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PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES

Volume 54, No. 22, pp. 381-392, 11 figs. November 14, 2003

The Genus Roboastra Bergh, 1877 (Nudibranchia: Polyceridae: Nembrothinae) in the Atlantic Ocean

Marta Pola!, Juan Lucas Cervera!, and Terrence M. Gosliner ! Departamento de Biologia, Facultad de Ciencias del Mar y Ambientales, Universidad de Cadiz, Apdo. 40, 11510 Puerto Real (Cadiz), Spain, marta.pola@uca.es; * California Academy of Sciences, Golden Gate Park, San Francisco, CA 94118, USA, tgosliner@ calacademy.org.

The systematics of the phanerobranch dorid genus Roboastra Bergh, 1877 in the Atlantic Ocean is reviewed. Roboastra europaea Garcia-Gomez, 1985 is redescribed and its geographical range updated. Roboastra caboverdensis sp. nov. is described from material from Cape Verde Archipelago. The two species differ in their color pattern. The arrangement of the yellow lines or bands differs between the two species with denser lines in R. europaea. The base of the rachidian radular tooth is more curved in R. caboverdensis than in R. europaea and the upper cusp of the inner lateral tooth is bifid in R. europaea while in R. caboverdensis it is simple.

Se revisa la sistematica del género del dérido fanerobranquio Roboastra Bergh, 1877 en el Océano Atlantico. Se redescribe Roboastra europaea Garcia-Gémez, 1985, asi como se actualiza su distribuci6n geografica. Se describe Roboastra caboverdensis sp. noy a partir de material procedente del archipiélago de Cabo Verde. Las dos especies se diferencian por su patron cromatico. La disposicion de las lineas 0 bandas amar- illas difiere entre las dos especies, con un mayor numero de ellas en R. europaea. La base del diente radular raquideo esta mas curvada en R. caboverdensis y la cuspide superior del diente lateral interno es bifida en R. europaea mientras que en R. caboverdensis es simple.

The genus Roboastra was described by Bergh (1877). Until Burn’s revision (1967), this genus included three species: Roboastra gracilis (Bergh, 1877) (type species), R. rubropapulosa (Bergh, 1905) and R. luteolineata (Baba, 1936), all with an Indo-Pacific distribution. Burn described a new species, R. arika and suggested that R. rubropapulosa should be considered as a synonym of R. gracilis. Some years later, Farmer (1978) described R. tigris from the eastern Pacific. Garctia- Gomez (1985) then described R. europaea from the Strait of Gibraltar, the only species known from Atlantic-Mediterranean waters. Thus, to date, the genus Roboastra includes five named species. The only morphological data stem from the original descriptions, with the exception of the redescription of R. gracilis by Burn (op. cit.) and its taxonomic comparison with R. luteolineata by Hamatani and Baba (1976).

No additional studies have treated members of this genus except for that of R. tigris (Carté and Faulkner 1983, 1986) and, more recently, in which R. europaea was the focus of molecular phylo- genetic (Grande et al., 2002) and feeding ecology (Megina and Cervera 2003) studies. Recent col- lections from the Cape Verde Archipelago (West Africa) have yielded several specimens of a sec- ond undescribed Atlantic species of this genus.

381

382 PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES Volume 54, No. 22

In this paper, we describe the new species from Cape Verde. We also redescribe R. europaea, largely from material from the Iberian Peninsula, and update its geographical range.

MATERIAL AND METHODS

Specimens were dissected by dorsal incision. At least three specimens of each species were examined anatomically. Their internal features were examined and drawn under a dissecting micro- scope with a camera lucida. Particularly interesting soft parts were critical-point dried for scanning electron microscopy (SEM). Special attention was paid to the morphology of the reproductive sys- tem. The buccal mass was removed and dissolved in 10% sodiun hydroxide until the radula was isolated from the surrounding tissue. The radula was then rinsed in water, dried, and mounted for examination by scanning electron microscopy.

The materials examined are deposited in the California Academy of Sciences, San Francisco (CASIZ), the Museo Nacional de Ciencias Naturales, Madrid (MNCN) and the Museu Municipal de Funchal (Historia Natural) (MMEP).

SPECIES DESCRIPTIONS

Family Polyceridae Alder and Hancock, 1845 Subfamily Nembrothinae Burn, 1967

Genus Roboastra Bergh, 1877

Roboastra europaea Garcia-Gomez, 1985 (Figs. 1A, 2, 3A—-C, 4, 5, 6)

MATERIAL EXAMINED.— MNCN 15.05/46612. 1 specimen, 10 m depth, Torre, Marbella, Spain, July 1995, J.L. Gonzalez, 30 mm. CASIZ 166049. 1 specimen, 10 m depth, Torre, Marbella, Spain, September 1995, M.T.Barrea, 18 mm. CASIZ 166053. 2 specimen, Torre, Marbella, Spain, August 1996, K.L. Schick, 10.7m, 15 y 19 mm. MNCN 15.05/29203, 1 specimen, La Herradura, Granada, Spain, February 1993, A.Barrajon and M. Zarauz, 14 mm. MMF 31021, | specimen, 100 m depth, Funchal, Madeira, June 1999, 35 mm. MNCN 15.05/46613. 1 specimen, 20 m depth, Ponta de Baleeira, Sagres, Portugal, July 2002, M.Pola, 14 mm. MNCN 15.05/46613. 1 specimen, 20 m depth, Ponta de Baleeira, Sagres, Portugal, July 2002, M.A. Malaquias, 10 mm. Specimens were collected on rocks and were measured preserved.

DISTRIBUTION.— This species is known mainly from the Strait of Gibraltar and southern Iberian Peninsula (Garcia-Gémez 1985; 2002!; Cervera et al. 1988; Garcia-Gémez et al. 1989, 1991; Moreno and Templado 1998; Schick 1998; Megina 2000; Ocana et al. 2000; Sanchez-Tocino et al. 2000; Grande et al. 2002; Megina and Cervera 2003). One misidentified specimen of Plo- camopherus trom Madeira deposited at the Natural History Museum (London) (Reg. No. 1863.9.19.3), supposedly collected by Rev. R. Lowe, was correctly identified as belonging to Roboastra, very probably R. europaea. This conclusion has been strongly supported by the recent collection of one specimen (also photographed) of this species at Funchal Harbour.

This species has been also recorded in southwestern Portugal (Calado et al. 2002) and Catalunian coasts (northeastern Iberian Peninsula, Mediterranean Sea) (K.L. Schick, pers. com- mun. ).

| The specimens described by Garcia~-Gémez (2002) are the same of those described by this author in 1985 for the orig- inal description of this species.

POLA ET AL.: NUDIBRANCH GENUS ROBOASTRA IN THE ATLANTIC OCEAN 383

EXTERNAL MORPHOLOGY (Fig. 1A).— The body is elongate and limaciform. The preserved animals are 10-40 mm in length. The body surface is lightly uneven with the edge of the mantle not sharply angled. Foot is linear with a pointed posterior end of the foot. The head is rounded with a pair of perfoliate rhinophores (bearing 30-35 lamellae) that are completely retractile into their sheaths. The oral tentacles are well developed and grooved dorsolaterally along a part of their

A a

Portugal. B. Roboastra caboverdensis sp. nov., specimen from Banco Joao Valente, Ilha da Boavista, Cape Verde.

384 PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES Volume 54, No. 22

length. There are five non-retractile, bipinnate gills surrounding the anal papilla and forming a half circle; the three central gills are larger than the two lateral ones. The genital aperture is located mid- way between the gills and rhinophores, on the right side. The body wall is highly muscular. Regarding the color pattern, this species can exhibits two color phases. One of them has a grey or bluish grey ground color; the other has dark blue ground color. Both phases have several yellow or yellowish orange bands on the notum and both sides of the body. These bands are variable in num- ber, shape, length and width. The rhinophores and oral tentacles are grey/bluish grey to dark blue. The inner side of the gill rachis are yellow or yellowish orange. The outer side is frequently also this color, but rarely may be a dark blue. The secondary pinnae are grey/bluish grey to dark blue. The yellow/ yellowish orange areas are surroundend by a tiny violet line that is easily visible in most animals, except in the darkest individuals. The rhinophoral sheaths are also grey/bluish grey to dark blue (Fig. 1A).

INTERNAL MORPHOLOGY.— A general view of the internal anatomy can be seen in Figure 2. The buccal mass is elongate and tubular, well developed with a pair of elongate pouches opening into the digestive system at the junction of the oral tube and muscular pharynx (Fig. 3). The sali- vary glands are short and thick, entering on the buccal mass and flanking the esophagus. The labi- al cuticle lacks any armature. There is a well developed blood gland that is granular in texture. The radular formula of two specimens of 15 mm length (preserved) is 23 x 4.1.1.1.4. and that of the 30 mm specimen (preserved) has the formula 25 x 4.1.1.1.4. (Fig. 4A—C). The rachidian tooth (Fig. 4B) is broad, thin and curved at its base with three well-differentiated cusps. The inner lateral tooth

nL gr ae

Figure 2 (left). Roboastra europaea Garcia-Gomez, 1985. General arrangement of the internal organs, au = auricle, bb = buccal bulb, be = bursa copulatrix, bg] = blood gland, ca = cephalic artery, cg = cerebral ganglion, hg+dg = hermaphro- dite gland+digestive gland, in = intestine, oe = oesophagus, ot = oral tube, pe = pericardium, m = rhinophoral nerves, vd = vas deferens, ve = ventricle, vg = vestibular gland.

FIGURE 3 (right). Roboastra europaea Garcia~-Gémez, 1985. Detail of the oral tube and buccal mass.

POLA ET AL.: NUDIBRANCH GENUS ROBOASTRA IN THE ATLANTIC OCEAN 385

AVA

FiGuRE 4. Roboastra europaea Garcia-Gomez, 1985. CASIZ 166053, scanning electron micrographs of radula: A. Half-row of radular teeth. B. Rachidian teeth. C. Inner lateral tooth.

(Fig. 4C) has a strongly curved bifid inner cusp. The inner branch of this cusp is thin and smaller than the second. The outer cusp is undivided with a long spur-like denticle near the base. The remaining lateral radular teeth are quadrangular and lack cusps or denticulation and become small- er near the margin.

REPRODUCTIVE SYSTEM (Fig. 5).— The hermaphroditic duct widens into a S-shaped ampulla which has thick walls. The bursa copulatrix is rounded and larger than the seminal receptacle, which is elongate. The seminal receptacle has a short duct that connects to the vagina near the bursa. The deferent duct, which lacks a morphologically well-differentiated prostate, is long and coiled and ends in a dilated penial atrium. The vestibular gland is large with muscular walls, con- vex on one side and concave on the other. The penis is located within the distal end of this muscu- lar portion, and it is armed with, at least, three different kinds of hooked and chitinous spines arranged in helicoidal rows. The types of spines and their arrangement on the penis are shown in Figure 6.

386 PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES Volume 54, No. 22

FIGURE 5. Roboastra europaea Garcia-Gomez, 1985. Reproductive system, am = ampulla, be = bursa copulatrix, fgm = female gland mass, hd = hermaphrodite duct, p = penis, pr = prostate, rs = receptaculum seminis, v = vagina, vd = vas deferens, vg = vestibular gland.

FIGURE 6. Roboastra europaea Garcia-Gomez, 1985. CASIZ 166053, scanning electron micrographs of penis: A. Protruded penis and penial armature. B. Detail of distal spines. C. Detail of middle spines.

POLA ET AL.: NUDIBRANCH GENUS ROBOASTRA IN THE ATLANTIC OCEAN 387

Roboastra caboverdensis Pola, Cervera, and Gosliner, sp.nov. (Figs. 1B, 7, 8, 9A-C, 10, 11A—D)

TYPE MATERIAL.— HOLOTYPE: CASIZ 166047, 1 specimen, 38 m depth, 15 miles NW Santo Antao Island, Cape Verde Archipelago, July 2002. PARATYPES: MMF35083, 1 specimen, Tarrafal Island. Cape Verde Archipelago. December 1998, P. Wirtz, 25 mm. MNCN. 15.05/46614, 2 speci- men, 20 m depth, Banco Joao Valente, Boavista Island, Cape Verde Archipelago, August 2002, M.A. Malaquias, 26/30 mm (70 mm in life). CASIZ 166052, 2 specimen, 30 m depth, Banco Joao Valente, Boavista Island, Cape Verde, August 2002, M.A. Malaquias, 31/37 mm (70 mm in life). MNCN. 15.05/46617. 3 specimens, Boavista Island, August 2002, C. Grande, 13/15/18 mm. CASIZ 166050, 1 specimen, Sao Vicente, October 2002, G. Calado, 20mm. Specimens were col- lected on rocks and were measured preserved.

ETyMOLoGy.— The name caboverdensis refers to the Cape Verde Archipelago where this species is found.

DISTRIBUTION.— Thus far, known only from Cape Verde Archipelago.

EXTERNAL MORPHOLOGY.— The body is elongate and limaciform with a long and pointed posterior end of the foot. The preserved animals are 10-40 mm in length. The living animals (Fig. 1B) may reach 70 mm in length. The body surface is strongly wrinkled. The foot is linear. The head is rounded with a pair of conical, completely retractile, perfoliate rhinophores with approximaly 35 tightly packed lamellae. The oral tentacles are strongly developed and dorsolaterally grooved along a part of their length. There are five non-retractile tripinnate gills, with the three anteriormost being more highly developed. The gills form a semicircle surrounding the anal papilla. The genital pore opens on the right side, midway between the gills and rhinophores. The ground color is dark blue, almost black. A wide yellow submarginal band follows the inner notal edge. This band is interrupt- ed in some specimens. A second yellow band arises from the former, just in front of both rhinophores and surrounds the inner side of their sheaths, continuing to the rear to the base of the gills. These bands can bifurcate at their origin. In this case, the sheath of the rhinophores is sur- rounded by the shorter branch. In either situation, these bands surround the gill to join each other posteriorly. These last bands can be interrupted or continuous. The edge of foot is also bordered by a wide yellow band. On the sides of the body, just below the notal edge, there is a line of the same colour that bifurcates and surrounds the genital pore, continuing to the end of the posterior end of the foot. Both branches can be continuous or not. Moreover, several yellow lines, varying in num- ber and length, are arranged between the dorsal and the foot bands. The oral tentacles, the rhinophores and the posterior part of their sheath are also blue-black. The gills are blue-black, but the inner and outer sides of the rachis of each one have a yellow line between them.

INTERNAL MORPHOLOGY.— The general arrangement of the internal organs is shown in Figure 7. The anterior digestive tract begins with a long thick-walled muscular oral tube, that continues into the buccal mass. At their junction, a pair of elongate pouches open into the digestive system (Fig. 8). There is a pair of small, short and wide salivary glands on the buccal mass, flanking the esophagus. The radular formula of two specimens of 70 mm (in life) is 33 x 3-4.1.1.1.3-4 (Figs. 9A-C). The rachidian tooth (Fig. 9B) is broad, clearly curved at the base, having three well-differ- entiated cusps. The inner lateral tooth (Fig. 9C) is hooked with two well developed elongate cusps. The inner one is very long, having sharp and curved edges on the internal side and a prominent pro- jection (see the arrows Fig. 9A) on its outer edge. The outer lateral teeth (3 to 4) are smaller and quadrangular without prongs, and decreasing in size from the inner to the outer side of the radula. A labial cuticle is present, but lacks armature.

REPRODUCTIVE SYSTEM.— The reproductive system is shown in Figure 10. The hermaphro-

388 PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES Volume 54, No. 22

ve

hg+dg ____\

Figure 8. Roboastra caboverdensis sp. nov. Details of the oral tube and buccal mass, bb = buccal bulb, bg = buc- cal ganglion, oe = oesophagus, ot = oral tube.

FIGURE 7. Roboastra caboverdensis sp. noy. General arrangement of the internal organs. au = auricle, bb = buccal bulb, bgl = blood gland, ca = cephalic artery, cg = cerebral ditic duct has an “S” shaped ampulla that con- ganglion, fm = female gland, hg+dg = hermaphrodite tjnues into the spermoviduct. The vas deferens glad dieestive late, ua = intestine, oe = Cesophaeus of = is lone and coiled. with a unitGmneeidtimlene oral tube, pe = pericardium, rn = rhinophoral nerves, ve = = L ventricle: slightly narrower in the prostatic part. It ends in

a dilated penial section. The penis is armed with, at least, three different kind of spines arranged in helicoidal rows. Types of spines and their arrangement on the penis are shown in Figures 11A—D. The bursa copulatrix is rounded and the seminal receptacle elongate. The seminal receptacle joins with the vagina, near the bursa via a short duct. The vagina is short and straight, opening into the genital atrium, near the vestibular gland. This gland is very well developed, flattened, with muscular walls.

DISCUSSION

In 1985, Garcia-Gomez described the first species of the genus Roboastra in the Atlantic Ocean, from the Strait of Gibraltar. The original description of the external anatomy, radula and reproductive system of Roboastra europaea is in agreement with our specimens of this species; however, our specimens exhibit a different pattern of coloration than has been previously described for this species (Schick 1998; Megina 2000; Garcia~-Gémez 2002:224, phot. 447; Sanchez 2001). Moreover, it is confirmed that the spicules of the surface of the mantle mentioned in the original description do not exist (perhaps they were an artifact of preservation). A pair of small, short and wide salivary glands on the buccal mass flanking the esophagus are described for the first time. These salivary glands are present in the other two genera of the subfamily Nembrothinae,

? The colour pattern supplied by Garcfa~-Gémez (2002) is an adaptation from his original description (Garcia-Gémez, 1985), with additional and later information, although the specimens included in the “Material” section are the same in both references.

POLA ET AL.: NUDIBRANCH GENUS ROBOASTRA IN THE ATLANTIC OCEAN

FIGURE 9. Roboastra caboverdensis sp. nov. CASIZ 166052, scanning electron micrographs of radula. A. Half-row of radular teeth. B. Rachidian teeth. C. Inner lateral tooth.

Nembrotha and Tambja, but in these they are longer and more robust than in Roboastra. Garcia- G6émez (1985) did not describe the presence of a pair of elongate pouches that open into the diges- tive system at the junction of the oral tube and muscular pharynx. The function of these structures is still unknown; nevertheless, Burn (1967) described similar structures in Roboastra gracilis.

The external and internal features of Roboastra caboverdensis permit us to distinguish it from its congeneric Atlantic species. The arrangement of the yellow lines or bands in both species is dif- ferent and are more numerous and tightly packed in R. europaea. Moreover, R. europaea has two colour phases, light and dark (see Cervera et al. 1988 and Ocajia et al. 2000, for a colour picture of the light phase).

Regarding the internal anatomy of both species, the base of the rachidian radular tooth is more

390 PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES

curved in R. caboverdensis and the upper cusp of the inner lateral radular tooth is bifid in R. europaea while in R. caboverdensis it is simple. The reproductive system of R. caboverdensis is similar to that described for R. europaea except that the portion of the ejaculatory duct near the prostate is more highly convoluted in R. europaea. The penis in both cases 1s armed and the spines, of three different sizes and shapes, are implanted in heli- coidal rows. In both R. europaea and R. caboverd- ensis, the distal two-thirds of the penis has elon- gate, curved spines, and the basal spines are medi- um sized but straighter than the distal ones. Be- tween them, there are some rows of short, curved spines, a few with little spines just behind them. There is another dark blue/black with yellow bands or lines nembrothid in the Cape Verde Archi- pelago, Tambja simplex Ortea and Moro, 1998. However, the yellow pattern of this species has few lines with a different arrangement, and the internal anatomy (salivary glands, labial cuticle, radular

Volume 54, No. 22

pr

am

FIGURE 10. Roboastra caboverdensis sp. nov. Re- productive system, am = ampulla, be = bursa copulatrix, fgm = female gland mass, hd = hermaphrodite duct, p = penis, pr = prostate, rs = receptaculum seminis, v = vagina, vd = vas deferens, vg = vestibular gland.

teeth and reproductive system) are characteristic of Zambja (Ortea and Moro 1998; Cervera et al.

2000).

10um pall

C. Detail of middle spines. D. Detail of basal spines.

FiGURE 11. Roboastra caboverdensis sp. nov. MNCN 15.05/46614, A. Protruded penis. B. Detail of distal spines.

10um ==

POLA ET AL.: NUDIBRANCH GENUS ROBOASTRA IN THE ATLANTIC OCEAN 3)

ACKNOWLEDGMENTS

Our most sincere gratitude to Drs. Gongalo Calado, Peter Wirtz, Manuel A. Malaquias and Cristina Grande, for providing us the Cape Verde specimens and their photographs, to Dr. César Megina, Karl L. Schick and Antonio D. Abreu (MMP) for giving us kindly their unpublished data and photographs of Roboastra europaea and R. caboverdensis. To Dr. David Reid (NHM) and Antonio D. Abreu for sending the material from Madeira. We also express our gratitude to Mr. José Maria Geraldia and Mr. Juan Gonzalez (from the Electron Microscopy Service of the University of Cadiz) and Mr. Scott Serata (from the Electron Microscopy Laboratory of the California Academy of Sciences) for providing facilities to take Scanning Electron Microscope photographs. Marta Pola (M.P.) deeply thanks Yolanda Camacho-Garcia her assistance during the stay at the California Academy of Sciences.

Finally, this paper has been benefited by the following projects REN2001-1956-C17-02/GLO (Spanish Ministry of Science and Technology), REN2000-0890/GLO (Spanish Ministry of Science and Technology) and PEET Grant DEB-9978155 (National Science Foundation, USA). One of the authors (M.P.) has been benefited by a predoctoral fellowship and a grant for a short stay at the California Academy of Sciences, both funded by the Spanish Ministry of Education, Culture and Sports.

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SANCHEZ, A. 2001. (February 8) Roboastra europaea from Spain. [Message in] Sea Slug Forum. http://www.seaslugforum.net/find.cfm?id=3729

SANZHEZ-TOCINO, L., A. OCANA, AND F.J. GARCIA. 2000. Contribucion al conocimineto de los moluscos opis- tobranquios de la costa de Granada (sureste de la Peninsula Ibérica). Jberus 18(1):1-14.

ScuHIcK, K.L. 1998. Atlas submarino de la Costa del Sol. Marbella (Malaga, Spain), 71 pp.

_~

Copyright © 2003 by the California Academy of Sciences San Francisco, California, U.S.A.

PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES

Volume 54, No. 23, pp. 393-406, 12 figs. November 14, 2003

Redescription of Halgerda graphica Basedow and Hedley, 1905, with Observations on External Morphological Variation within Selected Species of Halgerda (Mollusca: Nudibranchia)

Shireen J. Fahey and Terrence M. Gosliner Department of Invertebrate Zoology and Geology California Academy of Sciences Golden Gate Park, San Francisco, California 94118, USA

Halgerda graphica Basedow and Hedley, 1905 is redescribed based on examination of two specimens; one collected in 1904 from Middle Harbour, Sydney, Australia, housed at the Australian Museum, Sydney, and another specimen collected in 1990, from Port Moorowie, near the type locality (Kangaroo Island, South Australia). The reproductive system is described and illustrated for the first time. This species has frequently been misidentified due to having similar external morphology to other Halgerda species. A comparison is made to those species. Halgerda graphica has a unique combination of external and internal characters that confirm it as a distinct Halgerda species. The external characters include a “hieroglyphic” pattern of yellow and black markings on the notum, small, similar-size dark spots on the ventral sur- face, a small, sparse, dark-colored gill and rhinophores with a white base, dark tip and a dark line on the posterior side. The external color variations of Halgerda dichromis Fahey and Gosliner, 1999, H. okinawa Carlson and Hoff, 2000 and H. wil- leyi Eliot, 1904 are also described, illustrated and compared to externally similar species. It is the unique combination of external morphological characters such as the color and pattern on the notum, the structure and color of the gills and rhinophores that help to distinguish each species, although examination of internal morphology can confirm the identification.

Basedow and Hedley (1905) described the nudibranch Halgerda graphica from two specimens dredged off Antechamber Bay, Kangaroo Island, South Australia. They had at the time examined a third specimen, which, although not included in the original description, they indicated that it belonged to their new species. The original description of the external and radular morphologies of the specimens were quite detailed, but the authors did not provide a description of the reproductive morphology. This species did not show up again until 1990. In the meantime, other authors (e.g., Coleman 1975, 2001; Kay 1979; Kay and Young 1969; Wells and Bryce 1993) have erroneously attributed the name Halgerda graphica to other species.

The present study describes two additional specimens of Halgerda graphica; the single spec- imen mentioned by Basedow and Hedley, collected in approximately 1904 at Middle Harbour, Sydney, and an additional specimen collected by N. Holmes in 1990 from Port Moorowie, Yorke Peninsula, South Australia.

The nudibranch genus Halgerda Bergh, 1880 has been studied extensively in recent years (Rudman 1978; Willan and Brodie 1989; Carlson and Hoff 1993, 2000; Gosliner and Fahey 1998;

! Contact author: sfahey @ calacademy.org

393

394 PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES Volume 54, No. 23

Fahey and Gosliner 1999a, 1999b, 2000, 2001a, 2001b). Since 1998, the number of described species increased from 14 to 35. Among Halgerda species are several that display external color variation in specimens from similar habitats and from varying geographic ranges. Four species, in particular, seem to be most commonly confused: Halgerda graphica, H. willeyi, H. okinawa Carlson and Hoff, 2000, and H. dichromis Fahey and Gosliner, 1999. The present study illustrates the color variations that can cause misidentification of these four species in the field and then makes comparisons with the externally most similar species. Field notes and photographic records of many observers, both amateur and professional, provide the basis of the discussion on external color variation presented in this paper.

DESCRIPTIONS OF TAXA

Labiostomata Valdés, 2002 Family Discodorididae Bergh, 1891

Genus Halgerda Basedow and Hedley, 1905 (Type species: Halgerda formosa Bergh, 1880, by monotypy)

Halgerda graphica Basedow and Hedley, 1905 (Figs 1-3)

TYPE MATERIAL.— The type material is probably lost; it is not at the Australian Museum. The type locality is Kangaroo Island, South Australia. The authors (Basedow and Hedley 1905) men- tion an additional specimen deposited at the Australian Museum, Sydney (C18168, Location #016276, collector not named) from Middle Harbour near Sydney, in September 1904. This spec- imen was examined and is both described below and hereby designated as the neotype.

OTHER MATERIAL EXAMINED.— South Australian Museum, TD16542, one specimen, dissect- ed, Port Moorowie, Yorke Peninsula, South Australia. 10 m deep, collected by Nigel Holmes, 15 December 1990.

EXTERNAL MORPHOLOGY.— Because there are no photographs or drawings available for spec- imen C18168 (1904), the following is a description of the specimen collected in 1990 by N. Holmes. This specimen is nearly identical to the drawing and description of Halgerda graphica provided by Basedow and Hedley in 1905 (Fig. 1A).

The preserved animal is 28 mm in length. The body profile is rounded, convex (Fig. 1B) and the dorsum has a low-ridged pattern. There are no small marginal tubercles. There is a low central ridge running the length of the dorsum that splits into several smaller ridges as it nears the gill pocket. The ridges have orange-yellow crests. The background color of the dorsum is gray-white. Between the ridges are black spots with some spots circled or semi-circled with the same yellow color as the ridges. The dark spots closest to the mantle edge are smaller than those on the dorsum. The mantle margin is translucent white when viewed dorsally, but when viewed ventrally, a yellow margin is apparent. On the underside of the mantle and along the side of the foot are dark spots of various sizes. The foot margin is yellow (Fig. 1C). The oral tentacles are long and tapered.

The long rhinophores have a bulging club that is tapered at the tips. The club is angled poste- riorly and there is dark brown to black coloration around the top half of the club up to the tip. The base is translucent white and there is a dark line on the posterior side of the rhinophores that extends from the base to the tip.

The bipinnate gill lies flat over the dorsum and is moderately pinnate. Each of the four main gill rachae has a brown stripe on the anterior sides. The anal papilla is long and is the same color as the body.

FAHEY AND GOSLINER: HALGERDA GRAPHICA 395

Vol XXDC Plate 10

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HALGERDA GRAPHICA, Basedow & Hedley.

FicurE 1. A. Halgerda graphica Basedow and Hedley, 1905, from the original color plate. B. Halgerda graphica South Australian Museum, (TD16542), photographed and collected by N. Holmes, 1990. Dorsal view. C. Ventral view.

BUCCAL ARMATURE.— The buccal mass has dark spots. The labial cuticle is smooth and devoid of any jaw rodlets. The radular sac is elongate and extends well behind the posterior end of the buccal mass. The radular formula of the specimen collected in 1990 is: 43x30.0.30 (TD16542) (Fig. 2A). The radu- lar formula of the specimen collected in 1904 could not be determined due to poor preser- vation and deterioration of the radula. The three outer teeth are much smaller than the inner and middle lateral teeth and the outer two teeth have tiny denticles (Fig. 2B). The 8 or so inner lateral teeth are smaller and have shorter hooks than the middle lateral teeth (Fig. 2C) and are arranged in a shallow V- shaped pattern in the center of the radula. The middle lateral teeth are hamate (Fig. 2D) with long, pointed hooks. They have a flat- tened flange, which overlaps the adjacent tooth.

REPRODUCTIVE SYSTEM.— The repro- ductive system is triaulic (Fig. 3). The long ampulla is tubular, curved into a complete loop and protrudes away from the bursa and prostate. The ampulla narrows into the post- ampullary duct, which bifurcates into the vas deferens and oviduct. The long oviduct enters the female gland mass. The female gland mass is about the same size as the bursa copulatrix. The long vas deferens sep- arates from the ampulla and widens into the glandular prostate. The prostate consists of two distinct glandular types and they are well differentiated as in most other members of Halgerda. The muscular portion of the defer- ent duct leaves the distal prostate in a long duct that curves into one loop and multiple half-loops, then enters the wide penial bulb. The long uterine duct emerges from the female gland mass and joins the ovoid recep- taculum seminis near its base. The duct con-

396 PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES Volume 54, No. 23

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FIGURE 2. Radular morphology of Halgerda graphica (TD16542). A. Entire radula. Scale = 2 um. B. Outer lateral teeth. Scale = 50 um. C. Inner lateral teeth. Scale = 100 um. D. Middle lateral teeth. Scale = 20 um.

necting the receptaculum and the bursa is long and coiled. The receptaculum seminis is much smaller than the thin-walled spherical bursa copulatrix. It lies under the bursa, but is not embedded in the prostate. The prostate does not completely cover the bursa copulatrix as is common in other, more highly derived species of Halgerda, but lies in a thin layer over two-thirds of the bursa. The vaginal duct that emerges from the base of the bursa copulatrix is long and thin. Near its exit into the bulbous vagina that is adjacent to the base of the penial sheath, is a muscular sphincter. The vagina has long folds in the walls and tubercular glands on the exterior. The common genital aper- ture is wide, large and has long fleshy folds that extend through the body wall. The opening of the female gland mass is adjacent to the genital aperture.

FAHEY AND GOSLINER: HALGERDA GRAPHICA 397

DISCUSSION

Although Basedow and Hedley (1905) described the external and radular morphology of Halgerda graphica, these authors did not illustrate or describe the reproductive morphol- ogy. Despite this, based on the unique color pat- tern of this species, there is little doubt that the specimens examined for this study are Halgerda graphica. Other authors (Coleman 1975, 2001; Kay 1979; Kay and Young 1969; Wells and Bryce 1993) have erroneously attrib- uted the name Halgerda graphica to other species. Wells and Bryce, mislabeled a speci- men of Halgerda gunnessi as H. graphica Basedow and Hedley, 1905; Kay misidentified a specimen of H. terramtuentis as H. graphica; __ Ficure 3. Reproductive morphology of Halgerda graph- and Coleman (1975, 2001) misidentified a See ee eee serena & specimen of H. willy as H. graphic um, p = penis, rs = receptaculum seminis, v = vagina. Scale Examination of the reproductive morphol- = 0.25 mm. ogy reveals similar characters to other

Halgerda such as a two-part prostate, a long, convoluted deferent duct, a bulbous penial sheath and a wide, muscular vagina. Radular characters also have similarities to other Halgerda species. Those characters are hooked mid-lateral teeth, finely denticulate outer teeth that are much smaller than the remaining teeth, and small inner later- al teeth.

Because of the similarity in external coloration of Halgerda graphica to H. gunnessi Fahey and Gosliner, 2001, H. johnsonorum Carlson and Hoff, 2000 and H. willeyi Eliot, 1904, these three are herein compared and contrasted to H. graphica. However, because Carlson and Hoff (2000) have already compared H. graphica to H. okinawa, we will not repeat what they have already done. Neither will we repeat what Fahey and Gosliner said when they compared H. gunnessi to H. john- sonorum and to H. formosa Bergh, 1880, nor what Carlson and Hoff (2000) had to say when they compared H. johnsonorum to H. willeyi. Rather, we encourage reference to their respective papers. Here we concentrate on comparing the external morphology of Halgerda graphica to its most sim- ilar species.

All four species of greatest concern to us, Halgerda graphica, H. gunnessi, H. johnsonorum and H. willeyi, have a white or gray-white ground color with yellow to yellow-orange ridge crests. Halgerda graphica has low ridges without tubercles as do H. gunnessi and H. johnsonorum. Only H. willeyi has prominent tubercles. Although both H. graphica and H. johnsonorum have dark spots or markings in the ridge concavities, only H. graphica has the “hieroglyphic markings” described by Basedow and Hedley. These markings consist of a dark spot at the center of the con- cavity surrounded by dark circles and lines (Fig. 1). The other two species, H. gunnessi and H. wil- leyi may also have dark lines or markings, but both lack the associated spots.

The coloration of the mantle edge also distinguishes these four species. Halgerda graphica does not have perpendicular dark markings along the mantle edge, but the edge markings of H. johnsonorum appear as continuous lines, which extend upward and into the ridge concavities on the dorsum. The dark perpendicular lines on the mantle margin of H. willeyi also extend up into the

398 PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES Volume 54, No. 23

ridge cavities, but they are more numerous when compared to H. graphica. Halgerda gunnessi does not have marginal lines (see Fahey and Gosliner 2001).

The ventral surfaces of the four species are not similar in that there are irregularly scattered dark spots without lines only on Halgerda graphica. Halgerda johnsonorum and Halgerda willeyi have black lines; H. gunnessi has no markings on its ventrum.

The coloration on the rhinophores and gills differs among the species. Halgerda graphica has dark coloration on the tips of the rhinophores and a dark line on the posterior side. This is similar to H. gunnessi. The other species have either dark spots (H. johnsonorum, H. willeyi) or dark spots plus a dark stripe on the rhinophores (H. johnsonorum) and large gills. The gill of H. graphica is small and darkly colored. The gill of H. willeyi is sparsely pinnate with dark speckles. The gill of H. johnsonorum is large and has dark spots, and the gill of H. gunnessi is large, feathery and has dark lined branches and a dark tip.

With regard to the internal morphology, Halgerda graphica has radular characters similar to those of H. gunnessi and H. willeyi. All three also have three small outer teeth. H. johnsonorum is distinct, having six outer teeth, with the penultimate being bifid. Halgerda graphica has two fine- ly denticulate outer lateral teeth; the outer three of H. willeyi and H. gunnessi are not denticulate.

The reproductive morphology of Halgerda graphica is most similar to H. willeyi. The obvious differences between the two are that the deferent duct of H. graphica is much longer and more con- voluted than in H. willeyi and the vaginal duct of H. graphica is much wider with the vagina, being much larger with tubercular glands on the exterior. A glandular vagina is not found in any of the other three species. Both Halgerda graphica and H. gunnessi have a vaginal sphincter.

The present study confirms the combination of external and internal morphological characters that identify Halgerda graphica and distinguish it from the four externally most similar species. The external characters that distinguish this species in the field are: the “hieroglyphic” yellow and black markings on the dorsum, no dark lines on the mantle edge, dark-tipped rhinophores with a posterior medial line, a small, dark gill and small, dark spots on the ventral surface.

Halgerda dichromis Fahey and Gosliner, 1999 (Figs. 4-5)

MATERIAL EXAMINED.— V8234, one specimen, dissected, 42 mm, Scottburgh, Kwazulu, Natal, South Africa, 25 m deep, collected by V. Fraser, 15 January 2000; V8233, one specimen, dis- sected, 20 mm, Park Rynie, KwaZulu, Natal, South Africa, 25 m deep, collected by V. Fraser, 28 December 1999; V8232, one specimen, dissected, 16 mm, Park Rynie, KwaZulu, Natal, South Africa, 25 m deep, collected by V. Fraser, 21 January 2000.

EXTERNAL MORPHOLOGY.— The external morphology of the specimens examined for this study are as described by Fahey and Gosliner with some color variation. The variation includes the presence of dark half-lines or spots on the dorsum of some specimens, in place of a heavy, dark line. The more juvenile specimens may not have any dark markings at all. Variations in the exter- nal color within this species are shown in Figures 4A-C.

RADULAR MORPHOLOGY.— There were no differences noted in the radular morphology between the recent specimens examined (Figs SA—D) and Fahey and Gosliner’s (1999) original description and line drawings. Figure 5A—D are the first SEMs of the radula of this species.

REPRODUCTIVE SYSTEM.— There were no differences in the sexually mature specimens exam- ined for this study (Fig. 6) and Fahey and Gosliner’s (1999) original description of Halgerda dichromis.

REMARKS.— Halgerda dichromis was described from a single specimen collected in 1980

FAHEY AND GOSLINER: HALGERDA GRAPHICA 399

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FiGure 4. Color variation of Halgerda dichromis. A-C, Photographed and collected by V. Fraser, 2000.

from Durban Harbor, South Africa. Since the original description, additional specimens have been collected and/or photographed from the same locality (present study) and, thus, allow a further examination of the species.

Halgerda dichromis has a