Isostichopus Deichmann, 1958

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 : 17-81

Genus Isostichopus Deichmann, 1958

Type species

Stichopus badionotus Selenka, 1867

Description (after Deichmann 1958)

Medium to large species, length to 50 cm, body wall firm and thick. Highly variable coloration ( Fig. 1 ). Body convex to quadrangular in cross-section. Large lateral papillae, usually sharply defining dorsum and ventrum (or bivium and trivium). Dorsal papillae irregularly arranged and in different sizes and shapes: wart-like, spiky, or with small points. Sole well developed, with three bands of cylindrical podia. Single stone canal attached to the mesentery; calcareous ring with massive radial pieces with posterior projections of different sizes, and narrow interradial pieces with projections pointed anteriorly and concave posterior margins ( Fig. 4 ). Ossicles: dorsal papillae with tables; thin C- or S-shaped rods in varying numbers and sizes; large, curved rods with quadrangular projections, sometimes perforated in the middle ( Fig. 2S ); few perforated plates in the tip ( Fig. 2U ). Tables in a dense layer, low, squat, with a circular disc with 8 to 12 small holes, four pillars, single crossbeam, and a wreath of small spines at the crown ( Fig. 2A–B ); tables with reduced disc ( Fig. 2C ), additional holes in more than one ring ( Fig. 20A ), or larger and modified discs also present ( Fig. 2D ), mainly at the top of papillae. Dorsal body wall with tables and a few thin C- or S-shaped rods only. Ossicles in dorsal papillae and body wall change during growth, though drastic ontogenetic changes occurring only in I. macroparentheses . Pedicels with low tables with large and not rounded central perforation ( Fig. 2E ); thin C-shaped rods less frequent than in the dorsal papillae; large endplates ( Fig. 2W ); numerous perforated or supporting plates with numerous holes ( Fig. 2V ); slightly or strongly curved rods with broad perforated expansions in the middle ( Fig. 2T ); both plates and rods larger than those of dorsal papillae. Ventral body wall with only tables and a few C-shaped ossicles. Tentacles with strongly or slightly curved spiny rods in varying sizes ( Fig. 2O ) and small tables as those of the body wall, or modified with low and incomplete spires ( Fig. 2F ). Mouth membrane with thin C-shaped rods, simple rods, and large tables, not documented previously for the genus, with well-developed spire, composed of at least ten pillars joining at the top, forming very dense and thick crown of spines, without crossbeams; discs of the same width as the spire, or wider with several rings of holes and several central perforations ( Figs 2H , 7D, 11, 16D). Longitudinal muscles containing C-shaped rods and simple rods. Posterior part of the cloaca with C-shaped, simple or bifurcated rods ( Fig. 11 ); anterior part with simple, branched rods, irregular plate-like branched rods ( Fig. 2R ) and large tables, with well-developed and very dense and thick spire, some with circular spire, without clear crossbeams, wide discs with several rings of holes and several central perforations ( Fig. 11 ). Respiratory trees with small tables as those of the body wall or strongly spinose straight or cross-shaped rods and large tridimensional spheres ( Fig. 2X ), not documented previously for the genus. Intestine with spinose or smooth ossicles in a cross shape ( Fig. 2P ). Gonads with delicate and long rods ( Figs 2N , 11). Rosettes not present in Isostichopus .

Distribution

Tropical and subtropical shores of America and the west coast of Africa ( Fig. 5 ).

Key to the species of the genus Isostichopus Deichmann, 1958

1. C-shaped ossicles> 90 µm on average and 2–3 times as long as the tables are high; disc tables in dorsal papillae and body wall completely reduced in adults ( Figs 2C , 10E, 23A); tridimensional spheres and straight/spiky rods in the respiratory trees ( Fig. 23F ); color not variable, dorsal side light yellow-brown in background, with irregularly arranged blurred large and small darker brown spots ( Fig. 24 ); distributed in the Gulf of Mexico and Caribbean Sea, confirmed in few localities ( Fig. 5B ), not a common species ................................................................. I. macroparentheses ( Clark, 1922)

– C-shaped ossicles <90 µm on average; disc tables in dorsal papillae and body wall with complete ring of holes, not reduced in adults; color highly variable; common and abundant species ............ 2

2. Table ossicles from top of the dorsal papillae in two shapes ( Figs 10C , 13A ), large, regular Isostichopus tables 58–86 µm (average = 71 µm) ( Fig. 2B ) and modified “ maculatus ” tables 60– 108 µm (average = 86 µm) ( Fig. 2D ); whitish spot-like granules on the skin ( Figs 1 , 14); distributed in the Mid and East Atlantic ( Fig. 5A ) ................................. I. maculatus maculatus ( Greeff, 1882)

– Table ossicles from top of the dorsal papillae only regular Isostichopus tables 29–70 µm (average = 47 µm) ............................................................................................................................................... 3

3. Large wart-like dorsal papillae ( Figs 19 , 21 ); table ossicles from top of the dorsal papillae only regular Isostichopus tables squarer than narrow in profile ( Figs 10D , 20A ); large tables with a circular spire well developed in the cloaca ( Figs 11D , 19C , 20F ); distributed in the East Pacific Ocean ( Fig. 5B ) ..................................................................................................................... I. fuscus ( Ludwig, 1875)

– Dorsal papillae variable in size and shape; table ossicles from top of the dorsal papillae only regular Isostichopus tables square or narrow in profile; distributed in the West Atlantic Ocean ................. 4

4. Semi-translucent and rugose body wall; spiral lines in dorsal and lateral papillae ( Figs 1 , 17); worm-like rod ossicles in dorsal papillae ( Figs 15B , 16A ); calcareous ring with dorsal radial plates with short posterior projections ( Fig. 4B ) in large specimens (L = 185 mm); adult specimens living hidden during day associated with live corals, sponges, rubble, and rocks, exposed for only short time ( Fig. 18 ) ........................................................................... I. maculatus phoenius ( Clark, 1922)

– Opaque and smooth body wall; no spiral lines in dorsal and lateral papillae ( Figs 1 , 8 ); no worm-like rod ossicles in dorsal papillae ( Fig. 7A ); calcareous ring with dorsal radial plates with long posterior projections turned inwards ( Fig. 4A ) in larger individuals (L = 160–235 mm); adult specimens living exposed on muddy, sandy, rocky substrates, seagrass beds and mixed bottoms ( Fig. 8 ) ................... ............................................................................................................. I. badionotus ( Selenka, 1867)

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. 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. 2 (see previous page). Ossicles of species and subspecies of Isostichopus Deichmann, 1958. A–H. Tables. A. Regular tables present in several parts of the body in the five species (1–2 = lateral view; 3 = top or dorsal view; 4 = ventral view). B. Large, regular tables, only present in I. maculatus maculatus (Greeff, 1882) (lateral view). C. Table with reduced disc, only present in the dorsal body wall of I. macroparentheses (Clark, 1922) adults (lateral view). D. Large tables with disc and spire modified, only present in the top of the dorsal papillae of I. maculatus maculatus – “modified maculatus tables” (lateral view, top view). E. Regular tables present in the ventral body wall and tube feet (top and lateral view). F. Tables with low and incomplete spires, present in the tentacles (top view). G. Tables with circular spire, several pillars, observed in the cloaca of I. fuscus (top and lateral view). H. Large tables with well-developed spires, several pillars forming a very dense and thick crown of spines, present in the mouth membrane and other internal organs (top and lateral view). I–T. Rods. I. Large thin C-shaped rods present in I. macroparentheses. J–K. Thin C, S-shaped rods present in the body wall, papillae and tube feet, and some internal organs. L. Thick C rods and worm-shaped rods present in the dorsal papillae of I. maculatus maculatus and I. maculatus phoenius (Clark, 1922). M. Simple rods present in several internal organs. N. Simple rods present in gonads. O. Simple rods present in the tentacles. P. Cross-shaped rods present in the intestine. Q. Branched rods present in several internal organs. R. Irregular plate-like branched rods present mostly in the anterior cloaca. S. Large, curved rods with quadrangular projections in the middle, present in the papillae. T. Large slightly or strongly curved rods with wide perforated expansions in the middle, present in the tube feet. U–X. Perforated plates. U. Perforated plates from papillae. V. Perforated plate from tube feet. W. End-plate. X. Tridimensional spheres only observed in the respiratory trees of I. macroparentheses. Photos by G. Borrero.

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. 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. 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. 23. Isostichopus macroparentheses (Clark, 1922), ossicles (specimen USNM E47524, 135 mm long). A. Thin C-shaped rods, tables, perforated plates, and large rods from the dorsal body wall and papillae. B. Tables, perforated plates, large rods and end plate from the ventral body wall and tube feet. C. Rods from tentacles. D. Rods from longitudinal muscles. E. Rods and C-shaped rods from the cloaca. F. Tridimensional sphere and straight rods from respiratory trees. G. Cross-shaped ossicles from intestine. Photos by G. Borrero.

Fig. 24. Color patterns and morphological variation of Isostichopus macroparentheses (Clark, 1922) (DNA sequences and detailed information of some specimens are indicated in Table 1, see Photo ID column for correspondence). A–B. Dorsal and ventral view of juvenile USNM 1659484-Be99 from Belize. C–D. Dorsal and ventral view of juvenile USNM 1659485-Be107 from Belize. E. Dorsal view of juvenile UF 20352 from Curaçao. F. Dorsal and ventral view of preserved specimens from British Virgin Islands (USNM E47524). G. Dorsal and ventral view of preserved specimens from US Virgin Islands (USNM E40833). H. Dorsal view of preserved specimen from English Harbor, Antigua Island (USNM E4391). I. Lateral view of preserved specimen from Carrie Bow Cay, Belize (USNM E18627). J–K. Dorsal and ventral view of specimen from Mexico. Photos: A–D, F–I by G. Borrero; J–K by F. Solís-Marín; E by Florida Museum of Natural History Data Collection. Scale bars: F = 20 mm; G = 10 mm; H–I = 1 mm each line.

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. 13. Isostichopus maculatus maculatus (Greeff, 1882) ossicles (neotype USNM E16150, 105 mm long). A. Thin C-shaped rods, modified maculatus tables, regular Isostichopus tables, perforated plates, and large, curved rods from the dorsal body wall and papillae. B. Tables, perforated plates, large, curved rods and end plate (not complete, ½ of the round plate) from the ventral body wall and tube feet. C. Rods and tables from tentacles. D. Rods from longitudinal muscles. E. Spinous irregular plate-like branched rods in the cloaca. F. Bifurcated spinous rod in the respiratory trees. G. Cross-shaped ossicles from the intestine. H. Simple rods from the gonads. Photos by G. Borrero.

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. 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. 15. Preserved specimens of Isostichopus maculatus phoenius (Clark, 1922). A. Dorsal and ventral view of the holotype from Buccoo Reef, Tobago (MCZ HOL-1182, 135 mm long). B. Holotype ossicles from dorsal papillae showing tables, thin C-shaped rods, worm-like rods, large, curved rods and perforated plates. C. Specimen from Antigua (USNM 1283367), dorsal and ventral view. D. Specimen from Antigua (MCZ HOL-4282), dorsal and ventral view. E. Specimen from Coco-Plum Key, Belize (USNM E18639), dorsal view. F. Specimen from Texas, Stetson Bank, USA (USNM 1080469), dorsal view. G. Specimens from Buccoo Reef, Tobago (MCZ HOL-1181; same locality as the holotype), dorsal view. Photos by G. Borrero. Scale bars: A = 10 mm; B = 100 µm; C–E, G = 20 mm; F = 10 mm.

Fig. 16. Isostichopus maculatus phoenius (Clark, 1922) ossicles (specimen USNM 1659477-BT43, 160 mm long). A. Thin C-shaped rods, tables, worm-like rods, perforated plates and large, curved rods from papillae and dorsal body wall. B. Thin C-shaped rods, tables, perforated plates, large, curved rods and end plate (not complete, broken at the outer edge) from ventral body wall and tube feet. C. C-shaped rods, simple rods and tables from tentacles. D. Large tables from mouth membrane. E. Thin C-shaped rods and simple rods from longitudinal muscles. F. Simple and bifurcated rods in a cross shape in the cloaca. G. Tables from respiratory trees. H. Cross-shaped rods from intestine. I. Simple rods from gonads. Photos by G. Borrero.

Fig. 18. In situ photographs of Isostichopus maculatus phoenius (Clark, 1922), showing the habitat of the species. A–I, L, P. Specimens from Bocas del Toro, Panama (L, the specimen was under the coral head; P, during the night). K, M–O. Galeta, Panama. J. Banco de las Ánimas, Colombia. Q–T. Mexico. Photos: B–D, F–G, P by A. Castillo; Q–T by F. Solís-Marín; J by N. Ardila; A, H–I, K–O by G. Borrero.

Fig. 8 (continued on next page). Color patterns and morphological variation of Isostichopus badionotus (Selenka, 1867) (DNA sequences and detailed information of some specimens are indicated in Table 1, see Photo ID column for correspondence). A–U, I’. Specimens with “Chips” color pattern from Bocas del Toro, Panamá (A–I), Neguanje, Colombia (J–L), La Guajira, Colombia (M–Q); juveniles from Neguanje, Colombia (R–U). V–B’. Specimens with “Uniform” pattern from Bocas del Toro (Panama) (V–X), La Guajira, Colombia (Y), Curaçao (Z), Magdalena, Colombia (A’–B’). C’–K’. Specimens with “Reticulated” pattern from Bocas del Toro, Panama (C’–E’), Juvenile from Neguanje, Colombia (F’), Punta Betin, Magdalena, Colombia (G’–I’), La Guajira, Colombia (J’–K’). L’–O’. Specimens with “Black and yellow” pattern from Bocas del Toro, Panamá (L’), Magdalena, Colombia (M’–O’). Photos: A–I, Q, V–X, C’–E’, L’, O’ by G. Borrero; R–U by G. Ospina; J–L by E. Acosta; M–P, Y, J’–K’ by E. Ortiz; Z, M’ by M. González-Wangüemert; G’–I’ by J. Gómez; and A’–B’, N’ by S. Zea. Scale bars = 10 mm.

Fig. 7. Isostichopus badionotus (Selenka, 1867) ossicles (specimen USNM 1659454-BT111, 190 mm long). A. Thin C-shaped rods, tables, perforated plates and large, curved rods from dorsal body wall and papillae. B. Thin C- and S-shaped rods, tables, perforated plates, large, curved rods and end plate (not complete, ¼ of the plate) from ventral body wall and tube feet. C. Rods and tables from tentacles. D. Large tables from mouth membrane. E. Thin C-shaped rods and simple rods from longitudinal muscles. F. Thin C-shaped rods, simple, cross-shaped and irregular plate-like branched rods in the cloaca. G. Table from respiratory trees. H. Cross-shaped ossicles from intestine. I. Simple rod from gonads. Photos by G. Borrero.