Isostichopus fuscus ( Ludwig, 1875 )

Borrero-Pérez, Giomar H., Solís-Marín, Francisco A. & Lessios, Harilaos, 2024, Understanding the color variability and resolving taxonomic confusion in the sea cucumber Isostichopus badionotus (Echinodermata, Holothuroidea): a revision of the genus Isostichopus, European Journal of Taxonomy 949 (1), pp. 1-96 : 63-72

Isostichopus fuscus ( Ludwig, 1875)

Figs 1 I’–O’, 3A–D, 4D, 5B, 9, 10D, 11D, 19–21; Tables 1–3

Stichopus fuscus Ludwig, 1875: 97–98 .

Stichopus badionotus – Selenka 1867: 316 (partim). — Clark 1922: 56 (partim).

Stichopus fusus – Théel 1886: 256. Typographic error.

Stichopus fuscus – Ludwig 1898: 5, pl. 1 figs 1–5. — Clark 1910: 350; 1922: 45 (as unidentifiable form). — Deichmann 1937: 163; 1938: 363. — Steinbeck & Ricketts 1941: 410.

Isostichopus fuscus – Deichmann 1958: 280–281, pl. 1 figs 1–3. — Hickman 1998: 56, appendix a, p. 65. — Solís-Marín et al. 2009: 138, fig. 44. — Borrero-Pérez & Vanegas-González 2022: 329– 334. — Purcell et al. 2023: 144–145.

Original name

Stichopus fuscus Ludwig, 1875 .

Current status

Isostichopus fuscus ( Ludwig, 1875) .

Name-bearing type

Syntype ZMH E.2689 .

Type locality

Manchalilla, Ecuador; proposed by Deichmann (1958) instead of Patagonia (probably wrong), as Ludwig (1898) reported the species in this locality.

Diagnosis

Reticulated, uniform chocolate brown, with stains or reddish color in the background with yellowish large wart-like dorsal papillae ( Figs 1 I’–O’, 21); large tables with a circular spire well developed in the cloaca ( Figs 11D , 19C , 20F ); distributed in the East Pacific Ocean ( Fig. 5B ); mtDNA divergence from other species of the genus> 6.1% in COI-Fr1 (barcoding region),> 9.5% in COI-Fr2 and> 5.2% in 16S ( Table 2 ).

Material examined

EAST PACIFIC – Mexico • 3 specs, Selenka’s syntype of S. badionotus (L = 180 to 220 mm); Guerrero, Acapulco ; A. Agassiz, collector number 239 leg.; MCZ HOL-743 • 1 spec. (L = 140 mm); Sonora, Pelican Point ; 30 Jul. 1969; B. Burch leg.; USNM E21411 • 1 spec. (L = 210 mm); Guerrero, Acapulco ; 4–6 Aug. 1982; Hassler exped.; MCZ HOL-742 • 2 specs (L = 210–230 mm); Oaxaca, Puerto Escondido ; 25–26 Mar. 1940; E.F Ricketts and J Steinbeck leg.; MCZ HOL-2113 • 1 spec.; Guerrero, Zihuanejo Bay, Playa Las Gatas ; depth 3 m; 14 Oct. 1995; M. Olivares leg.; rocky bottom; ICML-UNAM 5.13.52 • 1 spec.; Nayarit, Punta Mita, Corral del Mangle ; 21.7700583° N, 105.5174277° W; depth 5 m; 29 Jul. 1995; C. Vizcarra leg.; rocky bottom; ICML-UNAM 5.13.54 • 2 specs; Michoacán, Faro de Bucerías ; 18.3468861° N, 103.5119833° W; depth 4 m; 20 Dec. 1993; J. Mendoza. leg.; rocky bottom; ICML-UNAM 5.13.55 • 2 specs; Oaxaca, Puerto Angelito ; 15.6522222° N, 96.48527777° W; depth 4 m; 25 Jan. 1995; S. Ramírez leg.; rocky bottom; ICML-UNAM 5.13.63 • 1 spec.; Michoacán, Lázaro Cárdenas municipality, Pichilinguillo ; 18.0719444° N, 102.76° W; depth 6 m; Dec. 2006; rocky bottom; ICML-UNAM 5.13.69 • 4 specs; Baja California Sur , west coast of Mexico, Magdalena Bay ; 24.5138889° N, 112.0066666° W; depth 4 m; 18 Oct. 1987; F. Solís-Marín leg.; rocky bottom; ICML-UNAM 5.13.73 • 1 spec.; Guerrero, Zihuanejo Bay, Playa La Pedregosa Grande ; 17.6183333° N, 101.5311111° W; depth 5 m; 20 Oct. 1992; J. Vargas leg.; rocky bottom; ICML-UNAM 5.13.77 • 2 specs; Sonora, Laguna de Yavaros, La Barra pier; 31 Oct. 1970; Orbe leg.; rocky bottom; ICML-UNAM 5.13.78 • 1 spec.; Colima, Manzanillo, Peña Blanca ; 4 Oct. 1993; G. Ramírez leg.; ICML-UNAM 5.13.110 • 1 spec.; Colima, Revillagigedo Archipelago, Socorro Island ; 18.7249167° N, 110.9392222° W; depth 15–17 m; 29 Nov. 1997; H. Reyes leg.; ICML-UNAM 5.13.115 • 1 spec.; Nayarit, Isla Isabel ; 21.8425° N, 105.8861111° W; 20 Nov. 1997; J. Carballo leg.; rocky bottom; ICML-UNAM 5.13.121 • 1 spec.; Guerrero, Caleta de Campos, El Corralón ; 18.0697833° N, 102.7438333° W; depth 3 m; 2 Mar. 2010; F. Solís-Marín leg.; ICML-UNAM 5.13.126 • 1 spec.; Michoacán, Lázaro Cárdenas municipality, Mexcalhuacán ; 18.049° N, 102.6591666° W; depth 6–11 m; 4 Mar. 2010; F. Solís-Marín leg.; ICML-UNAM 5.13.127 • 1 spec.; Colima, Manzanillo, Canal de Tepalces ; 19.0047944° N, 104.2572305° W; depth 1 m; 15 Aug. 2010; E. Celaya leg.; ICML-UNAM 5.13.128 • 1 spec.; Jalisco, Puerto Vallarta, Majahuitas ; 20.5066667° N, 105.3855° W; depth 15 m; 23 Jan. 2010; F. Solís-Marín leg.; ICML-UNAM 5.13.130 . – USA • 1 spec. (L = 140 mm); California, San Diego ; 4–6 Sep. 1982, 18–22 Aug. 1982; Hassler exped.; MCZ HOL-758 . – Colombia • 1 spec. (L = 180 mm); Chocó, Piedra Bonita ; 5.59403° N, 77.5034° W; depth 12 m; 18 Oct. 2016; G. Borrero-Pérez, Riscales 2016 leg.; rocky bottom, among rocks; INV EQU4323 • 1 spec. (L = 115 mm); same data as for preceding; INV-EQU4324 • 1 spec.; Chocó, Chicocora ; 6.68023° N, 77.4305° W; depth 12 m; 18 Oct. 2016; G. Borrero-Pérez, Riscales 2016 leg.; rocky bottom, among rocks, IfRIC154R; INV TEJ1960 • 1 spec. (L = 120 mm); Chocó, Nuqui ; 5.5691389° N, 77.52369444° W; depth 10 m; 18 Sep. 2003; G. Borrero-Pérez, Nuqui 2003 leg.; rocky bottom, among rocks; INV EQU2746 • 1 spec. (L = 40 mm); Chocó, Piedra de Oswaldo ; 5.54429° N, 77.51554° W; depth 15 m; 19 Apr. 2016; J. Vanegas-González, Riscales 2016 leg.; rocky bottom, among rocks; INV EQU4229 • 1 spec. (L = 145 mm); Chocó, Punta Arusí ; 5.61111° N, 77.48512° W; depth 6 m; 24 Apr. 2016; J. Vanegas-González, Riscales 2016 leg.; rocky bottom, among rocks; INV EQU4230 • 1 spec. (L = 130 mm); Chocó, Parguera ; 5.60989° N, 77.50409972° W; depth 15.5 m; 20 Apr. 2016; J. Vanegas-González, Riscales 2016 leg.; rocky bottom, among rocks; INV EQU4231 • 1 spec. (L = 170 mm); Chocó, Punta Faro ; 6.82467° N, 77.68996° W; depth 12 m; 25 Oct. 2016; G. Borrero-Pérez, Riscales 2016 leg.; rocky bottom, among rocks; INV EQU4321 • 1 spec. (L = 165 mm); same data as for preceding; INV EQU4322 • 1 spec. (L = 130 mm); Chocó, Piedra de Rodrigo ; 6.78391° N, 77.69358° W; depth 19 m; 26 Oct. 2016; G. Borrero-Pérez, Riscales 2016 leg.; rocky bottom, among rocks; INV EQU4325 • 1 spec.; Malpelo Island ; 29 Feb. 1972; C. Birkeland leg.; USNM E23715 . – Panama • 1 spec.; Panama, Taboguilla Island ; 8.8005667° N, 79.52332777° W; depth 10 m; 31 Aug. 2015; H. Lessios and A. Calderón leg.; rocky bottom, hidden under rocks; IfTa210; Tiss-IfTa210 • 1 spec. (L = 150 mm); same data as for preceding; IfTa211; USNM 1659483 • 1 spec. (L = 200 mm); same data as for preceding; 17 Aug. 2015; IfIP322; USNM 1659482 • 1 spec. (L = 150 mm); same data as for preceding; IfTa213; USNM 1682794 • 1 spec. (L = 155 mm); same data as for preceding; If212; MBMLP-If212 • 1 spec.; Gulf of Panama ; 7.6666667° N, 78.75° W; 6 Sep. 1972; ICML-UNAM 5.13.98 . – Ecuador • 1 spec. (a piece of tegument); Galapagos Islands, San Cristobal Island ; depth 15 m; 1 May 1993; P. Humann leg.; USNM 1017480 • 1 spec. (L = 57 mm); Galapagos Islands, James Island ; 21 Jan. 1938; RV Velero III, Hancock Pacific exped.; MCZ HOL-1921 • 1 spec.; Galapagos Islands, Devil’s Crown ; depth 15 m; 17 Aug. 1998; Hickman, Cleveland leg.; 98- 502; UF 9112 • 1 spec.; Galapagos Islands, Champion ; 17 Aug. 1998; Hickman, Cleveland leg.; 98-503; UF 9651 • 1 spec.; Galapagos Islands, San Cristobal, Kicker Rock ; depth 21 m; 5 May 1996; Hickman, Cleveland leg.; under rock; 96 19; UF 9672 . – Peru • 2 specs; Isla Lobos de Afuera ; 6.9666667° S, 80.75° W; depth 5 m; 10 Jun. 1999; F. Solís-Marín leg.; rocky bottom; ICML-UNAM 5.13.72 .

GULF OF CALIFORNIA – Mexico • 1 spec. (L = 210 mm); La Paz, El Mogote ; 21–22 Mar. 1940; E.F Ricketts and J Steinbeck leg.; MCZ HOL-2115 • 6 specs; Sinaloa, Mazatlán Bay, Isla de Venados ; 23.3980556° N, 106.4722222° W; depth 7 m; 15 Feb. 1979; M.E. Caso. leg.; ICML-UNAM 5.13.23 • 1 spec.; Baja California Sur, La Paz Bay, Canal San Lázaro, Salvierra wreck; 24.3852778° N, 110.3008333° W; depth 20 m; 15 Aug. 1996; R. Murillo. leg.; rocky bottom; ICML-UNAM 5.13.56 • 1 spec.; Baja California Sur, La Paz Bay, Puerto Balandra ; 24.3284028° N, 110.3344222° W; depth 2 m; 28 Apr. 1969; G. Mendez leg.; rocky bottom; ICML-UNAM 5.13.57 • 1 spec.; Baja California Sur, La Paz Bay, Los Islotes ; 24.5858333° N, 110.3886111° W; depth 6 m; 20 Mar. 1993; C. Sánchez leg.; rocky bottom; ICML-UNAM 5.13.64 • 1 spec.; Baja California Sur, La Paz Bay, Isla Espíritu Santo, San Gabriel Bay ; 24.4405167° N, 110.3744416° W; depth 3 m; 25 Nov. 1963; M. Beltrán leg.; rocky bottom; ICML-UNAM 5.13.67 • 2 specs; Baja California Sur, La Paz Bay, Puerto Balandra ; 24.3283333° N, 110.3341666° W; depth 3 m; 29 Apr. 1969; M.E. Caso leg.; rocky bottom; ICML-UNAM 5.13.81 • 1 spec.; Sinaloa, Mazatlán Bay, Isla de Lobos ; 23.2302778° N, 106.4619444° W; 17 Nov. 1998; L. Carballo leg.; ICML-UNAM 5.13.122 • 1 spec.; Sonora, San Carlos ; 27.0156806° N, 111.0915° W; 16 Jan. 2010; F. Solís-Marín leg.; ICML-UNAM 5.13.129 • 2 specs; Baja California, Bahía de Calamajue ; 29.775° N, 114.2333333° W; May 1998; D. Gonzalez leg.; ICML-UNAM 5.13.116 • 1 spec.; Baja California Sur, South of Isla Santa Catalina ; 25.5148333° N, 110.778° W; depth 20–30 m; 24 Aug. 2008; F. Solís-Marín leg.; rocky bottom; ICML-UNAM 5.13.125 .

Description

EXTERNAL APPEARANCE. Medium to large size species up to 280 mm ( Solís-Marín et al. 2009), preserved specimens examined 40–230 mm long (n = 19). Body loaf-like, length/width ratio 3.0 ±0.9 (n = 19, 1.6–5.8). Living specimens convex in cross section, some specimens somewhat quadrangular, rounded in both anterior and posterior parts ( Fig. 21 ). Body wall firm and 2–7 mm thick (MCZ HOL-743, L = 220 mm). Anus supra-terminal, circular and surrounded by large papillae. Mouth directed ventrally, encircled by a collar of large papillae and 20 peltate tentacles; tentacles 10–12 mm long, shield 9–10 mm wide with deep 3–4 mm indentions (MCZ HOL- 743, 220 mm). Dorsal papillae large, not variable in shape, wart-like, even in small specimens (INV EQU4229, L = 40 mm, 2 mm high and 2.5 wide; MCZ HOL-743, L = 220 mm, 2–4 mm high and 4–5 mm wide), irregularly arranged, fewer on the dorso-lateral side ( Figs 19A , 21 ). Lateral row papillae large and rounded, sharply defining the dorsal and ventral surface in both juveniles and adults, in living or preserved specimens ( Figs 19A , 21 ). Preserved specimens usually with prominent papillae. Ventral surface densely covered with cylindrical pedicels, arranged in three longitudinal rows ( Fig. 21 ).

COLOR AND BODY WALL APPEARANCE. Body wall smooth and opaque, nor translucent, nor rugose in live and preserved specimens more than 110 mm long ( Figs 1 , 21). Color highly variable, four main patterns recognized ( Figs 1 , 21): (1) Chocolate brown uniform pattern (BU) ( Fig. 1 J’): uniform chocolate brown and yellow papillae. (2) Chocolate brown and stains pattern (BS) ( Fig. 1 I’): chocolate brown background with clearer stains and yellow papillae. (3) Chocolate brown and reddish pattern (BR) ( Fig. 1 K’): chocolate brown in the dorsal side that gradually changes to reddish in the lateral and ventral sides; some small specimens reddish in the entire body. (4) Reticulated pattern (R) ( Fig. 1 L’–O’): beige or white background with a reticulum of darker green or brown, which may also appear as small white or beige spots on a darker green or chocolate brown background. Some small specimens of this color. Large, rounded, and yellowish papillae are common in the four-color patterns. Larger specimens preserved in alcohol retain these color patterns. Dorsal papillae in the preserved specimens brown-yellowish and conspicuous. These characteristic dorsal papillae also present in Selenka’s specimens, mostly in the posterior part of the body ( Fig. 19A ). Small juveniles with semi translucent body wall; color in preserved juvenile (40 mm long) uniform beige (INV EQU4229, Fig. 21M ), the same as that of adults in a live juvenile specimen (80 mm long) ( Fig. 21N ).

INTERNAL ANATOMY (based on MCZ HOL-743, L = 220 mm). Calcareous ring stout, radial elements roughly quadrangular (6 mm wide and 7 mm long), with four anterior small lobes and short posterior projections in the dorsal radial plates; three ventral radial plates with shorter posterior projections; interradial elements almost as wide as radial elements and half as short (6 mm wide and 3 mm long) pointed anteriorly and concave posteriorly ( Fig. 4D ). Stone canal irregularly helical, about 24 mm long including the madreporite of 9 mm, attached to the mesentery, partially calcified, and pointed at the end. Tentacle ampullae about 18–30 mm long and 2 to 2.5 mm wide. One Polian vesicle, about 25 mm long by 9 mm wide. Gonads in two tufts, one on either side of dorsal mesentery, branched in cylindrical tubes, filled with eggs ( Fig. 11D ). Longitudinal muscles 5–8 mm wide, divided and attached to body wall. Respiratory trees inserted near the anterior part of cloaca, a common stem present, divided in a right tree and a left shorter one.

OSSICLES (based on MCZ HOL-743, MBMLP-IfTa212, INV EQU4229, INV EQU4324, INV EQU4323 and USNM 1682794 (SEM images, Fig. 19 ), specimens 40–220 mm long).

Dorsal papillae with tables, thin C-shaped rods, perforated plates, and large, curved rods ( Figs 10D , 20A ). Perforated plates not found in the 40 mm specimen, only in specimens longer than 115 mm. C-shaped deposits, few and rarely S-shaped, ranging from 46 to 109 (x = 71) µm long; usually at the papilla tip, sometimes at the papilla base, abundant or scarce even in different samples of tegument of the same specimen. No clear pattern in the C-shaped rod length in relation to body length ( Fig. 9A ). Numerous table ossicles 34–65 (x = 50) μm high and 42–95 (x = 63) µm across the disc. Spires composed of four pillars usually parallel, ending in triplets of blunt spines forming a wide crown and one crossbeam connecting adjacent pillars; in 40 mm long specimen a crown of many minute spines. Disc margins smooth and wide; discs with one rounded central perforation and 8 to 12 peripheral holes, usually arranged in one simple ring. Tables near the top of the papillae taller and larger, with several extra perforations arranged in more than one ring, and more square than those from the body wall ( Fig. 10D ). Changes of tables in size and shape during growth are not pronounced; lower tables in 40 mm specimen (34–46 μm high; x = 41) than in larger specimens (41–65 μm high, x = 50) ( Figs 9B , 10D ); disc tables in smaller and larger specimens less wide than in those of middle size ( Figs 9C , 10D ). Few perforated plates, located at the papilla tip, with few large perforations, larger in the center of the plate; plates 103–151 µm across; slightly or strongly curved rods 192–329 µm long, with quadrangular projections, sometimes perforated in the central part of the rod ( Fig. 20A ).

Dorsal body wall with tables and few C-shaped rods, rarely S-shaped ( Figs 10D , 20A ). Similar in shape to tables at the papillae but narrower and smaller 33–69 (x = 47) μm high and 37–71 (x = 52) µm across the disc, with regular discs with one ring of 8–10 holes ( Fig. 10D ); few C-shaped rods 47–60 µm long, present only in some of the specimens.

Pedicels with tables, C-shaped rods, perforated plates, large and curved rods, and end plates ( Fig. 20B ). C-shaped ossicles 57–86 µm long in some specimens. Numerous table ossicles 27–45 (x = 38) μm high and 46–76 (x = 56) µm across the disc; shape of the tables similar to those from the dorsal papillae and body wall, but with the central perforation usually bigger and not rounded in some tables, 10–13 peripheral holes in a simple ring, and usually no extra perforations. Numerous elongated perforated plates, with many perforations larger and elongated in the center of the plate; plates 207–383 µm long; slightly or strongly curved rods 285–483 µm long, usually with perforated central expansions; end plates 674–678 µm across.

Ventral body wall with only tables and few C-shaped ossicles.

Tentacles with rods and tables ( Fig. 20C ). Table ossicles 38–61 μm across disc; spire low, composed of four pillars which can be incomplete, without crossbeams connecting adjacent pillars; discs with a large and not rounded central perforation with various peripheral holes (5 to 12) arranged in one ring; margins usually spinous. Numerous strongly or slightly curved spiny rods 91–654 µm long.

Mouth membrane with C-shaped rods, simple rods, and tables in some specimens ( Fig. 11D ). C-shaped ossicles 42–79 µm long; rods 73–124 µm long; some large tables 123 µm high and 164–230 µm across the disc, with well-developed spire, composed of several pillars joined at the top, forming a very dense crown of spines, without distinguishable crossbeams connecting adjacent pillars; spire usually flat. Table discs with many peripheral perforations, arranged in several rings with spinous and thin margins, sometimes reduced, same width as the spire.

Longitudinal muscles with only C-shaped ossicles 40 to 67 µm long ( Fig. 20D ). Posterior cloaca with C-shaped ossicles, 49–77 µm long and rods 87–191 µm long ( Fig. 11D ). Anterior cloaca with C-shaped ossicles 57 µm long; simple or bifurcated rods 135–234 µm long; large tables and irregular plate-like branched rods ( Fig. 20E ). Large tables with a well-developed spire, composed of several joined pillars; discs smooth but with spiny margins, with several central perforations and 26 to 65 or more small peripheral holes, arranged in several rings (table disc diameter 122–184 µm, spire width 26–65 µm) ( Fig. 11D ). Large tables with a circular well-developed spire, composed of 5 to 9 pillars, not joining at the top, with at least one crossbeam connecting adjacent pillars at the top; lateral edges of the pillars usually with pointed projections; discs and margins very spiny, discs having several central elongated perforations and 5 to 48 or more large peripheral holes, arranged in several rings (discs 90–99 µm high, 121–209 µm across disc, 59–105 µm spire width) ( Figs 11D , 19C , 20F ). Perforated plates symmetrically radial similar to table discs, without spire, 109–234 µm long ( Fig. 11D ). Respiratory trees with small tables 55 µm high and 60 µm across the disc similar to those in the body wall ( Fig. 20G ), and with some tables like those having circular spires from the anterior cloaca, 104–107 µm across the disc and 67–72 µm spire width. Intestine with spinose or smooth deposits in a cross shape 62–148 µm long, sometimes with bifurcated ends, and some C-shaped ossicles 41–99 µm long ( Fig. 20H ). Gonads with delicate and long rods 300–405 µm and some small tables 51–57 µm high and 54–60 µm across the disc ( Fig. 11D ).

Distribution

Eastern Tropical Pacific from Baja California, Mexico, to Peru, including the Gulf of California, islands and rocky reefs, including the Revillagigedos Archipelago and Socorro Island ( Mexico), Isla del Coco ( Costa Rica), Malpelo and Gorgona ( Colombia), Galápagos ( Ecuador), and Lobos de Afuera Islands ( Peru) ( Deichmann 1958; Maluf 1988; Hooker et al. 2005; Prieto-Ríos 2010; Purcell et al. 2023) ( Fig. 5B ). We examined one specimen (L = 150 mm) collected in the Western Central Pacific ( Republic of the Marshall Islands, Caroline Islands, Pohnpei Island, Ponape) and deposited at the Museum of Comparative Zoology (MCZ HOL-786). The specimen was initially identified as Stichopus variegatus Semper, 1868 (a currently unaccepted species) but changed to S. fuscus (and even S. badionotus in some of the labels). We found that ossicles match those of Isostichopus fuscus , but that the large papillae characteristic of I. fuscus were absent. This specimen would extend the geographic distribution of I. fuscus to the Central Pacific, but more information is required for confirmation. Purcell et al. (2023: 145) include the Indo-Pacific Cocos (Keeling) Islands (possibly confusing them with Isla del Coco, Costa Rica) in the distribution of the species. This, as well as the inclusion of Patagonia in the map of the species, clearly appear to be errors ( Purcell et al. 2023). Bathymetric distribution: shallow subtidal zone to 39 m ( Deichmann 1958; Maluf 1988).

Habitat

Isostichopus fuscus is common in rocky bottoms and coralline patches along the coast. Specimens can be exposed or semi-hidden. In Baja California, it is found in coral and rocky habitats ( Purcell et al. 2023). Along the Colombian Pacific coast, they were observed inside crevices, between rocks or semi-exposed (Borrero-Pérez pers. obs.). In the Galapagos, they prefer rocky bottoms where the seaweed Ulva sp. is predominant ( Toral-Granda & Martínez 2007) and they are more active at night ( Shepherd et al. 2003).

Remarks

Deichmann (1958) clarified the status of I. fuscus by recognizing three specimens of Selenka’s cotypes of I. badionotus as I. fuscus ( Fig. 19A ), proposing Manchalilla, Ecuador, as the type locality, and describing the differences between I. badionotus and I. fuscus . Populations of Atlantic I. badionotus and Pacific I. fuscus have been confirmed as different species by molecular markers ( Byrne et al. 2010). The character proposed by Deichmann (1958) to distinguish I. fuscus from I. badionotus was the proportion (profile) of the tables in lateral view, narrower tables in I. badionotus but almost square ones in I. fuscus . In our observations, comparison of the ratio of table height to width shows some differences ( Fig. 10 ). However, table profile can be a variable and subjective character and depends on whether the tables are from the papillae or the body wall (tables of both species are more square in papillae and narrower in the body wall). Isostichopus maculatus phoenius and I. maculatus maculatus also possess tables that are more square than narrow in the papillae. Although this character could help identify individuals, for example in specimens from fishery confiscations, it is better to combine table profiles with external characters and geographic origin to identify I. fuscus reliably. A new diagnostic character of I. fuscus , not reported previously are large tables with a well-developed circular spire in the cloaca ( Figs 11D , 19C , 20F ).

Color variability in I. fuscus was also recorded by Deichmann (1958), who proposed that the “Reticulated” pattern corresponded to younger specimens and “Chocolate-brown” to adults. We found juveniles and adults with both color patterns ( Fig. 21 ), and we also found other color patterns including a chocolate-brown and reddish pattern, as well as completely red juveniles, also recorded by Clark (1910) in a live specimen from Peru.

Examination of dorsal papillae in four specimens (and several that were not measured) of I. fuscus , from 40 mm to 180 mm long, showed that ossicles become more abundant in the largest specimens. The largest C-shaped ossicles were in 155 mm long specimens. Spines at the crown spires were thick and strong in the largest specimens. Table height and disc diameter increased with body length in specimens 40 to 155 mm, but they were smaller in the 180 mm specimen ( Fig. 9A–C ). In contrast to I. badionotus , large specimens of I. fuscus had wide discs, similar to those of I. maculatus phoenius .

Biology

Commercial interest and decline of the populations of I. fuscus motivated studies on its ecology and biology. This information is mainly from the Gulf of California and from the Galapagos, the main localities of fishery. Information about I. fuscus in other areas in the Eastern Pacific is scarce. Isostichopus fuscus is a long-lived, slow-growing species that reaches sexual maturity in 5 years, at which point individuals are approximately 21 cm long in the Gulf of California ( Herrero-Pérezrul et al. 1999; Herrero-Pérezrul & Reyes-Bonilla 2008). In the Galapagos, the reported size of first maturity is between 21 and 23 cm ( Toral-Granda & Martínez 2004). In the Gulf of California spawning occurs between May and September, influenced by the increase in water temperature ( Fajardo-León et al. 1995; Herrero-Pérezrul et al. 1999). In the Galapagos, reproductive activity has been reported throughout the year, spawning occurs every month one to four nights after the new moon, regardless of temperature ( Mercier et al. 2007; Toral-Granda 2008b). Isostichopus fuscus is gonochoric, although there have been some cases of hermaphroditism, which may be related to low population densities due to overfishing ( Herrero-Pérezrul et al. 1998). The larval pelagic period lasts from 22 to 27 days; newly settled juveniles measure 1 mm in length; at 72 days they reach 3.5 cm and at 110 days they are 8 cm long ( Hamel et al. 2003; Mercier et al. 2007). The success of fertilization in sea cucumbers is a function of the spatial dispersion of the broodstock, so that minimum density is important ( Bell et al. 2008). For populations of I. fuscus at Galapagos, a density of ~ 1.2 ind/m 2 (~12 000 ind/ha) was estimated to achieve 50% fertilization success ( Shepherd et al. 2004). Highest population densities of I. fuscus were 3500 ind/ha in Galapagos in 1999, before the establishment of fishing seasons ( Toral-Granda 2005). On the coast of mainland Ecuador, in the provinces of Santa Elena and South Manabí, mean density was estimated as 100 ind/ha ( Aguilar et al. 2011, 2013). Densities were 4300 ind/ha in Jalisco, Mexico, in 1991 (Girón et al. 1991 in Glockner 2014) and 3780 ind/ha in Bahía de los Ángeles, Baja California, in 1992 (Salgado-Castro 1992 in Glockner 2014). Estimated densities at Gorgona Island ( Colombia) ranged between 150 and 600 ind/ ha ( Palacios & Muñoz 2012). Along the northern Pacific mainland of Colombia, I. fuscus was common in 2003 and 2016 (G.H. Borrero-Pérez pers. obs.).

Hosting of the parasitic worm Anoplodium sp. (Platyhelminthes: Rhabditophora) was reported in I. fuscus ( Hamel et al. 2017) . The rate of infestation was 1 to 725 of flatworms per sea cucumber. Individuals with a high rate of infestation had gonads that were very small or absent. Combined with overfishing, the infestation by this parasite could seal the fate of I. fuscus in certain regions of the Eastern Pacific ( Hamel et al. 2017).

Conservation status

Isostichopus fuscus is fished legally and/ or illegally in Ecuador, Mexico, Panama, and Peru ( Purcell et al. 2012, 2023). Currently Isostichopus fuscus is included as “Endangered (EN)” in the IUCN Red List of Threatened Species ( Mercier et al. 2013). It is the only sea cucumber species included in Appendix III of CITES proposed by Ecuador ( Toral-Granda 2008b). In addition, I. fuscus is under special protection by Mexican law (DOF 2010 in Glockner-Fagetti et al. 2016) and it is included in the Red Book of Marine Invertebrates of Colombia ( Borrero-Pérez & Vanegas-González 2022). Isostichopus fuscus is one of the most valuable species in the genus. It is sold at US $ 1.4 per fresh specimen in Ecuador and for US $ 498–527 kg- 1 in China ( Purcell et al. 2023). The average maximum market price for “Endangered” sea cucumbers in the IUCN red list, including I. fuscus , is US $ 1030 kg-1. Maximum price of species listed as “Vulnerable” is US $ 158 kg-1, of species listed as “Of Least Concern” is US $ 124 kg-1 and of species listed as “Data Deficient” is US $ 106 kg-1 ( Purcell et al. 2014). These authors propose that market value is one of the factors that most drives the risk of extinction of these species.

Along the mainland coast of Ecuador, the commercial extraction of this species began in 1989. Two years later, due to stock depletion, it moved to the Galapagos, where a management plan was developed in 1999 ( Bruckner et al. 2003). Currently, there is a total ban on fishing the species off continental Ecuador ( Purcell et al. 2023). The population densities of I. fuscus at Galapagos ranged from 3500 ind/ha in 1999 to 500 ind/ha in 2004 ( Toral-Granda 2005). These data revealed an alarming decline in population density, despite “presumably robust” populations in 1999 after a five-year fishing ban. In 2009 and 2010 there was a new moratorium on fishing as the minimum population density of 1100 ind/ha (11 ind/ 100 m 2), was not met ( Purcell et al. 2023). Currently, in the Galapagos Islands there are several management strategies that include a total allowable catch, minimum catch size (20 cm fresh or 7 cm dry), no-take reserves, a two month fishing season, and access only to artisanal fishers who are permanent residents of the islands ( Purcell et al. 2023).

In Mexico, commercial exploitation of I. fuscus started in 1988, on the western coast of the Baja California Peninsula ( Herrero-Pérezrul 2004). In the early 90s, the demand for this resource motivated the assessment of I. fuscus populations at new sites with fishing potential ( Glockner 2014). Population densities decreased from 1991–1992 to 2013 in localities surveyed such as Jalisco (4300 ind/ha in 1991, 60 ind/ha following years) and Bahía de los Ángeles (3780 ind/ha in 1992, 1000 ind/ha in 2005–2007, 700 ind/ha in 2013) (Girón et al. 1991; Girón & González 1992; Salgado-Castro 1992 all in Glockner 2014). The population density decreased by 82% during the time or evaluation and the average size of the individuals decreased by 26% ( Glockner 2014). The management measures of the species, such as limits to total allowable catch, establishment of minimum catch size, and closing the fishery during the season of reproduction, have not been sufficient to ensure the sustainable extraction of this species in Bahía de los Ángeles ( Herrero-Pérezrul & Reyes-Bonilla 2008; Glockner 2014). The observed values of density and mean length apparently affected reproductive success, because recruitment was low ( Glockner-Fagetti et al. 2016). Purcell et al. (2023) also report several management strategies in Mexico, including the establishment of a fishing season (October–May), a minimum legal size (400 g or 20 cm), annual permits and no-take reserves where the smallest individuals are found.

Preoccupation about the conservation of this species in regions besides Galapagos and Mexico is also justified because of the incessant growth of demands by Asian markets. Of concern is also that most of the known population densities in the eastern Pacific are lower than the estimated density proposed by Shepherd et al. (2004). In addition, the population densities after the fishing are lower than 1100 ind/ha, the threshold reference point presented by Purcell et al. (2023) for I. fuscus in Galapagos.

In Panama, there are reports of illegal extraction of I. fuscus and other species of sea cucumbers at the Perlas Islands and at the island of Coiba. Between 2004 and 2005, 689 kg dry weight of sea cucumbers were exported to Hong Kong ( China) from Panama ( Vergara-Chen et al. 2015). However, Executive Decrees 157-2003 and 217-2009 instituted a ban on harvest, possession, and commercialization of this organism ( Vergara-Chen et al. 2015). There are no fishing records on I. fuscus in Colombia and Peru. A first attempt to breed I. fuscus in land-based installations on the coast of Ecuador was reported by Mercier et al. (2004). Ongoing projects seeking to restore the sea cucumber population are being developed at the Provincia Santa Elena, Ecuador (https://www.eluniverso.com/vida/ 2017/05/21 / nota/6191473/proyecto-busca-repoblar-pelado-pepinos-mar-spondylus).

Figures

Fig. 1 (continued on next page). Color patterns of species and subspecies of Isostichopus Deichmann, 1958. A–J. Isostichopus badionotus (Selenka, 1867). A. Pink background and dark brown spots (Chips pattern – CH) (BT99, Panamá). B. Close-up of A, note large dark brown spots and small dots. C. Light brown background and darker ocellar spots (CH pattern) (INV TEJ1125-Ma10, Colombia). D. Close-up of C, note large ocellar spots and small black dots. E. Uniform black background (Uniform pattern – U) (BT59, Panamá). F. Beige background color with a reticulum of darker brown and yellow papillae (Reticulated pattern – R) (USNM 1659460-BT20, Panamá). G. Close-up of F, reticulated pattern in detail. H. Reticulated pattern with brown papillae (R pattern) (INV TEJ1167-SM4R, Colombia). I. Close-up of H, reticulated pattern in detail. J. Black background and yellow papillae (Black and yellow pattern-BY) (INV TEJ1176-SM13, Colombia). K–Y. Isostichopus maculatus phoenius (Clark, (BI), Maximum Likelihood (ML), and Neighbour-Joining (NJ). BI and ML were performed, using the GTR evolutionary model and NJ using K2P distances. BI was performed with MrBayes ver. 3.2.6 (Ronquist & Huelsenbeck 2003); the data set was run twice, using four Markov chains for ten million generations; trees were sampled every 500th generation, the first 2.5 million generations were discarded, and a 50% majority tree was obtained. ML analysis was performed in MEGA X (Kumar et al. 2018); support was assessed with 1000 bootstrap reiterations.

Fig. 11. Light microscope photographs showing ossicles from the mouth membrane, anterior cloaca, posterior cloaca, and gonads of the species and subspecies of Isostichopus Deichmann, 1958. A. I. badionotus (Selenka, 1867) (mouth membrane and gonads from the lectotype MCZ HOL-509; anterior and posterior cloaca from USNM 1659457-IbBT116). B. I. maculatus phoenius (Clark, 1922) (all ossicles from the holotype MCZ HOL-1182). C. I. maculatus maculatus (Greeff, 1882) (all ossicles from the neotype USNM E16150; male gonads at the bottom from the neoparatype USNM E16151). D. I. fuscus (Ludwig, 1875) (mouth membrane from MCZ HOL-742; anterior cloaca from MBMLP- If212; posterior cloaca and gonads from MCZ HOL-743). E. I. macroparentheses (Clark, 1922) (mouth membrane, anterior and posterior cloaca from USNM E47524; gonads from the holotype MCZ HOL- 921). Photos by G. Borrero. Scale bars = 100 µm.

Fig. 19. Preserved specimens of Isostichopus fuscus (Ludwig, 1875) from Acapulco, Mexico and of Selenka’s syntype of I. badionotus (Selenka, 1867) (MCZ HOL-743, 160–175 mm long). A. Dorsal view of three specimens. B. Ossicles from dorsal papillae. C. Large tables with circular spire from the anterior cloaca. Photos by G. Borrero. Scale bars: A = 30 mm; B–C = 100 µm.

Fig. 20. Isostichopus fuscus (Ludwig, 1875) ossicles (specimen USNM 1682794-Ta213, 155 mm long). A. Thin C-shaped rods, tables, perforated plates and large, curved rods from dorsal body wall and papillae. B. Thin C-shaped rods, tables, perforated plates, large, curved rods and end plate (fragment) from ventral body wall and tube feet. C. Rods and tables from tentacles. D. Thin C-shaped rods from longitudinal muscles. E. Rods bifurcated from the cloaca. F. Large tables with a circular spire well developed in the anterior cloaca. G. Tables from respiratory trees. H. Rods in cross shape, simple rods, and C-shaped rods in the intestine. Photos by G. Borrero.

Fig. 5. Geographic distribution of species and subspecies of Isostichopus Deichmann, 1958. A. I. badionotus (Selenka, 1867) (gray circles), I. maculatus phoenius (Clark, 1922) (red squares) and I. maculatus maculatus (Greeff, 1882) (blue circles). B. I. fuscus (Ludwig, 1875) (green circles) and I. macroparentheses (Clark, 1922) (orange circles). Locations for I. badionotus and I. fuscus were constructed based on observation records in Global Biodiversity Information Facility data and from museum specimens. Locations forI. maculatus phoenius, I. maculatusmaculatus andI. macroparentheses were constructed based only on confirmed localities of collected or preserved museum specimens.

Fig. 21. Color patterns and morphological variation of Isostichopus fuscus (Ludwig, 1875) (DNA sequences and detailed information of some specimens are indicated in Table 1, see Photo ID column for correspondence). A–C, D–E-bottom, F-top, G–H. Specimens with “Reticulated” pattern from Taboguilla, Panama (Ta210) (A), Perlas Islands, Panama (B), North Chocó, Colombia (C, D–E-bottom dorsal and ventral view, F-top, G–H). D–E-top, I, K–L. Specimens with “Chocolate brown and reddish” pattern from North Choco, Colombia (I, D–E-top-dorsal and ventral view, K-small specimen completely red), and Perlas Islands, Panamá (L, small specimen completely red). J. Specimen with “Chocolate brown and stains” pattern from Mexico. F-bottom. Specimen with “Chocolate brown uniform” pattern from North Chocó, Colombia. M. Preserved juvenile from North Choco, Colombia (original coloration not recorded). N. Juvenile from Mexico, “chocolate brown uniform with yellow papillae” pattern. Photos: F–I by L. Chasqui; L by A. Calderón; J, N by C. Sánchez; A–E, K, M by G. Borrero. Scale bars: B, M = 10 mm; D–E = 30 mm; C, K, N = 20 mm.

Fig. 4. Comparison of the calcareous rings of species and subspecies of Isostichopus Deichmann, 1958. A. I. badionotus (Selenka, 1867). B. I. maculatus phoenius (Clark, 1922) (A–B showing calcareous rings from specimens of different sizes). C. I. maculatus maculatus (Greeff, 1882). D. I. fuscus (Ludwig, 1875). E. I. macroparentheses (Clark, 1922). Dimensions of the individuals from which each ring was obtained are shown next to their museum catalog number. Abbreviations: ip = interradial plate; rp = radial plate. Scale bar = 4 mm.

Fig. 10. Light microscope photographs of the same specimens as in Fig. 9 (see the length (L) for correspondence), comparing ossicle size and shape from dorsal papillae and dorsal body wall from small to large specimens from each of the species and subspecies of Isostichopus Deichmann, 1958. A. I. badionotus (Selenka, 1867). B. I. maculatus phoenius (Clark, 1922). C. I. maculatus maculatus (Greeff, 1882). D. I. fuscus (Ludwig, 1875). E. I. macroparentheses (Clark, 1922). Photos by G. Borrero. Scale bars = 100 µm.

Fig. 9. Box-plots comparing ossicle size from dorsal papillae from small to large specimens(along x axis) from each of the species and subspecies of Isostichopus Deichmann, 1958. A. Dorsal papillae: C-shaped ossicle length. B. Dorsal papillae: table height. C. Dorsal papillae: table disc diameter. Photos of the ossicles of the same specimens are presented in Fig. 10. Specimens IDs: I. badionotus (Selenka, 1867) L = 40 mm, USNM E11783; L = 130 mm, USNM 1659462-BT48; L = 195 mm, USNM 1659454- BT111; L = 230 mm, USNM 1659447–BT116; I. maculatus phoenius (Clark, 1922) L = 25 mm, INV EQU4565; L = 90 mm, USNM 1659481-Ga224; L = 125, USNM 1659472-BT192; L = 185, USNM 1659479-BT53; I. maculatus maculatus (Greeff, 1882) L = 55 mm, ASI1; L = 110 mm, ASI4; L = 150 mm, CV1; I. fuscus (Ludwig, 1875) L = 40 mm, INV EQU4229; L = 115 mm, INV EQU4324; L = 55 mm, MBMLP-If212; L = 180 mm, INV EQU4323; I. macroparentheses (Clark, 1922) L = 20 mm, USNM 1659484-Be99; L = 40 mm, USNM 1659485-Be107; L = 65 mm, MCZ HOL-1214; L = 135 mm, USNM E47524.