 46.04–59.6 16.0–26.7 . Length by width measurements (in µm) are presented as ranges, with exceptionally small Cnidae type -mastigophore (G) -mastigophore (G) -mastigophore II (D) p p b A. texaensis Spirocyst (C) Basitrich (F) Basitrich (F) Holotrich I (H) Holotrich II (I) Basitrich (F) Holotrich III (A) Small basitrich (E) Basitrich (F) Holotrich III (A) Small basitrich (E) Basitrich (B) Microbasic Basitrich (B) Small basitrich (E) Microbasic Microbasic Large basitrich Large Tentacles Table 4. Cnidae Table of Hedgpeth (1952). Tissue Spherules Column Limbus Actinopharynx Filaments or large measurements given in parentheses. Cnidae of the same general that differ in size or morphology are designated by designated are morphology or size in differ that general same the of Cnidae parentheses. in given measurements large or roman numerals. Letters refer to Figure 2. Carlgren and Hedgpeth (1952), Belém and Monteiro (1981) did not distinguish between types of holotrichs. We did not find the larger size of basitrichs in the actinopharynx reported by Carlgren and 414 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 2, 2004
The holotype of B. texaensis (USNM 49988) is poorly preserved and heavily dis- sected. Because the margin has been damaged, cnidae could not be sampled from the acrorhagi. However, the column contains small holotrichs, identical in size and morphol- ogy to those in the column of specimens we identified as A. texaensis. Additionally, the anatomy and cnidae of this specimen are identical to those of other specimens attributed to this species.
Isoaulactinia Belém, Herrera, and Schlenz, 1996
Definition.—Actiniidae with well-developed pedal disc. Column with adhesive ver- rucae arranged in vertical rows; verrucae bigger and lobulated distally. Margin den- ticulate, with small, simple, endocoelic, and exocoelic marginal projections that contain basitrichs and macrobasic p-mastigophores. Fosse shallow. Tentacles simple, conical, entacmeaic, with ectodermal longitudinal muscles. Two well-developed siphonoglyphs. Marginal sphincter muscle circumscript to circumscript-diffuse; retractor muscles strong, restricted. Perfect mesenteries fertile. Same number of mesenteries proximally and distally. Cnidom: spirocysts, microbasic b-mastigophores, microbasic p-mastigoph- ores, and macrobasic p-mastigophores. (Reorganized from Belém et al., 1996, so that definition is parallel to that of Anthopleura.)
Isoaulactinia stelloides (McMurrich, 1889) Figures 2,5
Aulactinia stelloides McMurrich, 1889; Hickson, 1889; Carlgren, 1895; Verrill, 1899 Aulactinia stella Duerden, 1897 Bunodella stelloides Verrill, 1899 Bunodactis stelloides Verrill, 1900, 1905, 1907; Watzl, 1922; Pax, 1924; Carlgren, 1949; Lewis, 1960; Corrêa, 1964; McCommas, 1983, 1991 Isoaulactinia stelloides Belém et al., 1996 non Bunodactis stella Verrill, 1864
Diagnosis.—Isoaulactinia with cream-colored column covered to limbus with simple verrucae and 48 or more tentacles. Oral disc with opaque white or cream lines radiating from mouth, tentacles with opaque white or cream crossbars and tips. Type Material.—None known. McMurrich (1889) did not name type specimens, and we have been unable to locate specimens collected from the type locality of the Bahamas with a date of collection appropriate to McMurrichʼs (1889) original description. Material Examined.—Aruba: North Coast (NNM 10921) Bonaire: Playa Grandi (NNM 10918) Colombia: Cartagena (NNM 10925) Curaçao: Spaansche Haven (ZMA Coel 2265) Cuba: Havana (AMNH 1285) Florida: Franklin Co. (USNM 52544) Puer- to Rico: Mayagüez (NNM 10927); Quebrada Honda (NNM 10926); San Juan (NNM 10920) St. Eustatius: Zeelandia (NNM 10917). External Anatomy.—Column cylindrical, oral disc diameter generally greater than or equal to pedal disc diameter, pedal disc diameter 5.0–15.0 mm, column height 10.0–22.5 mm (Fig. 5A); cream to light brown in life (Belém et al., 1996), light tan or paler after preservation. Column with approximately 48 rows of simple, cup-shaped endocoelic ver- rucae; most rows extend to limbus. Verrucae translucent, paler than column, those of distal column larger, denser, more prominent than those of proximal column. Distal most verrucae project slightly above margin; oral surface of fosse without spherule (Fig. DALY AND DEN HARTOG: TAXONOMY AND USAGE OF ANTHOPLEURA 415
Figure 5. Anatomy of Isoaulactina stelloides. A) External anatomy, preserved specimen. Column stout, with verrucae extending from margin to limbus. Scale = 10 mm. B) Detail of distal margin, showing endocoelic and exocoelic marginal projections. Scale = 1.0 mm. C) View of Fig. 5B from above, showing shallow fosse and flat, spherule-less oral surface of marginal projection. Scale = 1.0 mm. D) Longitudinal section through distal column, showing marginal sphincter muscle. Scale = 100 μm. E) Longitudinal section through a tentacle, showing brooded juvenile (arrow). Scale = 1.0 mm. 5B,C). Oral disc and tentacles of preserved specimens unmarked, same color as column. Tentacles 48–96, longitudinally furrowed, perforate, in three or four cycles. Internal Anatomy.—Marginal sphincter endodermal, circumscript, palmate (Fig. 5D). Actinopharynx long, deeply folded and grooved, with two aborally prolonged sipho- noglyphs each attached to a pair of directive mesenteries. Mesenteries hexamerously arranged, in up to four cycles, with first two or three cycles perfect (mesenterial arrange- ment may be obscured by longitudinal fission). Perfect mesenteries with large oral and marginal stomata. Retractor muscles strong, restricted, with branches of approximately equal height; retractor muscles of larger mesenteries with short free flap on side of mus- cle closer to body wall. Parietal diffuse, narrow, tall, with few, short branches and long free flap. Lamella between retractor and parietal muscles with short muscle processes; processes not concentrated into accessory muscle. Simultaneously hermaphroditic, mes- 416 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 2, 2004
Table 5. Cnidae of Isoaulactinia stelloides. Length by width measurements (in µm) are presented as ranges, with exceptionally small or large measurements given in parentheses. Letters refer to Figure 2. The cnidae of the marginal spherule and upper column were sampled separately; the measurements were pooled because cnidae from the upper column and spherule were indistinguishable. We did not find any basitrichs in the tentacles that we could identify with the “opaque basitrichs” of Belém et al. (1996), and were unable to discern two size classes of basitrichs in the tentacles. We infer, based on similarities in morphology and size range, that the “bigger b-rhabdoids” of Belém et al (1996) are equivalent to our Microbasic b-mastigophore. Tissue Cnidae type Present study Belém et al., 1996 Tentacle Spirocyst (C) 13.9–26.0 × 1.5–3.3 (5.1) 10.2–23.8 × 1.4–2.3 Basitrich (F) 13.07–25.2 × 1.8–4.2 14.3–23.8 × 1.4–2.7 Small basitrich 8.8–17 × 1.4–2.7 Opaque basitrich 8.2–19.0 × 1.7–2.7 Macrobasic p-mastigophore (L) 22.3–32.2 × 6.1–11.5 19.7–28.6 × 4.6–9.5 Spherule and Basitrich (F) 9.6–15.5 × 1.8–3.1 9.7–19.3 × 1.4–2.9 distal column Macrobasic p-mastigophore (L) 23.5–28.6 × 6.8–7.7 12.7–38.8 × 4.6–8.6 Limbus Basitrich (F) (10.8) 11.4–17.8 × 1.8–3.5 Long, curved basitrich (J) 24.7–43.8 × 1.2–3.1 Macrobasic p-mastigophore (L) 20.9–32.7 × 6.6–9.5 Actinopharynx Small basitrich (E) 9.8–14.2 × 1.2–2.7 9.1–14.8 × 1.1–2.3 Basitrich (B) 16.2–24.2 × 2.1–3.2 14.5–37 × 2.0–4.3 Microbasic p-mastigophore (G) 22.8–33.1 × 4.5–7.5 Macrobasic p-mastigophore (L) 22.2–27.1 × 6.2–10.5 19.6–26.2 × 4.3–7.4 Filament Small basitrich (E) 9.6–15.0 × 1.7–2.8 9.5–20.5 × 1.4–2.0 Basitrich (B) 17.6–23.2 × 1.8–3.1 15.1–31.4 × 1.4–3.9 Long, curved basitrich (J) 31.9–48.7 × 1.4–2.8 Microbasic p-mastigophore (G) 22.8–33.6 × (4.2) 4.8–7.4 22.4–33.3 × 3.4–6.8 Macrobasic p- mastigophore (L) 23.6–33.0 × 6.0–10.7 21.1–30.6 × 5.4–7.5 Microbasic b-mastigophore (K) 30.2–42.9 × 3.4–5.3 (5.8) 28.6–38.8 × 2.7–4.8 enteries of first two cycles, except directives, fertile; directives and imperfect mesenter- ies sterile. Cnidom.—Spirocysts, basitrichs, microbasic b-mastigophores, microbasic p-mastigo- phores, macrobasic p-mastigophores (Fig. 2). See Table 5 for size and distribution. Natural History.—Zooxanthellate, intertidal to shallow subtidal. Broods internally, coelenteron may contain developing polyps (Fig. 5E).
DISCUSSION
DIAGNOSIS OF ANTHOPLEURA.—The original description of Anthopleura by Duchassaing and Michelotti (1860) was vague, and did not mention acrorhagi or cnidae, two of the characters now used to define the genus (e.g., McMurrich, 1889; Carlgren, 1949; Hand, 1955; England, 1987; Belém and Pinto, 1990). Verrill (1869), McMurrich (1889, 1901), and Carlgren (1949) among others amended the generic definition to clarify the distinc- tion between members of Anthopleura and members of other genera in the Actiniidae. Many of these revisions were made without reference to the type species of Anthopleura, and the criteria have never been applied systematically to all potential species of An- thopleura; consequently, the definition and composition of Anthopleura is confused. We find that members of all of the features that have been proposed as diagnostic for Anthopleura occur in A. krebsi: simple, perforate, adhesive verrucae that are larger and more numerous distally than proximally and simple, conical, marginal projections that DALY AND DEN HARTOG: TAXONOMY AND USAGE OF ANTHOPLEURA 417
bear holotrichous marginal spherules on their oral surface. Anthopleura pallida and A. texaensis share these features with A. krebsi. Because some of these features are also characteristic of other genera in the Actini- idae, England (1987) and Belém and Pinto (1990) suggested that additional characters be used to define Anthopleura. England (1987) noted that the column of a member of Anthopleura contains heterotrichous nematocysts, unlike that of a member of Bunodac- tis, Gyractis, or Aulactinia. Heterotrichs differ from holotrichs in having a tubule that varies in diameter along its length, rather than a tubule of constant diameter (Mariscal, 1974; England, 1987). Belém and Pinto (1990) suggested that morphology of the micro- basic p-mastigophores found in the filaments might reliably distinguish Anthopleura from its allies. Although members of A. krebsi have nematocysts that meet the criteria established by England (1987) and Belém and Pinto (1990), using column heterotrichs or filament microbasic p-mastigophore shape to diagnose Anthopleura is problematic because few authors have recorded cnidom with the precision necessary to use either criteria. Heterotrichs and holotrichs are not easily distinguishable; no author other than England (1987) has made the distinction between the two in describing the cnidom of a species of Anthopleura. The criterion of Belém and Pinto (1990) requires that variation in shape and size of microbasic p-mastigophores of the filaments and actinopharynx be accurately documented and compared. The comparability of measurements taken from different authors using different equipment and different methods, and the appropriate method of comparing sizes or shapes of cnidae between species have yet to be deter- mined (Fautin, 1988; Williams 1996, 1998, 2000). Furthermore, the shape of the micro- basic p-mastigophores in the filaments in some species of Aulactinia, Bunodosoma, and Gyractis (e.g., Dunn et al., 1980; den Hartog, 1987; Belém and Pinto, 1990; den Hartog and Vennam, 1993) is similar to that of A. krebsi, which suggests that this feature does not distinguish members of Anthopleura from those of other genera. Comprehensive studies of the type species of Aulactinia, Bunodactis, Bunodosoma, and Gyractis are necessary to resolve taxonomic questions about the composition and definition of these genera relative to Anthopleura. DIFFERENTIAL DIAGNOSES.—Members of the species of Anthopleura found in the Gulf of Mexico and Caribbean can be distinguished from one another and from members of I. stelloides by several macroscopic features (Table 1). Although preserved specimens lack the color and habitat information that most easily differentiates between of A. krebsi and those of A. pallida, preserved specimens of A. krebsi can be distinguished from those belonging to A. pallida as the verrucae of A. krebsi are more prominent than those of A. pallida, and remain cup-shaped and distinct beyond the longitudinal midline of the column. Microscopic features further distinguish A. krebsi and A. pallida: a member of A. krebsi lacks long, thin basitrichs in the limbus and large microbasic b-mastigophores in the filaments; a member of A. pallida has large microbasic b-mastigophores in the filaments and has long, thin basitrichs in the limbus. RECONCILING AND INTERPRETING PREVIOUS REPORTS.—The specimens identified by Carl- gren (1952) and Belém and Monteiro (1981) as A. varioarmata resemble A. texaensis in many respects: they have the same number of tentacles and mesenteries, similar mar- ginal sphincter muscles, and cnidae of similar size and morphology in most tissues. However, the spherule holotrichs reported by both Carlgren (1952) and Belém and Mon- teiro (1981) are much smaller than those we found in the spherules of specimens of A. texaensis. The holotrichs reported by Carlgren (1952) and Belém and Monteiro (1981) overlap in size range with the holotrichs we found in the distal column. We provisionally 418 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 2, 2004
refer these specimens to A. texaensis, but recognize that the specimens that Carlgren (1952) and Belém and Monteiro (1981) called A. varioarmata may belong to a different, as yet unnamed, species. Although Verrill (1905) clearly recognized Bunodactis stelloides var. catenulata as distinct from B. s. stelloides McMurrich, 1889, his description is insufficient to discrimi- nate between the species now called A. pallida and I. stelloides. Verrill (1905) did not mention marginal spherules, nor are they apparent in his figure 116. Verrill (1905) also did not specify the number of tentacles. Accounts of the biology of B. s. catenulata are similarly confused or lacking. For example, Verrill (1905) reported that B. s. catenulata is viviparous. One of us (JCdH) observed that specimens of A. pallida from Bermuda are oviparous. Verrill (1905) either confused at least some specimens of his B. s. catenulata with those of the species now called I. stelloides, or erroneously attributed characteris- tics of the viviparous I. stelloides to his B. s. catenulata. No voucher specimens are available for the two molecular phylogenetic analyses that include members of Anthopleura from the Gulf of Mexico and Caribbean (S. McCom- mas, Southern Illinois University Edwardsville, pers. comm.; J. Geller, Moss Landing Marine Laboratory, pers. comm.). The collection of the NNM includes specimens of A. pallida (NNM 32304) collected by R. Seaton, who provided specimens for the study by McCommas (1991). The specimens in the NNM were collected at the same location and at approximately the same time as those sampled by McCommas; therefore, it is likely that the samples McCommas (1991) called A. pallida are correctly identified. However, as there are no specimens that correspond to those McCommas (1991) identified as A. carneola or B. stelloides, it is impossible to determine the identity of those samples. Be- cause A. krebsi and A. pallida are sympatric, the sister-group relationship McCommas (1991) proposed may be the result of two individuals of the same species having been sampled, and thus not indicative of a close phylogenetic relationship between the two species. However, recent research on other, well-known species of Anthopleura (e.g., McFadden et al., 1997, Pearse and Francis, 2000; Geller and Walton, 2001) has shown that some sympatric species are sibling species; A. krebsi and A. pallida may be another such example. Given the geographic distance separating Puerto Rico (the collection lo- cality for the sample McCommas identified as A. stellula) and the Western Indian Ocean (the known range of A. stellula), it is unlikely that the specimens sampled by McCommas (1991) belong to this species. The sample identified as A. stellula falls outside the clade containing other Anthopleura species, most closely allied to members of Bunodosoma; the sample may be a member of that genus, rather than a member of Anthopleura. Geller and Walton (2001) specifically addressed the identity of the sample they called A. carneola because their specimen lacked holotrichs in the marginal spherules. There are two possible explanations for the absence of holotrichs. The specimen may have contained only a few holotrichs, which went undetected. Not every spherule contains holotrichs, and even in those that do, holotrichs may be patchily distributed (Carlgren, 1940; Hand, 1955; England, 1987). Ecology, age, and post-collection factors like dura- tion and condition of captivity or exposure to conspecifics may affect holotrich density (Uchida, 1940; Hand, 1955; Francis, 1976, 1988; MD pers. obs.). Thus, it is possible that the specimen sampled by Geller and Walton (2001) belonged to either A. krebsi or A. pallida. Alternatively, the specimen may not have any holotrichs, in which case it was probably a member of I. stelloides, the only verrucae-bearing actiniid from Florida that does not have holotrichous marginal spherules. DALY AND DEN HARTOG: TAXONOMY AND USAGE OF ANTHOPLEURA 419
ACKNOWLEDGMENTS
This work was funded by NSF DEB 9978106 (Partnerships in Enhancing Expertise in Tax- onomy grant to D.G. Fautin). Specimens were collected with the permission of Florida Depart- ment of Fisheries and Wildlife (Permit 01S-614). J. Geller and S. McCommas provided assistance and information about the specimens they studied; C. H. Bigger, R. N. Mariscal, and E. E. Rup- pert provided field information. S. D. Cairns (USNM), L. van Ofwegen (NNM), and M. Siddall (AMNH) kindly provided specimens. This manuscript benefited from comments and suggestions from A. Ardelean, P. Braga-Gomes, D. G. Fautin, L. Gusmaõ, and three anonymous reviewers.
LITERATURE CITED
Andres, A. 1883. Le Attinie. Coi Tipi del Salviucci, Rome. 460 p. Belém, M. J. C. and D. C. Monteiro. 1981. Anthopleura varioarmata Watzl, 1922 (Actiniaria, Endomyaria), uma nova ocorrência de Actiniidae. Pages 193–203 in Seminários de Biologia Marinha. Academia Brasileira de Ciências, Rio de Janeiro. ______and S. M. Pinto. 1990. Morphological and microanatomical study of Anthopleura krebsi Duchassaing & Michelotti, 1860 (Cnidaria, Anthozoa, Actiniidae), a new record in Bra- zil. An. Acad. Bras. Ci. (Rio de Janeiro) 62: 183–192. ______, A. Herrera, and E. Schlenz. 1996. On Isoaulactinia stelloides McMurrich, 1889), n. gen., n. comb. (Cnidaria; Actiniaria; Actiniidae). Biociências 4: 77–88. Bigger, C. H. 1976. The acrorhagial response in Anthopleura krebsi: intraspecific and interspecific recognition. Pages 127–136 in G.O. Mackie, ed. Coelenterate ecology and behavior. Plenum Press, New York. ______. 1980. Interspecific and intraspecific acrorhagial aggressive behavior among sea anemones, a recognition of self and not-self. Biol. Bull. 159: 117–134. ______. 1982. The cellular basis of the aggressive acrorhagial response of sea anemones. J. Morphol. 173: 259–278. Boveri, T. 1893. Das Genus Gyractis, eine radial-symmetrische Actinienform. Zool. Jahrb. Abt. Syst. 7: 241–253. Cairns, S., J. C. den Hartog, and C. Arneson. 1986. Phylum Cnidaria, Class Anthozoa. Pages 159– 193 in W. Sterrer, ed. Marine fauna and flora of Bermuda. John Wiley and Sons, New York. Carlgren, O. 1895. Jahrsberichte für 1889, 1890, und 1891 über die Anthozoen. Arch. Naturg. 1: 235–298. ______. 1940. Some new South African Actiniaria and Zoantharia. Ark. Zool. 32: 1–7. ______. 1949. A survey of the Ptychodactiaria, Actiniaria and Corallimorpharia. Kungl. Sven- ska Vetenskapsakad. Handl. (4th series) 1: 1–121. ______. 1952. Actiniaria from North America. Ark. Zool. (2nd series) 3: 373–390. ______and J. W. Hedgpeth. 1952. Actiniaria, Zoantharia and Ceriantharia from shallow water in the northwestern Gulf of Mexico. Publ. Inst. Mar. Sci. (Univ. Texas) 2: 143–172. Corrêa, D. D. 1964. Corallimorpharia et Actiniaria do Atlantico Oeste Tropical. Doctoral Disserta- tion, Universidade de São Paulo, São Paulo. 139 p. ______. 1973. Sobre anêmonas-do-mar (Actiniaria) do Brasil. Bol. Zool. Biol. Mar. 30: 57– 468. Duchassaing de Fonbressin, P. and J. Michelotti. 1860. Mémoire sur les corralliares des Antilles. Imprimerie Royale, Turin. 89 p. ______and ______. 1864. Supplément au mémoire sur les corralliares des Antilles. Imprimerie Royale, Turin. 112 p. ______and ______. 1866. Supplément au mémoire sur les corralliares des Antilles. Memoire Reale Academia delle Scienze di Torino 8: 97–206. Duerden, J. E. 1897. The Actiniaria around Jamaica. J. Inst. Jamaica 2: 449–465. 420 BULLETIN OF MARINE SCIENCE, VOL. 74, NO. 2, 2004
Dunn, D. F., F. -S. Chia, and R. Levine. 1980. Nomenclature of Aulactinia (= Bunodactis), with a description of Aulactinia incubans n. sp. (Coelenterata: Actiniaria), an internally brooding sea anemone from Puget Sound. Can. J. Zool. 58: 2071–2080. England, K. W. 1987. Certain Actiniaria (Cnidaria, Anthozoa) from the Red Sea and tropical Indo- Pacific. Bull. Brit. Mus. Nat. Hist. 53: 205–292. Fautin, D. G. 1988. The importance of nematocysts to actinian taxonomy. Pages 487–500 in D. A. Hessinger and H. M. Lenhoff, eds. The biology of nematocysts. Academic Press, New York. ______and F. -S. Chia. 1986. Revision of sea anemone genus Epiactis (Coelenterata: Ac- tiniaria) on the Pacific coast of North America, with descriptions of two new brooding species. Can. J. Zool. 64: 1665–1674. Francis, L. 1976. Social organization within clones of the sea anemone Anthopleura elegantissima. Biol. Bull. 150: 361–376. ______. 1988. Cloning and aggression among sea anemones (Coelenterata: Actiniaria) of the rocky shore. Biol. Bull. 174: 241–253. Geller, J. B. and E. D. Walton. 2001. Breaking up and getting back together: evolution of symbio- sis and cloning in sea anemones (genus Anthopleura) inferred from a molecular phylogeny. Evolution 55: 1781–1794. Gomes, P. B., M. J. Belém, and E. Schlenz. 1998. Distribution, abundance and adaptations of three species of Actiniidae (Cnidaria, Actiniaria) on an intertidal beach rock in Carneiros Beach, Pernambuco, Brazil. Misc. Zool. 21: 65–72. Hand, C. 1955. The sea anemones of central California part II. Wasmann. J. Biol. 13: 37–99. den Hartog, J. C. 1987. A redescription of the sea anemone Bunodosoma biscayensis (Fischer, 1874) (Actiniaria, Actiniidae). Zool. Med. (Leiden) 61: 533–559. ______. 1994. Sea anemones of the Seychelles. Pages 75–80 in J. van der Land, ed. Oce- anic Reefs of the Seychelles Vol. 2. National Museum of Natural History, Leiden. ______and J. Vennam. 1993. Some Actiniaria (Cnidaria: Anthozoa) from the west coast of India. Zool. Med. (Leiden) 67: 601–637. Hedgpeth, J. W. 1954. Anthozoa: the anemones. Fish. Bull. Fish Wildlife 55: 285–290. Hemprich, F. G. and C. G. Ehrenberg. 1834. Beiträge zur physiologischen Kenntniss der Coral- lenthiere im allgemeinen, und besonders des rothen Meeres, nebst einem Versuche zur physi- ologischen Systematik derselben. Abh. Königl. Akad. Wiss. Berl. 1: 225–380. Herrera Moreno, A. 1981. Nuevos registros de anémonas (Coelenterata: Actiniaria y Corallimor- pharia) para aguas cubanas. Poeyana 214: 1–3. Hickson, S. J. 1889. Coelenterata. Zool. Rec. 26: 1–24. International Commission on Zoological Nomenclature (ICZN). 1999. International code of zoo- logical nomenclature. International Trust for Zoological Nomenclature, London. 306 p. Lewis, J. B. 1960. The fauna of the rocky shores of Barbados, West Indies. Can. J. Zool. 38: 391–435. Mariscal, R. N. 1974. Nematocysts. Pages 129–166 in L. Muscatine and H.M. Lenhoff, eds. Coel- enterate biology: reviews and new perspectives. Academic Press, New York. Mathew, K. 1967. Observations on Anthopleura nigrescens. Bull. Dept. Mar. Biol. Oceanogr. 3: 41–44. McCommas, S. A. 1983. A taxonomic approach to evaluation of the charge state model using twelve species of sea anemone. Willey Zool. Res. 103: 741–752. ______. 1991. Relationships within the family Actiniidae (Cnidaria, Actiniaria) based on molecular characters. Hydrobiologia 216/217: 509–512. Mc Fadden, C. S., R. K.Grosberg, B. B. Cameron, D. P. Karlton, and D. Secord. 1997.Genetic relationships within and between clonal and solitary forms of the sea anemone Anthopleura elegantissima revisited: evidence for the existence of two species. Mar. Biol. 128: 127–139. McMurrich, J. P. 1889. The Actiniaria of the Bahama Islands, W.I. J. Morphol. 3: 1–80. ______. 1901. Report on the Hexactiniae of the Columbia University Expedition to Puget Sound during the summer of 1896. Ann. NY Acad. Sci. 14: 1–46. Pax, F. 1907. Vorarbeiten zu einer Revision der Familie Actiniidae. Königl. Univ. Breslau. 87 p. DALY AND DEN HARTOG: TAXONOMY AND USAGE OF ANTHOPLEURA 421
_____. 1924. Actiniarien, Zoantharien und Ceriantharien von Curaçao. Nat. Art. Magis. (Amster- dam) 23: 93–122. Pearse, V. and L. Francis. 2000. Anthopleura sola, a new species, solitary sibling species to the aggregating sea anemone Anthopleura elegantissima. Proc. Biol. Soc. Wash. 113: 596–608. Pires, D. O., C. B. Castro, A. E. Migotto, and A. C. Marques. 1992. Cnidários bentônicos do Arqui- pélago de Fernando de Noronha, Brasil. Bol. Mus. Nac. (Rio de Janeiro) 354: 1–21. Presnell, J. K. and M. P. Schreibman. 1997. Humasonʼs animal tissue techniques. Johns Hopkins University Press, Baltimore. 572 p. Ruppert E. E. and R. S. Fox. 1988. Seashore animals of the southeast. University of South Carolina Press, Columbia. 429 p. Schmidt, H. 1972. Prodromus zu einer Monographie der Mediterranean Aktinien. Zoologica 121: 1–146. Uchida, T. 1938. Reports of the biological survey of Mutsu Bay 33. Actiniaria of Mutsu Bay. Sci. Rep. Tohoku Univ. (Biology) 13: 281–317. ______. 1940. The fauna of Akkeshi Bay X. Actiniaria. J. Fac. Sci. Hokkaido Univ. (Zoology) 7: 265–275. ______. 1941. Actiniaria collected in the vicinity of Onagawa Bay. Sci. Rep. Tohoku Univ (Biology) 16: 383–390. Verrill, A. E. 1864. Revision of the polypi of the eastern coast of the United States. Mem. Boston Soc. Nat. Hist. 1: 1–45. ______. 1869. On the geographical distribution of the polyps of the west coast of America. Trans. Conn. Acad. Arts Sci. 1: 558–567. ______. 1871. Synopsis of the polyps and corals of the North Pacific Exploring Expedition, under Commodore C. Ringgold and Capt. John Rodgers, U.S.N., from 1853-1856. Collected by W. Stimpson, Naturalist to the Expedition. Comm. Essex Inst. 6: 51–104. ______. 1899. Descriptions of imperfectly known and new Actinians, with critical notes on other species, II. Am. J. Sci. 7: 41–50. ______. 1900. XIV. Additions to the Anthozoa and Hydrozoa of the Bermudas. Trans. Conn. Acad. Arts Sci.10: 551–572. ______. 1905. The Bermuda Islands, Part IV and V. Trans. Conn. Acad. Arts Sci. 12: 45– 348. ______. 1907. The Zoology of Bermuda. A.E. Verrill, New Haven. 168 p. Watzl, O. 1922. Die Actiniarien der Bahamainseln. Ark. Zool. 14: 1–89. Williams, R. B. 1996. Measurements of cnidae from sea anemones (Cnidaria: Actiniaria): statisti- cal parameters and taxonomic relevance. Sci. Mar. 60: 339–351. ______. 1998. Measurements of cnidae from sea anemones (Cnidaria: Actiniaria), II: fur- ther studies of differences amongst sample means and their taxonomic relevance. Sci. Mar. 62: 362–371. ______. 2000. Measurements of cnidae from sea anemones (Cnidaria: Actiniaria), III: ranges and other measures of statistical dispersion, their interrelations and taxonomic rele- vance. Sci. Mar 64: 49–68. Zamponi, M. O., M. J. C. Belém, E. Schlenz, and F. H. Acuña. 1998. Distribution and some eco- logical aspects of Corallimorpharia and Actiniaria from shallow waters of the South American Atlantic coasts. Physis 55: 31–45.
DATE SUBMITTED: 23 May, 2003. DATE ACCEPTED: 23 September, 2003.
ADDRESSES: (M.D.) Department of Ecology and Evolutionary Biology and Division of Inverte- brate Zoology, KU Natural History Museum and Biodiversity Research Center, University of Kansas, Lawrence Kansas 66045; (J.C. den H.) Nationaal Natuurhistorisches Museum, Darwin- weg, P.O. Box 9517, NL-2300 RA Leiden, The Netherlands (deceased). CORRESPONDING AUTHOR: (M.D.) E-mail: