Isozoanthus antumbrosus, Swain, Timothy D., 2009

Swain, Timothy D., 2009, Isozoanthus antumbrosus, a new species of zoanthid (Cnidaria: Anthozoa: Zoanthidea) symbiotic with Hydrozoa from the Caribbean, with a key to hydroid and sponge-symbiotic zoanthid species, Zootaxa 2051, pp. 41-48 : 42-46

Isozoanthus antumbrosus new species

Synonymy. Parazoanthus tunicans “black” sensu Sinniger et al., 2005 Parazoanthus tunicans sensu Reimer et al., 2008

Isozoanthus sp. nov. sensu Swain , in press

Material examined. Isozoanthus antumbrosus : Atlantic Ocean, Caribbean Sea, Netherlands Antilles, Curaçao, Spaanse Water Baai channel, 12°3΄55ʺ N, 68°51΄10ʺ W, 10 m, 1 December 2007, associated with Dentitheca dendritica , preserved in 4% formalin, stored in 70% ethanol, USNM 1113090, holotype. A second individual was collected at the same location and time, USNM 1113091, paratype. Atlantic Ocean, Caribbean Sea, Dominica, Salisbury, Whale Shark Reef, 15°26΄24ʺ N, 61°27΄26ʺ W, 21 m, 12 November 2003, preserved in 70% ethanol, consumed in analyses, paratype. USNM 50878. Morphological measurements from photographs taken in Panamá and Tobago. DNA sequences culled from GenBank: EU418275 ( Curaçao), EU418276 ( Dominica), EU418277 and EU828761 ( Panamá), and AY995940 ( Parazoanthus tunicans “black” sensu Sinniger et al. 2005 , Honduras). Unidentified anthozoans: USNM 17218, 50354, 50777, 50778, 52526. Parazoanthus tunicans : Atlantic Ocean, Caribbean Sea, Netherlands Antilles, Curaçao, Spaanse Water Baai channel, 12°3΄55ʺ N, 68°51΄10ʺ W, 10 m, 1 December 2007, associated with Dentitheca dendritica , preserved in 4% formalin, stored in 70% ethanol, USNM 1113089. Morphological measurements from photographs taken in Panamá and Tobago. DNA sequences culled from Genbank: EU418339 ( Curaçao), EU418340 ( Dominica), EU418341 and EU828760 ( Tobago), and AY995941 ( Parazoanthus tunicans “white” sensu Sinniger et al. 2005 , Honduras).

Diagnosis. Zooxanthellate Parazoanthidae symbiotic with Dentitheca dendritica . Expanded polyps dichromatic; coenenchyme, column, and oral disk seal brown with 30–38 golden tentacles. Coloration of oral disk and tentacles recalls an annular solar eclipse. Largest expanded polyp columns 8.9 mm long, 4.3 mm in diameter; oral disk diameter 4.8 mm. Contracted polyps monochromatic, with 15–19 distinct capitular ridges.

Colony. Coenenchyme thin and encrusting, completely enveloping the central and secondary axial branches of D. dendritica colonies; usually not covering the finest pinnate branches, where the hydroid zooids are located ( Fig. 1 ). Coenenchyme usually seal brown (but can appear dark olive green or nearly black) and densely infiltrated with calcareous sediment and siliceous spicules (and therefore appearing “flecked” with white).

Polyp. Fully expanded polyps dichromatic: capitulum and oral disk seal brown, tentacles translucent golden; color most saturated at the bases of tentacles ( Fig. 1 ). Column 4.1–8.9 mm long, 2.2–4.3 mm in diameter, and infiltrated with calcareous sediments and siliceous spicules in a gradient that diminishes toward the bases of tentacles. Oral disk 2.7–4.8 mm in diameter, concave with obvious ridges corresponding to tentacles and internal mesenteries; a central, oval protrusion bears a slit-like mouth. Tentacles 30-38, in two cycles (alternating tentacles directed toward and away from the coenenchyme), 1.9–5.0 mm long and 0.4–0.7 mm in diameter at the point of insertion in the oral disk, and gradually tapered to rounded, nearly white tips.

Polyps at intervals of approximately 1.5–2.5 polyp diameters, often in an orthogonal or distichous (on the finest hydroid branches) arrangement with oral disks nearly parallel to the plane of pinnate hydroid branches. Tentacles of adjacent polyps nearly touching at tips but not interdigitating ( Fig. 1 ).

Contracted polyps seal brown, mammiform, 2.2–4.2 mm in diameter and extending 3.3–9.9 mm above surrounding coenenchyme. Capitulum bearing 15–19 distinct ridges.

Internal Anatomy. Mesenteries 30–38, in typical macrocnemic arrangement (fifth mesentery complete; Fig. 2). Retractor muscles and mesoglea of macrocnemes minimal. Mesenterial filaments present. Marginal sphincter muscle endodermal and diffuse (Fig. 2). Ectoderm and mesoglea of column with many lacunae left behind by dissolved calcareous and siliceous particles (Fig. 2). Encircling sinus usually imperceptible.

Distribution. Found on coral reefs or rocky substrata at 1–60 m in Honduras, Panamá, Colombia, Curaçao ( Netherlands Antilles), Tobago ( Trinidad and Tobago), Suriname, and Dominica. Not observed free of D. dendritica colonies, which are found throughout the Caribbean but rarely dominate the benthic invertebrate community except in areas of consistently high current (e.g., channel between Trinidad and Tobago).

Etymology. "Antumbra" is the astronomical term for the region from which an occulting body appears surrounded by the light source producing an annular eclipse. Coloration of the oral disk and tentacles recalls the appearance of an annular solar eclipse. From the Latin noun umbra, feminine, meaning shadow; used here as the masculine adjective, antumbrosus , to agree with the Latinized Isozoanthus , masculine, from the Greek anthos, neuter, meaning flower.

Differential Diagnosis. Although colonies of P. tunicans and I. antumbrosus both associate with D. dendritica colonies, distinct morphological and molecular differences separate them (Swain in press). Isozoanthus antumbrosus polyps have darker colored column and coenenchyme; significantly greater (t = 23.4, df = 190, p = 8.2 × 10-58, n polyps = 192, n colonies = 37) numbers of tentacles and capitular ridges (Fig. 3); significantly longer (t = 2.1, df = 28, p = 5.3-4, n polyps = 30, n colonies = 17) and wider (t = 2.1, df = 20, p = 6.2-5, n polyps = 22, n colonies = 16) polyp columns; and significantly larger (t = 2.0, df = 30, p = 4.4-8, n polyps = 32, n colonies = 20) oral disk diameters. Twelve nucleotide substitutions within the first internal transcribed spacer (ITS1) nuclear gene ( Table 1 ) and seven nucleotide substitutions (and one deletion) within the 16S mitochondrial gene (Table 2) consistently differentiate I. antumbrosus from P. t u n i c a n s. No substitutions or deletions occur within 16S sequences between P. tunicans “white” sensu Sinniger et al. (2005) and P. t u n i c a n s or between P. tunicans “black” sensu Sinniger et al. (2005) and I. antumbrosus (Table 2).

FIGURE 2. A. Cross-section of Isozoanthus antumbrosus polyp at the region of the actinopharynx (A) showing the dorsal directives (DD), siphonoglyph (S) and the macrocnemic (complete) fifth mesenteries (5th). Note the abundant lacunae (L) in the mesoglea and ectoderm. B. Longitudinal section of contracted Isozoanthus antumbrosus polyp at the region of the capitulum showing the endodermal sphincter muscle (ESM), actinopharynx (A), oral disk (OD) and tentacles (T). Note the abundant lacunae (L) in the mesoglea and ectoderm.

Species and collection location ITS1 nucleotide position and identity

TABLE 2. Comparison between Isozoanthus antumbrosus and Parazoanthus tunicans of the nucleotide sequences of the 16S ribosomal RNA mitochondrial gene (16S). Nucleotides that are identical to the first sequence are indicated by dots (·), missing data are indicated by question marks (?), and gaps in the alignment are indicated by dashes (—).

Species and collection location 16S nucleotide position and identity

Other similar species. Swain (in press) demonstrated a strong tendency for closely related zoanthids (regardless of current taxonomy) to form symbioses with closely related host species (phylogenetic conservatism) and presented morphological and genetic evidence for a transoceanic distribution of some species. Therefore, any macrocnemic zoanthid species that forms associations with hydroids representing Dentitheca and its relatives must be differentiated. Members of Parazoanthus gracilis ( Lwowsky 1913) form associations with hydroids of the genus Plumularia ( D. dendritica was originally described as a Plumularia ) in Japan but have tentacles numbering 36–42 ( Lwowsky 1913) and distinct 16S and COI DNA sequences ( Reimer et al. 2008). Members of Parazoanthus dichroicus Haddon & Shackleton, 1891 b have 18 capitular ridges and form associations with hydroids of the genus Plumularia in the Torres Straits ( Australia) but have polyps measuring 2.5 × 1.5 mm that are dichromatic when contracted (capitulum yellow) and have a “dichroic effect" on preserving alcohol ( Haddon & Shackleton 1891b). Members of Parazoanthus douglasi Haddon & Shackleton, 1891 b form associations with hydroids in the Torres Straits but are uniform sandy brown in color, have indistinct capitular ridges, and are facultative symbionts ( Haddon & Shackleton 1891b). Members of Parazoanthus elongatus McMurrich, 1904 form associations with hydroids in Chile but have a distinct cuticle and thick mesoglea, mesenteries numbering 28–32, and polyps measuring 15–20 mm in length ( McMurrich 1904). Members of Epizoanthus patagonichus Carlgren, 1899 form associations with hydroids in Chile and Argentina ( Cutress & Pequegnat 1960) and have polyps measuring 5–6 mm in length and 4.5–5.0 mm in diameter with 32 mesenteries but have rust-red tentacles and are facultative symbionts ( McMurrich 1904).

FIGURE 3. Comparison of tentacle numbers observed on polyps of Isozoanthus antumbrosus (n polyps = 80, n colonies = 18) and Parazoanthus tunicans (n polyps = 112, n colonies = 19) in Panamá and Tobago.

Remarks. Symbiosis with D. dendritica dominates the life history of I. antumbrosus . Although the position of a symbiotic relationship along the parasitism–mutualism continuum cannot be decided on the basis of one-time observations, examination of many holobionts may provide clues (e.g., Beaulieu 2001) that can help shape future experiments. Of more than 200 observed associations, in only one did an I. antumbrosus colony completely cover a D. dendritica colony. Usually the coenenchyme of I. antumbrosus colonies envelops the central and secondary axial branches of D. dendritica colonies but not the finest pinnate branches, where the hydroid zooids are located ( Nutting 1900). Repeated observations of associations with live hydroid colonies that do not cover the critical zooid supporting branches suggest that the I. antumbrosus - D. dendritica symbiosis is not parasitic, but the definitive experiments have not yet been completed. By comparison, P. gracilis colonies associated with hydroids in Izu, Japan, seem to be aggressive parasites, as five years of repeated photographs show hydroid zooids steadily disappearing beneath the coenenchyme of P. gracilis (pers. comm., J. Reimer).

In contrast to the Caribbean sponge-symbiotic zoanthids, which have largely nonoverlapping suites of host sponge species ( Swain & Wulff 2007), the Caribbean hydroid-symbiotic zoanthids share the same single host species (Swain in press), and colonizations by I. antumbrosus and P. tunicans are observed on the same individual host. Contact regions between the two species often include a bare zone of exposed hydroid axial skeleton and reduced, damaged, or contracted zoanthid polyps. Competition among sponge-symbiotic zoanthids has only been documented in a single study, and the outcome of that competitive bout was decidedly uncertain; different outcomes were observed at different times across different regions of the zoanthid colonies ( West 1979).

The genera of Macrocnemina are currently uncertain and include distinct subdivisions within genera ( Sinniger et al. 2005, Reimer et al. 2008, Swain in press) and close evolutionary relationships among some species currently assigned to separate genera (Swain in press). The morphology of I. antumbrosus is consistent with the genus Isozoanthus (fifth mesentery complete, marginal sphincter muscle endodermal, and mesogloeal ring-sinus inconspicuous), but molecular phylogenetics ( Sinniger et al. 2005, Reimer et al. 2008, Swain in press) indicates that the closest known relatives are representatives of the genus Parazoanthus (fifth mesentery complete, marginal sphincter muscle endodermal, and mesogloeal ring-sinus conspicuous). Sinniger et al. (2005), Reimer et al. (2008), and Swain (in press) indicate that the clade of zoanthids that includes I. antumbrosus is distinct from the clade of zoanthids that includes the type species of the genus Parazoanthus ( Parazoanthus sensu stricto: Reimer et al. 2008 ), suggesting that I. antumbrosus is not a representative of Parazoanthus . Because the inconsistency between morphological and molecular data cannot be resolved with currently available data, I accept the morphological definition of Isozoanthus here, with the stipulation that it will probably change to a different (not yet described) genus in the future.

Figures

FIGURE 1. A. Line drawing showing Isozoanthus antumbrosus colonized Dentitheca dendritica. Scale bar is solid for colony and checkered for polyp detail inset. Drawing by J. Putnam H. of Florida State University. B. In situ macrophotograph of Isozoanthus antumbrosus with Dentitheca dendritica zooids visible in background.

Tables

TABLE 1. Comparison between Isozoanthus antumbrosus and Parazoanthus tunicans of nucleotide sequences of the first internal transcribed spacer region of the ribosomal RNA nuclear gene (ITS 1). Nucleotides that are identical to the first sequence are indicated by dots (·), missing data are indicated by question marks (?), and ambiguous nucleotides are indicated by standard letter code (M = A or C, K = G or T).

Parazoanthus tunicans Tobago Parazoanthus tunicans Dominica	216 G ·	244 C ·	255 T ·	269 C ·	273 G ·	280 T ·	304 C ·	328 G ·	349 G ·	356 T ·	358 G ·	380 M T	385 K A	386 T?
Parazoanthus tunicans Curaçao Isozoanthus antumbrosus Dominica Isozoanthus antumbrosus Panamá	· A A	· T T	· G G	· T T	· A A	G · ·	· T T	· A A	· A A	· A A	· A A	G A A	A A A	· C C
Isozoanthus antumbrosus Curaçao	A	T	G	T	A	·	T	A	A	A	A	A	A	C