A Field Key to the Identification of Tropical Western Atlantic Zooxanthellate Octocorals (Octocorallia: Cnidaria)

Home , Ellisella, Ellisellidae, Erythropodium, Eunicea, Gorgonia, Gorgonia flabellum

JUAN ARMANDO SÁNCHEZ1 AND HERMAN H. WIRSHING2

1Departamento de Ciencias Biológicas, Universidad de los Andes, P.O. Box 4976, Bogotá, Colombia; Corresponding author: [email protected] 2National Coral Reef Institute, Oceanographic Center, Nova Southeastern University, 8000 North Ocean Drive, Dania Beach, FL 33004, USA

ABSTRACT.—Despite their abundance and ecological importance, octocorals have received relatively little taxonomic attention compared to scleractinian (stony) corals. Identification of octocoral species is often difficult and ambiguous, and requires thorough microscopic examination of skeletal components (sclerites). Here, we provide a key for field identification—no microscope required—of 51 zooxanthellate (harboring photosynthetic dinoflagellate symbionts) octocoral species (3 soft and 48 gorgonian octocorals) from the tropical western Atlantic. The key is based on characters from colony branching pattern, surface morphology and texture, extended polyp size, and colony color. Although species confirmation by microscopic examination is still recommended, it is hoped that tools, such as this key, and approaches for fast octocoral identification will ease the difficulty of carrying out surveys and monitoring programs.

KEYWORDS.—Octocorals, symbiotic, zooxanthellae, coral reefs, Caribbean, gorgonians, soft corals, identification keys

INTRODUCTION species harbor algal symbionts. Though Eastern Pacific reefs and littoral zones are The underwater landscape of many also dominated by gorgonian octocorals in- Caribbean coral reef environments is domi- cluding Caribbean congeners, only the nated by zooxanthellate (harboring photo- counterparts present in the Atlantic host synthetic dinoflagelate symbionts) octo- symbionts (e.g., Muricea). In a typical corals (Octocorallia: Cnidaria), commonly Southern Caribbean coral reef such as the referred to as “gorgonians” and “soft cor- fringing system in the vicinity of Bocas del als”. Gorgonian is a common name derived Toro, Panama, only 7 (11%) out of 61 spe- from the now controversial ordinal classi- cies of octocorals found do not host symbi- fication Gorgonacea, and is used to loosely onts (see Appendix). Although gorgonian categorize octocorals which contain some octocorals are susceptible to diseases (e.g., form of branching morphology with a sup- Smith et al. 1996), Caribbean gorgonians porting internal axis of fused sclerites, seem to be very resistant to coral bleaching scleroprotein (gorgonin), or non-scleritic or expulsion of their symbionts (Lasker calcium carbonate (Grasshoff and Bargi- 2003; Lewis and Coffroth 2004), which will bant 2001). Other octocorals, those which likely have an impact on reef community do not contain a supporting internal axis or structure where scleractinian corals are skeleton and are united in a common fleshy more susceptible to bleaching related mor- mass, are referred to as soft corals (Fabri- tality. Despite their abundance and ecologi- cius and Alderslade 2001). Scleractinian cal importance, however, octocorals have and soft corals dominate Indo-Pacific reefs not had comparable research to that of (Fabricius and Alderslade 2001) whereas scleractinian corals. A reason for this may gorgonian octocorals are the most promi- be the extreme difficulty in differentiating nent anthozoan found on tropical western gorgonian groups and species, which often Atlantic reefs. Unlike in the Indo-Pacific, requires thorough microscopic examina- most tropical western Atlantic gorgonian tions of sclerites and axis (e.g., Bayer 1961). 508 ZOOXANTHELLATE OCTOCORALS 509

Since species familiarization and surveys fore, it is important that dubious identifica- are the base for further research, it is essen- tions be confirmed with microscopic tial to develop tools, keys, and approaches examination of sclerites. Finally, these keys for fast octocoral identification. In addition, are not intended to be exact, exhaustive or as new species of octocorals are described exclusive, but to provide a means to annually, and scanning electron micros- quickly and accurately identify octocoral copy (SEM) is becoming the dominant colonies in the field. method to morphologically describe octo- As with the analysis of any group, it is corals, the complete microscopic examina- unavoidable to use specialized terminology tion of octocoral traits for ecological or to describe particular traits. The use of other rapid surveys will require unrealistic terminology was minimized as much as amounts of resources and effort. Conse- possible and the few used terms are de- quently, it is important to develop tools for scribed in detail in Table 1. Sources of ter- fast and accurate identification of octocoral minology on gorgonian traits were ex- fauna. tracted and/or modified from Bayer (1961), Field surveys, photography-collection, Cairns (1977) and Bayer et al. (1983). Addi- and microscopic examination are the most tional information and concepts on external reliable approaches to become familiar features and branching patterns of Car- with octocoral species. Here, we provide a ibbean gorgonian octocorals are found in means to identify octocorals based entirely Sánchez and Lasker (2003) and Sánchez et on field-observable characteristics. A al. (2004). complementary analysis of underwater observations and microscopic examinations of octocoral sclerites has made it possible to Key to Zooxanthellate octocorals of the develop a set of keys to accurately identify tropical western Atlantic gorgonian octocorals in their habitat. Dur- ing the 2003-Invertebrate Workshop 1a. Colonies with no axis, encrusting or (Smithsonian Institution, Bocas del Toro, single branches rising from a base: Panama) preliminary ideas and notes on a Soft corals ------2 field key for the identification of Caribbean 1b. Colonies with an axis, not encrust- zooxanthellate octocorals were tested ing; branching dichotomous, pin- through direct observations, digital pho- nate, bushy, or candelabral: ------4 tography, and microscopic examinations. 2a. Coenenchyme purplish with shades Our observations are not limited to Panama of gray or tan; apertures open, en- and include surveys from southeastern crusting or branching; polyps dark Florida, Puerto Rico, Bahamas, México, and large (> 1 cm): ------3 Belize, Tobago and Colombia, which give 2b. Coenenchyme beige; polyps light us an ample model of the variation found and small (< 1 cm): ------within the tropical western Atlantic. The ------Erythropodium caribaeorum keys were designed for the identifica- (Duchassaing & Michelotti) (Fig. 1 A) tion, without colony collection or micro- 3a. Colonies with rod-like branching, usu- scopic examination of sclerites, of most ally connected by a stolonal mat: ---- zooxanthellate octocorals common to the ------Briareum asbestinum (Pallas) region. They are based on the combination (Fig. 1 B) of several characters: colony branching pat- 3b. Colonies encrusting forming soft tern, surface morphology and texture, ex- meat-ball like lobes; usually en- tended polyp size and color, and colony crusting gorgonian corals: ------color. Color was used only when no other ------Briareum polyanthes (Duchassaing external character was available to differ- & Michelotti) (Fig. 1 C) entiate among species. When ever size was 4a. Colonies with pinnate branches, used in the keys, it refers to a relative com- anastomosing, or plume-like with parison to the next closest species. There- flattened branchlets, never round or 510 J. A. SÁNCHEZ AND H. H. WIRSHING

TABLE 1. Definitions of terms used in the keys.

Anastomosing Condition in which the branches of a colony fuse to form a meshed pattern. Aperture Opening of the calyx into which the polyp retracts. Ascending Description of upward growing branches that are usually long and directed vertically. Axis Inner supporting structure of holaxonian gorgonians. Branch axils Junction where two branches come together. Branchlets Branches that arise from other branches, daughter branches, usually located terminally and smaller than the rest. Bushy Colonies with abundant branching not forming an obvious pattern. Calyx, Calyces Casing in which the polyp sits; may or may not be present as projections from colony surface. Candelabral (candelabrum) Branching pattern in which the colony is flattened in one plane. Clavate Branch tip ending in a rounded lobe. Clonal Asexually propagating colony by stolons or fragments. Coenenchyme Tissue between the polyps. Cross-section Cut through a branch at right angles to the longest axis. Dichotomous Branching pattern consisting of repeated bifurcations. Encrusting Growth form in which the colony takes the shape of the surface on which it grows. Fan-shaped Flattened colony shape with branches packed closely together. Gaping Referring to an aperture that is conspicuously open. Lateral branching Colony growth in which branching originates as irregular or alternate side daughter branches. Pinnate Feather-like branching pattern which consists of a primary branch with secondary branches emerging on either side of mother branch. Pinnules Lateral branchlets in pinnate branching. Plume, Plumose Branching pattern that resembles a feather, usually long and flowing. Polyp An individual of the colony, emerging from the calyx aperture and bearing tentacles. Ramifications Referring to whether branches have other branches emerging from them. Shrubby Description of colony that is short with most of its growth occurring laterally. Stolon A part of a colony that grows horizontally on the substrate, from which new upright branches arise. Tapering Referring to branches that become gradually smaller at their ends.

rod-like; calyces generally along ei- [A] Key to the “gorgoniid” gorgonians ther side of branch, never uniformly around the branch; or bushy colo- 1a. Colonies with branches intercon- nies with thin branches flattened or nected, forming a net-like fan: ----- triangular in cross-section: ------Gorgonia spp. (AI) ------“gorgoniid” gorgonians* [A] 1b. Colonies with pinnate branches in *(Most genera in this group belong to the the form of a plume, or bushy colo- family Gorgoniidae minus Pterogorgia, whose nies whose branches are flat or tri- phylogenetic placement is uncertain.) angular in cross-section: ------2 4b. Colonies candelabral, bushy or pin- 2a. Colonies bushy with extremely nate; branches rod-like, circular in flattened tape-like branches or cross-section ranging from short and sometimes triangular in cross- stubby to long and ascending: ------section; polyps white: ------“plexaurid” gorgonians* [B] ------Pterogorgia spp. (AII) *(Most genera in this group belong to the 2b. Colonies with pinnate branching family Plexauridae minus Plexaurella,a (pinnules), forming plumes; polyps likely gorgoniid, and Muriceopsis, whose brown or golden: ------phylogenetic placement is uncertain.) ------Pseudopterogorgia spp. (AIII) ZOOXANTHELLATE OCTOCORALS 511

FIG.1.A.Erytropodium caribaeorum (Bocas del Toro-BT, Panama, B. Briareum asbestinum (Serrana Bank, Co- lombia), C. B. polyantes (BT, Panama; Eleuthera I., Bahamas), D. Gorgonia mariae (Belize; BT, Panama), E. G. ventalina (Uraba, Colombia), F. G. flabellum (Belize; BT, Panama), G. Pterogorgia anceps (BT, Panama), H. P. guadalupensis (BT, Panama), I. Pterogorgia sp. (BT, Panama), J. P. citrina (Quitasueño, bank). (Photos J. A. Sánchez). [AI] Gorgonia boxed in cross-section; branch tips long, thin, and flattened; ------1a. Colonies with a tightly anastomos------Pterogorgia anceps (Pallas) ing mesh; mesh square: ------2 (Fig. 1 G) 1b. Colonies with branches partially 2a. Colonies usually tall and heavily pinnate and reticulate (may be branched; blades broad and flat: ---- mostly pinnate or mostly reticu------Pterogorgia guadalupensis late), mesh wider than longer: ----- (Duchassaing & Michelotti) (Fig. 1 H) ------Gorgonia mariae Bayer (Fig. 1 D) 2b. Colonies small, usually less than 20 2a. Colonies with round branches, or cm; blades narrow: ------3 slightly flattened in the plane of the 3a. Colonies sparsely branched, with fan: ------ascending branch tips; polyps arise ------Gorgonia ventalina Linnaeus from a common groove: ------(Fig. 1 E) ------Pterogorgia sp. (Fig. 1 I) 2b. Colonies with robust branches and 3b. Colonies bushy with branching in coenenchyme flattened at opposite multiple directions; polyps arise angles to the fan’s surface: ------from individual calyces, not a com------Gorgonia flabellum Linnaeus mon groove: ------(Fig. 1 F) ------Pterogorgia citrina (Esper) (Fig. 1 J) [AII] Pterogorgia

1a. Cross-section of branches flat, from [AIII] Pseudopterogorgia base to tip: ------2 1b. Cross section of branch base with 3 or 1a.Colony surface slimy when 4 flaps which appear triangular or touched: ------2 512 J. A. SÁNCHEZ AND H. H. WIRSHING

1b. Colony surface not slimy, coarse 4a. Branches flat, remain separated when when touched:------3 dry; polyps regularly placed along 2a. Colonies tall with long, regularly branch edge; multiple stems (large branching pinnules; extremely colonies similar in form to P. ameri- slimy and full of mucus when cana but not slimy): ------alive; branchlets mat together when ------Pseudopterogorgia acerosa (Pallas) dry: ------(Fig. 2D) ------Pseudopterogorgia americana 4b. Branches long; polyps mostly ir- (Gmelin) (Fig. 2A) regularly placed along branch edge; 2b. Colonies less than 1 meter with short usually one main stem: ------and irregular pinnules, moderately ------Pseudopterogorgia rigida slimy with no mucus; branchlets do (Bielschowsky) (Fig. 2E) not mat when dry: ------Pseudopterogorgia elisabethae Bayer (Fig. 2B) [B] Key to the “plexaurid” gorgonians 3a. Pinnules short and thin, paired on either side of main branch and 1a. Apertures slit-like; if apertures oval, spaced at regular intervals (similar gaping or pore-like, branching obvi- to P. elisabethae but pinnules thinner, ously dichotomous; pale baige to more closely spaced and always yellow: ------Plexaurella spp. (BI) paired): ------1b: Branching never dichotomous; ap------Pseudopterogorgia bipinnata ertures round or oval, sometimes (Verrill) (Fig. 2C) obscured by upturned lower lip:--- 2 3b. Pinnules longer and wider, not 2a. Branches slimy; calyces never raised paired or placed at regular inter- or rough to touch; apertures round vals, but closer together and taper- or oval, sometimes gaping with ing: ------4 slightly raised rims on terminal

FIG.2.A.Pseudopterogorgia americana (Serrana Bank, Colombia), B. P. elisabethae (Roncador Bank, Colombia), C. P. bipinnata (Belize), D. P. acerosa (San Salvador, Bahamas), E. P. rigida (Belize). (Photos J. A. Sánchez). ZOOXANTHELLATE OCTOCORALS 513

branches; lower calycular lip never [BI] Plexaurella spp. present:------BII 2b. Branches not slimy; calyces ranging 1a. Colonies with thick branches; slit- from flat to prominent, sometimes like apertures:------2 rough and spiny; lower calycular 1b. Colonies bushy with thinner branches lip always present at least as a weak coming from the base; apertures oval, shelf:------3 pore-like:------4 3a. Colonies pinnate or plumose: ------4 2a. Branches long and conspicuously 3b. Colonies bushy, candelabral, or thick with sparse branching; not with ascending branches: ------5 bushy, usually tall; calyces form 4a. Calyces prominent, rough and hemispherical mounds: ------spiny: ------Plexaurella nutans (Duchassaing ------Muricea pinnata Bayer (Fig. 4 A) & Michelotti) (Fig. 3 A) 4b. Calyces at most slightly raised with 2b. Colonies shrubby with short branches a weak shelf-like calycular lip: ----- ranging from moderately stout to ------Muriceopsis spp. (BIII) stout; calyces highly conspicuous to 5a. Calyces prominent, rough and spiny; flat; polyps short when extended: ---- 3 color usually yellow-green, white or 3a. Colonies bushy, branching from the orange: ------Muricea spp. (BIV) base; calyces slightly elevated to 5b. Calyces almost flat to tubular or smooth; branches thin and long: --- with lower lip, never rough and ---- Plexaurella fusifera Kunze (Fig. 3 B) spiny; color pale to dark brown, 3b. Colonies with moderate branch- grey, pink or purple: ------ing, branching dichotomous; caly------Eunicea spp. & Plexaura spp. (BV) ces usually form hemispherical

FIG.3.A.Plexaurella nutans (BT, Panama), B. P. fusilera (BT, Panama), C. P. dichotoma (Belize), D. P. grisea (BT, Panama), E. Plexaurella sp. (BT, Panama), F. Plexaura kuna (Belize), G. Eunicea knighti (Belize), H. Pseudoplexaura porosa (Quitasueño Bank, Colombia), I. P. crucis (Serrana bank, Colombia). (Photos J. A. Sánchez). 514 J. A. SÁNCHEZ AND H. H. WIRSHING

mounds; branches somewhat ro- 2a. Branching uniformly pinnate; branch bust: ------pinnules short and firm; found ------Plexaurella dichotoma (Esper) throughout the reef: ------(Fig. 3 C) ------Muriceopsis flavida (Lamarck) 4a. Coarse and firm branches: ------(Fig. 4 G) ----- Plexaurella grisea Kunze (Fig. 3 D) 2b. Branching not entirely pinnate; 4b. Flexible and slimy branches: ------branches long and flexible; found ------Plexaurella sp. (Fig. 3 E) only on reef slope: ------Muriceopsis petila Bayer (Fig. 4 H) [BII]

1a. Branches long and ascending: ------2 [BIV] Muricea spp. 1b. Branches short and profusely rami- fied: ------1a. Branches robust, flattened and ellip------Plexaura kuna Lasker, Kim & tical in cross section: ------2 Coffroth (Fig. 3 F) 1b. Branches thin and delicate, cylindri- 2a. Bulb or knob at some or all of the cal in cross section: ------branch tips, sometimes present on ------Muricea laxa Verrill (Fig. 4 B) the branches or branch axils; polyp 2a. Colonies bushy; branches elongate tentacles darker than polyp body; and ascending with thin tips: ------colonies reddish brown: ------Muricea elongata Lamouroux ------Eunicea knighti Bayer (Fig. 3 G) (Fig. 4 C) 2b. Conspicuous knobs never present 2b. Colonies candelabral, tending to at branch tips; extended polyps uni- branch in one plane; branchlets form in color; colonies purple, short, never elongate; branches ocher, greenish-yellow, or light ol- thick to the tip: ------3 ive gray-brown: ------3 3a. Colonies yellowish, orange or am- 3a. Polyp apertures dark and conspicu- ber; branch axils conspicuously ous; branches thick: ------flattened; branches tightly com------Pseudoplexaura porosa (Houttuyn) pacted: ------(Fig. 3 H) ------Muricea muricata (Pallas) 3b. Polyp apertures small; branches (Fig. 4 D) thin: ------4 3b. Colonies white to grey; branch axils 4a. Outer coenenchyme particularly not conspicuously flattened; branch- greenish-yellow; colonies short but ing open: ------profusely branched: ------Muricea atlantica (Kükenthal) ---- Pseudoplexaura crucis Bayer (Fig. 3 I) (Fig. 4 E) 4b. Outer coenenchyme beige to pale purple; colonies tall with long, slen- der tapering branches: ------[BV] Eunicea spp. & Plexaura spp. --- Pseudoplexaura flagellosa (Houttuyn) & Pseudoplexaura wagenarii (Stiasny).* 1a. Calyces elongate, tubular or conical; *(These two species can only be distin- lower lip alone may be slightly up- guished by microscopic examination.) turned, but never with a conspicuous sharp upper lip:------2 [BIII] Muriceopsis spp. 1b. Calyces never tubular or conical, present as an upturned lip, bump, 1a. Colonies tall; branches thin; branch- or hemispherical in shape:------5 ing pinnate: ------2 2a. Branches thin, usually single branches 1b. Colonies short (<20 cm) and bushy; rising from the base; calyces longer branches robust: ------than branch diameter: ------Muriceopsis bayeriana Sánchez ------Eunicea laxispica (Lamarck) (Fig. 4 F) (Fig. 5 A) ZOOXANTHELLATE OCTOCORALS 515

FIG.4.A.Muricea pinnata (Lee Stocking Island, Bahamas), B. M. laxa (BT, Panama), C. M. elongate (BT, Panama), D. M. muricata (Belize), E. M. atlantica (BT, Panama), F. Muriceopsis bayeriana (BT, Panama), G. M. flavida (Lee Stocking Island, Bahamas), H. M. petila (Belize). (Photos J. A. Sánchez).

2b. Branches thicker, calyces not longer 5b. Colonies bushy or tall; branches as- than branch diameter:------3 cending; if branching in one plane, 3a. Colonies candelabral with a ten- branches thin and calyces incon- dency to be bushy; some or most spicuous, never hemispherical:----- 7 calyces with a slightly upturned 6a. Calyces hemispherical with up- lower lip; branch axils thick; color turned lower lip; colonies medium light yellowish brown: ------to light brown, branches never ------Eunicea mammosa Lamouroux stout: ------(Fig. 5 B) ------Eunicea succinea (Pallas) (Fig. 5 F) 3b. Colonies ascending; branch axils 6b. Calyces with conspicuous upturned not noticeable; coenenchyme dark lower lip that is not hemispherical to almost black:------4 and tends to be pointed; apertures 4a. Branches long and thick; coenen- may be gaping: ------8 chyme dark with pale to white con- 7a. Colonies bushy, from short and spicuously tubular calyces: ------shrubby to broad, tall and flat; ------Eunicea sp. 1 (Fig. 5 C-D) branches thin:------9 4b. Branches long and thin; calyces and 7b. Colonies ascending, never broad or branches usually same dark color; flattened; branches thick: ------10 most calyces conical, some may be 8a. Colonies dark brown; compressed mound-like: ------branches elliptical in cross section; ------Eunicea clavigera Bayer (Fig. 5 E) apertures small with a projecting 5a. Colonies candelabral or with a ten- lower lip; diameter of branch-ends dency to branch in one plane; same or smaller than branch; never branches stout or moderately thick clonal: ------and elongate; if branches thin caly------Eunicea tourneforti Milne Edwards ces hemispherical: ------6 & Haime (Fig. 5 G) 516 J. A. SÁNCHEZ AND H. H. WIRSHING

FIG.5.A.Eunicea laxispica (Abaco, Bahamas), B. E. mammosa (Roncador bank, Colombia), C. E. colombiana (San Salvador, Bahamas), D. E. sp. 1 (Fuerte I., Colombia), E. E. clavigera (BT, Panama), F. E. succinea (BT, Panama), G. E. tourneforti (Serrana Bank, Colombia), H. E. laciniata (BT, Panama). (Photos J. A. Sánchez).

8b. Colonies medium brown; branches may appear sealed or gaping: ---- cylindrical and usually stout; aper------Eunicea calyculata Ellis & tures with eight surrounding lob- Solander (Fig. 6 B) ules and larger projecting lower lip 11a. Calyces present as an inconspicu- tip; branch ends usually bulbous ous lip or not at all; branches and clavate; branching may be brittle; colonies bushy with promi- horizontal, appearing to rise from nent lateral branching------12 a stolon and highly clonal: ------11b. Colonies pale, medium to light ------Eunicea laciniata Duchassaing browns, or purple, never black; & Michelotti (Fig. 5 H) true calyces may be present: ------13 9a. Colonies with elongate, straggling 12a. Colonies dark brown to black; ---- branches; calyces conspicuous with ------Plexaura homomalla (Esper) regularly placed upturned lower (Fig. 6 D) lips giving a rugged texture: ------12b. Colonies lavender to pale grey; ------Eunicea sp. 2 (Fig. 6 C) ------Plexaura kuekenthali Moser 9b. Colonies with flat calyces or pre- (Fig. 6 E) sent as a slight lip or mound: ----- 11 13a. Colonies broad, usually tending to 10a. Color dark; calyces with upturned be in one plane; branching usually lower lip usually giving a coarse profuse; calyces absent or present texture: ------as a lower lip, apertures small (pin------Eunicea asperula Milne Edwards hole in appearence): ------& Haime (Fig. 6 A) ------Eunicea flexuosa (Lamouroux) 10b. Color variable from light to dark; (Fig. 6 F) calyces flat or mound-like; aper- 13b. Colonies bushy, but never flat- tures with ridges on inner lip, they tened with tendency to be in one ZOOXANTHELLATE OCTOCORALS 517

FIG.6.A.Eunicea asperula (Belice; BT, Panama), B. E. calyculata (Roncador bank, Colombia), C. E. sp. 2 (San Salvador, Bahamas), D. Plexaura homomalla (Quitasueño Bank, Colombia), E. P. kukenthali (BT, Panama), F. Eunicea flexuosa (Belize), G. E. pallida (BT, Panama), H. E. fusca (BT, Panama). (Photos J. A. Sánchez).

plane; apertures clearly observ- lower lip: ------able: ------14 ------Eunicea palmeri Bayer 14a. Colonies nearly white: ------15 14b. Colonies not nearly white: ------16 15a. Colonies small, few ramifications; DISCUSSION branches brittle; occasionally clonal: ------Most tropical western Atlantic zooxan------Eunicea pallida Garcia-Parrado thellate gorgonian octocorals are closely re- and Alcolado (Fig. 6 G) lated phylogenetically (Sánchez et al. 2003; 15b. Colonies tall, profusely branched; Wirshing et al. 2005), and comprise a highly branches flexible: ------endemic fauna. Consequently, most taxa --- Eunicea pinta Bayer and Deichmann have sister species with similar morpho- 16a. Colonies usually small and rather logical characters, which makes it, in some bushy; terminal branches thin; cases, extremely difficult to differentiate calyces small and irregular in ap- species without thorough microscopic ex- pearance; often clonal: ------amination. In addition, most species are ------Eunicea fusca Duchassaing morphologically plastic and exhibit exten- and Michelotti (Fig. 6 H) sive variation both within habitats and over 16b. Colonies bushy, but more flat- environmental gradients. This makes most tened or candelabral; color usually observable traits a potential source of con- light browns or beige, sometimes fusion among species. In spite of this, it is with hints of lavender or purple; possible, after familiarization with the or- apertures may be slightly gaping ganisms, to identify tropical western At- and regularly placed; calyces lantic gorgonians macroscopically. It is rec- sometimes smooth or present as ommended that identifiers unfamiliar with 518 J. A. SÁNCHEZ AND H. H. WIRSHING

FIG. 7. Flow chart diagram for fast visual identification of Caribbean symbiotic gorgonian corals (Octocorallia: Cnidaria). gorgonian taxonomy confirm macroscopic scopically. Microscopic confirmations pro- identifications with microscopic analysis vide excellent feedback and reinforce the until a foundation is established on which identifier’s confidence in macroscopic field to confidently differentiate species macro- identifications. Most species should be- ZOOXANTHELLATE OCTOCORALS 519

FIG. 7. Continued come readily distinguishable in the field, able traits like branching pattern (e.g., Mu- and any dubious identification narrowed to riceopsis and Pseudopterogorgia with pinnate two or three species which could then be branching), calyx morphology (e.g., Plexau- verified by a minimal amount of micro- rella grisea and Psuedoplexaura spp. with flat scopic examination. Figure 7 illustrates a calyces), surface texture (e.g., Plexaura kuna scheme of how the keys may be adapted and Pseudoplexaura crucis with a slimy tex- into a flow chart based on basic morpho- ture) and color among others. Therefore, it logical characters. The chart follows a is important to recognize that these are ar- simple dichotomous pattern based on the tificial keys to species level, and not a taxo- presence or absence of a character, and nomic or systematic review based on mor- ends with a cluster of individual species phological similarities. However, the keys each differentiated by a brief diagnostic de- do attempt to follow taxonomic lines. They scription. Although it may be an oversim- loosely group most members of the family plification, Fig. 7 can be used as a rapid Plexauridae, key [A], and Gorgoniidae, key underwater guide. Bayer (1961) is still the [B], together. Although each family may most comprehensive source of keys and seem easily distinguishable by their over- morphological information for microscopic all appearance, they do not have a truly identifications of tropical western Atlantic independent evolutionary origin, but are gorgonians. In addition, several new spe- largely para—and polyphyletic (Sánchez et cies of Muriceopsis and Eunicea were re- al. 2003; Wirshing et al. 2005). Muriceopsis-a cently distinguished (Sánchez 2001 and un- plexaurid—and Pterogorgia-a gorgoniid— published), and provide further details on do not show a phylogenetic relationship particular characters. with their respective families, and Plexau- Convergent evolution in morphological rella-a plexaurid-shares a close phyloge- traits appears to be a recurrent pattern in netic relationship with the Gorgoniidae. the evolution of Caribbean gorgonian cor- Therefore, we placed “plexaurids” and als (Sánchez 2004; Wirshing et al. 2005). “gorgoniids” in quotes in the keys. Most Convergence is recognized in many observ- genera key out into separate individual 520 J. A. SÁNCHEZ AND H. H. WIRSHING keys. Key [BII], however, is a mixture of more easily approach and familiarize one- species from three genera (Plexaura, Pseudo- self with zooxanthellate gorgonian octo- plexaura and Eunicea). Eunicea spp. and corals even though the possibility exists Plexaura spp. were combined in key [BV] that all of the species included may have because there are no conspicuous macro- cryptic sibling species yet to be discovered. scopic characters with which to separate them, and Muricea pinnata keys out early in Acknowledgments.—Special thanks to key [A] because of its pinnate branching Rachel Collin (STRI-Smithsonian) who co- which is unlike the other Muricea spp. ordinated and directed the Invertebrate Several species of the gorgoniid genus Workshop at Bocas del Toro, Panama, and Pseudopterogorgia have not been included in encouraged the writing of this paper. Help the keys because specimens were not yet during surveys and comments from Alison available. Although many Caribbean Pseu- Acosta are greatly appreciated. Field sup- dopterogorgia were included in the first port from The Ocean Conservancy (TOC, comprehensive compendium of the tropi- Washington, D.C., USA), CORALINA (San cal western Atlantic (Bayer 1961), they have Andrés and Providencia, Colombia), State rarely been seen in shallow-water gorgon- University of New York at Buffalo ian surveys thereafter (e.g., Jordán 1989; (Howard Lasker), Caribbean Marine Re- Yoshioka and Yoshioka 1991; Sánchez et al. search Center (Lee Stocking Island, Baha- 1997). According to further sclerite analy- mas), the Gerace Research Center-College ses, Pseudopterogorgia rigida and P. blanquil- of the Bahamas, INVEMAR (Santa Marta, lensis as well as P. elisabethae and P. albatros- Colombia) and the National Museum of sae appear to be the same species, with the Natural History, Caribbean Coral Reef Eco- latter in each group corresponding an eco- systems-CCRE, Smithsonian Institution logical morphotype of the former. Pseudo- (Klaus Ruetlzer and Stephen Cairns) is pterogorgia hystrix, P. navia and P. hum- greatly acknowledged. The assistance and melincki, though they have been observed encouragement of Charles Messing (Ocean- in several surveys, are also morphologi- ographic Center, Nova Southeastern Uni- cally plastic but are extremely rare com- versity, Dania Beach, FL) with the develop- pared to the abundance of P. americana, P. ment of the keys was invaluable. bipinnata. P. acerosa, P. elisabethae and P. rigida. Alternatively, the Eunicea, are com- LITERATURE CITED prised of 16 common species, and are likely the most diverse group of zooxanthellate Alcolado, P. M. 1985. Sinonimia de Plexaura fusifera gorgonians found in the tropical western Kunze, 1916, con P. dichotoma (Esper, 1791) (Coel- Atlantic. enterata: Gorgonacea). Poeyana 294:1-3. Bayer, F. M. 1961. The shallow water Octocorallia of Plexaurella dichotoma and P. fusifera have the West Indian region. Stud. Fauna Curaçao 12:1- nearly identical sclerites with overlapping 373. variation, which has been used as a crite- Bayer, F. M., M. Grasshoff, and J. Verseveldt. 1983. An rion for synonimizing the two species (Al- illustrated trilingual glossary of morphological and ana- colado 1985). We decided to keep the two tomical terms applied to Octocorallia, Leiden: E.J. Brill. species based entirely on external features. Cairns, S. 1977. Guide to the Commoner Shallow-Water For instance, it is common to see very thick Gorgonians (Sea Whips, Sea Feathers, and Sea Fans) of Florida, The Gulf of Mexico, and the Caribbean Region. and clavate colonies of P. dichotoma along University of Miami Sea Grant Program. side long and stiff colonies of what is prob- Fabricius, K., and P. Alderslade. 2001. Soft corals and ably P. fusifera. However, it is unknown if sea fans: a comprehensive guide to the tropical shallow the thin, P. grisea-like colonies with polyp water genera of the central-west Pacific Ocean and the apertures like slits definitely belong to P. Indian Ocean and Red Sea. Melbourne: New Litho. fusifera, or to another species. This is a case Grasshoff, M., and G. Bargibant. 2001. Coral reef gorgonians of New Caledonia. Faune et Flore Tropicales, where a taxonomic revision, preferably cor- number 38. roborated with independent characters Jordán, E. 1989. Gorgonian community structure and (e.g., DNA sequences), is greatly needed. reef zonation patterns of Yucatán coral reefs. Bull. Finally, this paper is meant to be a tool to Mar. Sci. 45:670-696. ZOOXANTHELLATE OCTOCORALS 521

Lasker, H. R. 2003. Zooxanthella densities within a SUBCLASS OCTOCORALLIA HAECKEL, 1866 Caribbean octocoral during bleaching and non- (=ALCYONARIA)(OCTOCORALS) Coral Reefs bleaching years. 22(1):23-26. Family VIRGULARIIDAE Verrill, 1868 Lewis, C. L., and M. A. Coffroth. 2004. The acquisition Genus Stylatula Verrill, 1864 of exogenous algal symbionts by an Octocoral after Stylatula sp.* bleaching. Science 304:1490-1492. Family TELESTIDAE Milne Edwards & Haime, 1857 Sánchez, J. A. 2001. Systematics of the Southwestern Genus Carijoa Müller, 1867 Caribbean Muriceopsis Aurivillius (Cnidaria: Octo- Carijoa riisei (Duchassaing & Michelotti, 1860)* corallia) with description of a new species. Bull. Family BRIAREIDAE Gray, 1859 Biol. Soc. Wash. 10:160-180. Genus Briareum Blainville, 1830 Sánchez, J. A. 2004. Evolution and dynamics of Briareum asbestinum (Pallas, 1766) branching colonial form in marine modular Cni- Briareum polyanthes Duchassaing & Michelotti, 1860 darians: Gorgonian Octocorals. Hydrobiologia 530 Family ANTHOTHELIDAE Broch, 1916 (1):283-290. Genus Erythropodium Kölliker, 1865 Erythropodium caribaeorum (Duchassaing & Michelotti, Sánchez J. A., and H. R. Lasker. 2003. Patterns of Mor- 1860) phologic Integration in Branching Colonies of Ma- Family PLEXAURIDAE Gray, 1859 rine Modular Organisms: supra-module organiza- Genus Plexaura Lamouroux, 1812 tion in Gorgonian Corals. Proc. Roy. Soc.B -Biol. Sci. Plexaura homomalla (Esper, 1792) 270:2039-2044. (DOI: 10.1098/rspb.2003.2471) Plexaura kükenthali Moser, 1921 Sánchez, J. A., J. M. Díaz, and S. Zea 1997. Gorgonian Plexaura kuna Lasker et al., 1996 communities in two contrasting nvironments on Genus Pseudoplexaura Wright & Studer, 1889 oceanic atolls of the southwestern Caribbean. Bull. Pseudoplexaura porosa (Houttuyn, 1772) Mar. Sci. 61(2):61-72. Pseudoplexaura flagellosa (Houttuyn, 1772) Sánchez J. A., C. S. Mcfadden, S. C. France, and H. R. Pseudoplexaura wagenaari (Styasny, 1941) Lasker. 2003. Molecular Phylogenetic analyses of Pseudoplexaura crucis Bayer, 1961 shallow-water Caribbean octocorals. Mar. Biol. 142: Genus Eunicea Lamouroux, 1816 975-987. Eunicea mammosa Lamouroux, 1816 Sánchez J. A., H. R. Lasker, E. G. Nepomuceno, J. D. Eunicea succinea (Pallas, 1766) Sánchez, and M. J. Woldenberg. 2004. Branching Eunicea laxispica Eunicea fusca Duchassaing & Michelotti, 1860 and Self-Organization in Marine Modular Colonial Eunicea flexuosa (Lamouroux, 1821) Organisms: a Model. Am. Nat. 163(3) (0003-0147/ Eunicea laciniata Duchassaing & Michelotti, 1860 2004/16303-20458). (NEW) Eunicea tourneforti Milne Edwards & Haime, 1857 Smith, G., L. D. Ives, I. A. Nagelkerken, and K. B. Eunicea asperula Milne Edwards & Haime, 1857 Ritchie. 1996. Aspergillosis associated with Car- Eunicea clavigera Bayer, 1961 ibbean sea fan mortalities. Nature 382:487. Eunicea knighti Bayer, 1961 Wirshing H. H., C. G. Messing, C. J. Douady, J. Reed, Eunicea calyculata (Ellis & Solander, 1786) M. J. Stanhope, and M. S. Shivji. 2005. Molecular Eunicea pallida Garcia-Parrado & Alcolado, 1997 evidence for multiple lineages in the gorgonian Eunicea sp. 1 family Plexauridae (Anthozoa: Octocorallia). Mar. Eunicea sp. 2 Biol. 147(2):497-508. Genus Muriceopsis Aurivillius, 1931 Yoshioka, P. M., and B. B. Yoshioka 1991. A compari- Muriceopsis flavida (Lamarck, 1815) son of the survivorship and growth of shallow- Muriceopsis petila Bayer, 1961 water gorgonian species of Puerto Rico. Mar. Ecol. Muriceopsis bayeriana Sánchez, 2001 Prog. Ser. 69:253-260. Genus Plexaurella Kölliker, 1865 Plexaurella dichotoma (Esper, 1791) Plexaurella nutans (Duchassaing & Michelotti, 1860) Plexaurella fusifera Kunze, 1916 APPENDIX Plexaurella grisea Kunze, 1916 Plexaurella sp. List of 61 octocorals (Anthozoa: Cni- Genus Muricea Lamouroux, 1821 daria) observed in the reefs and sand/ Muricea muricata (Pallas, 1766) rubble slopes in the vicinity of Bocas del Muricea atlantica Kükenthal, 1919 Muricea laxa Verrill, 1864 Toro, Panama (1-30 m). All species were Muricea elongata Lamouroux, 1821 collected and the identification confirmed Muricea pinnata Bayer, 1961 through microscopic observations (J. A. Family GORGONIIDAE Lamouroux, 1812 Sánchez, Bocas del Toro, Invertebrate Genus Pseudopterogorgia Kükenthal, 1919 Workshop 2003). Voucher specimens are Pseudopterogorgia bipinnata (Verrill, 1864) Pseudopterogorgia acerosa (Pallas, 1766) deposited at Bocas del Toro field station Pseudopterogorgia elisabethae Bayer, 1961 (Smithsonian Institution, Panama). Species Pseudopterogorgia americana (Gmelin, 1791) with a star (*) are aposymbiotic octocorals. Pseudopterogorgia rigida (Bielschowsky, 1929) 522 J. A. SÁNCHEZ AND H. H. WIRSHING

Pseudopterogorgia hystrix Bayer, 1961 Lophogorgia punicea (Milne Edwards & Haime, 1857)* Genus Gorgonia Linnaeus, 1758 Lophogorgia cardinalis Bayer, 1961* Gorgonia ventalina Linnaeus, 1758 Genus Leptogorgia Milne Edwards & Haime, 1857 Gorgonia sp. cf. flabellum Linnaeus, 1758 Leptogorgia stheno (Bayer, 1952)* Gorgonia mariae Bayer, 1961 Leptogorgia euryale (Bayer, 1952)* Genus Pterogorgia Ehrenberg, 1834 Leptogorgia medusae (Bayer, 1952)* Pterogorgia citrina (Esper, 1792) Family ELLISELLIDAE Valenciennes Pterogorgia anceps Pallas Genus Ctenocella Valenciennes, 1955 Pterogorgia guadalupensis Subgenus Ellisella Gray, 1858 Pterogorgia sp. Ctenocella (Ellisella) schmitti (Bayer, 1961)* Genus Lophogorgia Milne Edwards & Haime, 1857 Ctenocella (Ellisella) sp. cf. barbadensis* Leptogorgia sp.* Ctenocella (Ellisella) sp.*