THE VELIGER TheVeliger49(3):105-119 (October 1, 2007) C' CMS, Inc., 2006 The Genus Paradoris Bergh, 1884 (Nudibranchia: Discodorididae) in the Tropical Americas, and South Africa with the Description ofa New Species YOLANDA CAMACHO-GARCIA' and TERRENCE M. GOSLINER- ' Museo de Zoologia, Escuela de Biologia, Universidad de Costa Rica, San Pedro de Monies de Oca, San Jose, Costa Rica (e-mail: [email protected]) -Department of Invertebrate Zoology and Geology, California Academy of Sciences, 875 Howard Street, San Francisco, California 94103, USA (e-mail; [email protected]) Abstract. A newspecies of^ParadorisBergh, 1884, P. caeruleussp. nov. is described based on specimenscollected from South Africa. The coloration, radular morphology, and details ofthe reproductive system ofthis species differ significantly from other previously described Paradoris species by having a blue body with gray-blue spots and a few black spots on the dorsum, as well as an accessory gland with two stylets in each sac. A redescription ofP. nmlciher and P. lopezi is based on newly collected material ofthese species from the Caribbean coast ofCosta Rica and the Galapagos Islands. The range ofP. lopezi is extended, from Mexico to the Galapagos Islands. INTRODUCTION synonymized most recently with Paradoris dubia A taxonomic revision of Paradoris Bergh, 1884, (Bergh, 1904) by Dayrat (2006) based on similarities recently published by Dayrat (2006) recognizes eight nofewthesrpeepcireosducftriovme sdyesteepm.wVaatledresso(f200N1e)wdesCcarliebdeodntiwao: species from the Pacific, Atlantic, and Indo-Pacific Paradoris araneosa and Paradoris imperfecta; the latter oceans: P. indecora (Bergh, 1881); P. dubia (Bergh, was synonymized with the former by Dayrat (2006). 1904); P. liturata, (Bergh, 1905); P. erythraeensis & Finally, Hermosillo Valdes (2004) described Para- (Vayssiere, 1912); P. mulciber (Marcus, 1970); P. doris lopezi, a new species from Mexico. Pt.surluogpeenzsiisHeBramboas,il1l9o86;&P.Vaalrdaense,os2a00V4a.ldeAsc,co2r0d0i1;ngantdo frPoamratdhoeristypmeulcmiabteerri(alMardceussc,rib1e9d70)friosmknBroawzinl oannldy Dayrat (2006), Paradoris is characterized by the redescribed by Dayrat (2006). This species and Para- following combination of characters: labial armature doris lopeziHermosillo &Valdes, 2004 are the only two with three jaw plates, radula elongated and narrow, members of the genus Paradoris reported from the grooved outeredge ofthe hook ofthe lateral teeth, and Americas. The present paper redescribes these species grooved oral tentacles. on the basis of several new specimens collected from The first reference to Paradoris in the Western the Caribbean coast ofCosta Rica and the Galapagos Atlantic Ocean was the description of Paradoris Islands, Ecuador, respectively. We also describe one mulciber from Brazil (Marcus, 1970), originally de- new species from South Africa. scribed as the type species of the new genus Percunas Marcus, 1970. Later, Marcus (1976) synonymized MATERIALS AND METHODS Percunas with Paradoris. Ortea (1995) revised the species of the genus from the Canary Islands. Accord- The material studied is deposited at the Zoology ing to this author, there were four species in this area, Museum of the University of Costa Rica, the De- however Dayrat (2006) synonymized three of these partment of Invertebrate Zoology and Geology of the species with P. indecora, based on individual variation. California Academy of Sciences, San Francisco, USA This author, as well as Ortea (1995), also concluded (CASIZ), and the Natural History Museum of Los that Paradoris granulata Bergh, 1884, the type species Angeles County (LACM). ofthe genus, is ajuniorsynonym ofDi.scodoris indecora Specimenswerepreservedin 70% ethanol. They were Bergh, 1881. dissected by dorsal incision, and their reproductive The first reference ofthis genus in the Pacific Ocean systems were examined and drawn under a dissecting wasthe description ofParadoris tsurugensisfromJapan microscope with camera lucida. At least two specimens by Baba (1986, 1989). Later, Miller (1995) described of each species were examined anatomically and Paradoris leuca from New Zealand, which was dissected for this study. The buccal masses were Page 106 The Veliger, Vol. 49, No. 3 dissected and immersed in sodium hydroxide, rinsed, and branchial leaves. The oral tentacles are fmger-like and then mounted on stubs for SEM examination. and have a longitudinal groove on their external side. The accessory gland from the reproductive system The anteriorborder ofthe foot is grooved and notched was dissected and placed in different concentrations of (Figure 2B). The foot is completely covered by the alcohol for at least 20 min and then transferred to notum when the animal is in motion. a solution ofxylol for 20 min. After the tissue became The background color of the dorsum in hving translucent, the gland was mounted on a cover slide. animals is light brown to pale cream, with numerous The styletsweredrawn usinga microscopewith camera small dark brown spots (Figure lA) very densely lucida. arranged on the entire dorsum and at the base of the tubercles. Each spot itself is composed of an aggrega- SPECIES DESCRIPTIONS tion of minute brown specks. The apices of large tubercles are yellowish. The rhinophores and branchial Genus Parudoris Bergh, 1884 leaves are pale brown with small, dark brown spots Paradoris nmlcibev (Marcus, 1970) arranged irregularly. The tips of the branchial leaves are yellowish, and the branchial sheath is undulate. The (Figures IA, 2, 3, 4) ventral side ofthe animal is cream colored. The sole of the foot has more dark spots than the hyponotum, but Type material examined: Holotype: Juriac;u, Maranhao they are smaller (Figure 2B). The same spotting occurs Province, Brazil 00 04'S, 44 33'W, 6 September 1967, 1 on the ventral surface, foot, and mantle. The tentacles specimen (previously dissected), 21 mm preserved are covered with brown speckles. length, leg. Almirante Saldanha R/V (MZSP 41291). Anatomy: The jaw has three distinct pieces with Other material examined: Ponta de Pedra, Pernanbuco a number ofsimple, regularly arranged elements about vPiroouvsilnyced,issBercatzeild,),3305 Amumgusprtes1e9r7v0e,d l1ensgpthe,cilmeeg.nM(oprne-- 818\\mxx\minplreensgetrhv(eFdigluernegt3hA)s.pTechiemeranduilsar55forXmu(l1a8.o0f.1a8n) mm tonchet (MZSP 41292, # 1045 Marcus Coll.); Manza- (INB001501499) and a 40 preserved length spec- nillo. Area de Conservacion Amistad Caribe, Sixaola, imen is 47 X (16.0.16) (LACM ACC 4308). In general, Limon, Costa Rica (9 38'42"N, 82°39'29"W), 20 the teeth are broad and hook-shaped. All the lateral October 1998, 4 specimens (3 dissected), 27-56 mm teeth, including the outermost, are smooth. They preserved length, collected under rocks by SCUBA, become gradually larger from the innermost to the 9 m depth, leg. S. Avila (INBOOl501499); Silal de mid-laterals, then become smaller and less angular Cahuita, Parque Nacional Cahuita, Limon, Costa Rica from the mid-laterals to the outermost. The innermost (9=44'35"N, 82 48'21"W), 21 September 1999, 2 speci- teeth are thin, pointed, and angular (Figure 3B). The mm mens (one dissected) 15-29 preserved length, mid-lateral teeth have a groove on the lower side ofthe collected under rocks by SCUBA diving, 12.5 m depth, cusp (Figure 3C). The outeiTnost have a prolongation leg M. Calderon (INBOO1496697). on the upper side ofthe teeth (Figure 3D). There is no sharp distinction between the base and the cusp in the Geographic range: This species was previously known outennost tooth. (fErsopminoBrsaazi&l O(rMtaerac,us2,001)19.70S,om1e97a6d)diatinodnalCosspteaciRmiecnsa leftThoen atmoppulalnad,awnhteircihoristolotnhge faenmdalteubgullaanrd,sisanldocnaetxedt have been collected from the Caribbean (Vinicius to the bursa copulatrix. The deferent duct is large and Padula, personal communication). thin throughout its length (Figure 4A) and leads to External morphology: Living animals range from 20- a granular and convoluted prostate that is folded upon 60 mm long. The body is oval and elevated, widest in itself. At the distal end, there is an unarmed penis that the middle region (Figures A, 2A). Themantlemargin is wider than the rest of the duct. The long vagina 1 is wide, undulating, and spiculose. The dorsum is connects to two accessory glands and three muscular covered with rounded, widely spaced tubercles of sacs containing one stylet each (Figure 4B). Two ofthe various sizes. The largest ones are generally situated sacs are located on the dorsal side and one onmthme in the middle region of the notum (Figure 2A), and ventral side ofthe vagina. Each stylet is about 0.6 mostofthem areelevated. Some specimens haveoneor in length. Thewhitish bursacopulatrix issemi-spherical two tubercles located anteriorly and posteriorly on the and thin-walled. From the bursa copulatrix leads rhinophoral sheath. The rhinophores have 19-21 very another thin duct that connects to the oval seminal thin lamellae. The rhinophoral and branchial sheaths receptacle and the uterine duct. are undulate. The gill consists of six tripinnate branchial leaves. Other specimens examined have Remarks: Paniduyisnnilciher(Marcus, 1970) is the only around the same number oflamellaein the rhinophores species of the genus Paradoris reported from the Y. Camacho-Garcia & T. M. Gosliner, 2006 Page 107 Figure 1. Living animals of Panidoris. A. Panidoris niulciher. Costa Rica (INB001501499) photo by Y. Camacho-Garcia. B. Purculoris ccwndeiis sp. nov.. South Africa (CASIZ 073954) photo by T.M. Gosliner. C. Living animal of Paradoris lopezi. Galapagos Islands(LACM 71-45) photograph by D.K. MuUiner. D. Dorsal viewofapreservedanimaloiParadorislopezi(CASIZ 105978) photograph by M. Zuiiiga. E. Ventral view ofa preserved animal ofParadoris lopezi(CASIZ 105978) photograph by M. Ziifiiga. Note: In fig. ID, E, the blue color on the pictures is due to an accidental stain ofthe specimen with methylene blue. Page 108 The Veliger, Vol. 49, No. 3 Figure2A. Dorsalviewofapreservedanimal ofPciradorismukiberfrom Limon,Caribbeancoast ofCosta Rica(INBOOl501499). B. Ventral view; scale bar = 5 mm. Atlanticcoast ofthe Americas. Theoriginal description A drawing ofthe reproductive system ofa specimen of this species (in the genus Perciinas) was a brief from the Caribbean made by Vinicius Padula (un- description, later expanded by Marcus (1976). The published data) consistently shows the presence oftwo specimens exaiiiined here are identical to those de- accessory glands and three stylets. Also, the ampulla scribed by Marcus (1970, 1976), and there is no has a U-shaped form and a long and convoluted detectable variation among the specimens. The only prostate folded upon itself that is also present in the differences between Marcus's descriptions and ours three specimens we dissected from Costa Rica. The (also pointed out by Dayrat, 2006) are that the prostate only difference found in the reproductive system ofthe is larger in the original description than that found in specimen from the Caribbean that differs from ours the present material, the branchial sheath of our and that of Marcus (1976) is that the duct that leads specimens has several undulations rather than being from the seminal receptacle joins the duct from the smoothasin Marcus'sdescription, and the rhinophoral vagina before it enters into the bursa copulatrix. sheaths in some specimens examined here have one or Ortea (1995) stated that P. indecora is possibly an two tubercles on each side. amphiatlantic species and that P. mulciber is a junior Y. Camacho-Garcia & T. M. Gosliner, 2006 Page 109 Figure3. ScanningelectronmicrographsofFaradorisinulciher{IN'B00150\499).A.Jawelements,scalebar = 25 i^m.B.Innermost radularteeth, scale bar = 75 |am; C. Mid-lateral radular teeth; scale bar = 75 |,tm. D. Outermost radular teeth scale bar = 75 |j.m. synonym ofP. indecora. Dayrat (2006) concluded that differences, and considering the geographical range of "the differences between nndciber and indecora are the species, Dayrat agreed to keep these species as two shght" and that mulciber and indecora cannot be valid species. Based on the new specimens we examined distinguished from each other. Despite these shght from Costa Rica, we conclude that these two species Page 110 The Veliger, Vol. 49, No. 3 Figure4A. Reproductive system o'i Paniduviaiiiiilcibcr (1NB00I501499), scale bar = 18 mm. B. Detail ofthe reproductive system (INB001501499), scale bar = 23 mm; Abbreviations: ag = accessory gland, am = ampulla, be = bursa copulatrix. dd = deferent duct, fg = female gland, pr = prostate, s = stylet, sr = seminal receptacle, st = stylet sac. v = vagina. are distinct (Table 1) based on several anatomical Fernandina, Galapagos Islands, Ecuador, 16 Septem- differences. For example, in these specimens, and that ber 1974, 3 specimens (dissected for this study) 26- mm which V. Padula examined from the Caribbean, there 61 preserved length, collected in the intertidal are consistently two accessory glands with three stylets. rocky shoreunder rocks, leg. G. H. Wellington (CASIZ Panuloris indecora has only one accessory gland and 105978); Darwin Research Station, Academy Bay, a maximuiTi of three stylets (Dayrat, 2006). Also, P. Santa Cruz Island, Galapagos Islands, Ecuador indecorct has fewer, smaller tubercles arranged in two (0"45'06"S, 90 15'38"W), March 1971, 1 specimen, mm m mid-dorsal lines (see description by Valdes, 2002, and 25 preserved length, collected between 1-3.3 Ortea, 1995:fig. 2) while those ofP. nni/ciher are larger, depth, leg. Ameripagos Expedition (LACM 71-45). more numerous, and more evenly distributed over the entire dorsum (Figure 2). Geographicrange: This speciesisknown only from Baja California Sur and Bahia Banderas, Mexico, and the Paradoris lopezi Hermosillo & Valdes, 2004 Galapagos Islands (present study). (Figures IC-E, 5A, B, 6A-D, 7A, B) External morphology: The dorsum is covered with numerous, seinispherical tubercles of different sizes Type material examined: Holotype: Punta de Pichilin- arranged regularly (Figures IC, 5A). Generally, the gue, Baja California Sur, La Paz, Mexico. (24 2r25"N, largest tubercles are located near the center. There are 105''33'88"W), 31 October 2004, 1 specimen (previously no tubercles located on the rhinophoral or branchial dissected), 32 mm preserved length, collected under sheaths in any ofthespecimens. Thegill iscomposedof coral rubble at 1 m depth, leg. A. Hermosillo (CASIZ six tripinnate branchial leaves,mamnd the rhinophores 171661). have 18-20 lamellae in a 36 preserved length specimen (CASIZ 105978). An SEM of the notum Other material examined: Punta Espinosa, Isla Fernan- (not included here)clearlyshowsthepresericeofmantle dina, Galapagos Islands, Ecuador, 16 September 1974, holes. Themargin ofthemantleiswideandundulating. mm 1 specimen, 71 preserved length, collected in the The anterior border ofthe foot is grooved and notched intertidal rocky shore under rocks, leg. G. H. (Figure 5B). Theoral tentaclesareconical andgrooved. Wellington (CASIZ 117625); Punta Espinosa, Isla The background color of the living animals is gray Y. Camacho-Garcia & T. M. Gosliner, 2006 Page 111 Figure 5A. Dorsal view of a preserved animal of Paradoris lopezi (CASIZ 117625) from Punta Espinosa, Galapagos Islands, Ecuador. B. Ventral view, scale bar = 5 mm. with numerous small brownish orange spots arranged foot and are arranged irregularly (Figures IE, 5B). very densely on the entire dorsum (Figure IC). The The rhinophores are light brown with small darker gray color is darker towards the middle of the brown spots. dorsum. The tubercles have a pale gray base and an osrpaencgiemetnip.haTshereieghatr)e sceovmerpaolseladrgeofblaanckapgagtrcehgeaste(onoef Aan3a5tommmy:prTehseervreaddulleanrgtfhosrpmeucliameins a4n2dX55(X22.(02.62.20).26i)n small black specks. There are simple black and brown in a 61 mm preserved length specimen. The radula is spots near the margin of the mantle as well. Opaque very elongated and the labial cuticle has three pieces. white spots are also present all over the dorsum. The Jaw elements are arranged regularly (Figure 6A) rachises of the branchial leaves are dark gray with (CASIZ 105978). The innermost teeth are larger, more small brown spots, the tips being yellowish. The foot angular, and more pointed than the rest (Figure 6B). is pale gray spotted with brown. The color of the The midlateral teeth are hook-shaped and pointed ventral side ofthe mantle is pale gray with some dark (Figure 6C). Generally, the teeth have a prolongation brown spots. These spots are larger than those on the on the upper side that is strongest in the outer teeth. Page 112 The Veliger, Vol. 49, No. 3 Figure 6. Scanningelectronmicrographs oiParadorislopczi(CASIZ 117625). A. Jaw elements, scale bar = 25 \xm. B. Innermost radularteeth, scalebar = 75 |am; C. Mid-lateral radularteeth. scale bar = 75 p.m. D. Outermost radularteeth, scale bar = 75 )im. There is not a sharp distinction between the base and its bifurcation into the oviduct and deferent duct. There the cusp in the outermost teeth (Figure 6D). is a large and convoluted prostate (Figure 7A). The The ampulla is long, wider in the middle, and folded deferent duct gradually narrows before ending in upon itself. It has a long duct located distally. prior to a short, unarmed penial section. The vagina is long Y. Camacho-Garcia & T. M. Gosliner, 2006 Page 113 B Figure 7A. Reproductive system ofFaracloris lopezi (CASIZ 117625), scale bar = 18 mm. B. Detail ofthe reproductive system (CASIZ 117625), scale bar = 23 mm. Abbreviations: ag = accessory glands, am = ampulla, be = bursa copulatrix, dd = deferent duct, fg = female gland, pr = prostate, s = stylets, sr = seminal receptacle, st = stylet sac, v = vagina. and connects with two accessory glands and three three specimens from Isla Fernandina, Galapagos. The muscular sacs, each containing a single stylet about specimendesignatedastheholotypehashighertubercles mm 0.9 in length. The glands and the sacs are both (about 1.3 mm), and smaller and lighter spots on the located on the dorsal side (Figure 7B). The bursa hyponotum and notum. On the other hand, the speci- copulatrix is pale cream, semispherical, and twice the mens from Isla Fernandina have lower tubercles and size of the seminal receptacle. There is a convoluted bigger and darker spots on the hyponotum and notum. duct that leads from the bursa copulatrix to the oval ThereareseveralmorphologicaldifferencesbetweenP. seminal receptacle and to the uterine duct. lopeziand P. mukiber. In P. lopezi, there are long black patches clearly visible all over the dorsum, and single Remarks: Dayrat (2006) found some differences in the blackandbrown-orangespotsclosetothemarginofthe original description of the species when reexamining mantle (Figure IC), whereas no dark pigmentation is the type material. For example, the oral tentacles were present on the dorsum or mantle in P. mulciber (Figure grooved (Dayrat, 2006) instead of not grooved 1A). Also, whilethefoot ofParadorismulciberhasmore (Hermosillo & Valdes, 2004), and there were two butsmallerdarkspotsthanthehyponotum(Figure2B), accessory glands and three stylet sacs (Dayrat, 2006) P. lopezi has fewer but larger dark spots on both the instead ofjust one stylet sac and two accessory glands footand hyponotum (Figure IE). Thetubercles present (Hermosillo & Valdes, 2004). The three specimens we on each side of the rhinophoral sheaths in P. nnilciber examined from the Galapagos Islands are in complete are not present in any of the specimens examined of agreement with the description provided by Dayrat P. lopezi. Paradoris indecora (Bergh, 1881) from the (2006). However, wealso observed somemorphological Mediterranean differs from P. lopezi by the external differences between the holotype from Mexico and the coloration and the mid-dorsal position ofthe tubercles. Page 114 The Veliger, Vol. 49, No. 3 Paradoris diibia, described by Bergh (1904), is also spots present around the margins of the notum. easily distinguished from P. lopeziby the white color of Around the larger and smaller tubercles, there is an the body with dark brown spots, the translucent color aggregation ofminute white spots that are also present of the foot, the smooth dorsum, and the lack of along the mantle margins. The branchial leaves and the accessory glands and stylets. Paradoris tswugensis base of the rhinophores are brownish black in color, (Baba, 1986. 1989) from Japan differs sHghtly from while the tips ofthe rhinophores are white. P. lopezi in external morphology and coloration (see The ventral side of preserved specimens is cream. Hermosillo & Valdes, 2004); for example, P. lopezi has The foot has several brown spots along the external more stylet sacs (Table 1) but fewer teeth ([42 X margin that are also present on the hyponotum. [22.0.22]) than P. tsurugensis (90 X [20-25.0.20-25]) in However, there are no spots present on the sole of specimens ofcomparable size. the foot. The oral tentacles are lightly speckled with We agree with Dayrat (2006) that the presence of brown. dark red tubercles on the dorsal notum is probably mm a good character to distinguish P. lopezi from the rest Anatomy: The radular formula of a 25 long aorfantehoesa,spePc.ielsitiiorfata,thaendgePn.useryPtahrraadeoenrsiiss,. such as P. aspe2c3immenm ilson5g0 sXpeci(m21e.n0.2i1s) 38(SAXM (2A13.60.02119)) (CaAn-d SIZ073954). The jaw elements are arranged regularly Paradoris caeru/eiis, new species in three discrete pieces (Figure 8A). The teeth are strong, smooth, and slender. The innermost teeth are (Figures IB, 8, 9) less angular and pointed than in the other species (Figure 8B). The midlateral teeth are hook-shaped and Type material: Holotype: Phillips Reef, Algoa Bay, pointed (Figure 8C). The outermost teeth do not have Indian Ocean coast. Cape Province, South Africa, the prolongation on the upper side or cusp sometimes Febmrumary 1984, 1 specimen (dissected for this study) present in other species of Paradoris (Figure 8D). 25 preserved length, collected at 10-15 meters The ampulla is short, tubular, and convoluted in the depth by SCUBA diving, leg. WR. Liltved (SAM middle section, and itbranches into a short oviduct and A36019); Paratype: Phillips Reef, Algoa Bay, Indian the prostate. The oviduct enters the female gland mass Ocean coast. Cape Province, South Africa, May 18, distally. The thick and convoluted deferent duct leads mm 1984, 1 specimen (dissected for this study) 24 to a short and granular prostate (Figure 9B). The preserved length, leg. WR. Liltved (CASIZ 073954), deferent duct opens into a common atrium with the with two microslides. vagina. The penis is unarmed. There is a pair ofhighly ramified accessory glands and two muscular sacs Geographic range: This species is known only from containing two stylets each. The glands and the sacs South Africa (present study). are located on the dorsal side (Figure 9C). Each stylet mm External morphology: The body is oval and elongated, ias albaorguet 0a.n2d ovailn lbeunrgstah.cTohpuelasthroirxt.vaFgrionamcotnhneecbtusrstao higher in the middle portion. The dorsum is covered copulatrix leads another short duct that connects to the with numerous low tubercles of various sizes closely seminal receptacle and the short uterine duct. The arranged and densely distributed. Wider tubercles are surrounded by smaller ones. There are no larger bursa copulatrix is about five times larger than the seminal receptacle. tubercles located on the rhinophoral sheaths as in P. mulciber. There are numerous large holes covering the Etymology: From the Latin "caeruleus'' in reference to surface of the notum. The gill is composed of seven the blue color ofthe species. tripinnate branchial leaves, and the rhinophores have mm 10 lamellae in a 24 preserved length specimen Remarks: Dayrat (2006) described specimens from (SAM A360I9). The number oflamellae and branchial the Cape Province of South Africa that he attributed leaves in the other specimen available are not provided to Paradoris erythraeensis (Vayssiere, 1912). These since these structures were retracted in their sheaths. animals differ from the holotype of P. erythraeensis Themantleiswide and undulating. The anterior border in several important aspects of their anatomy. The of the foot is grooved and notched (Figure 9A). The holotype of P. erythraeensis has a series of conical oral tentacles are finger-like in shape and grooved. The tubercles on the back. Gohar & Abu-Ela (1959) also foot is completely covered by the notum when the noted these tubercles in another specimen they animal is in motion. examined from the Red Sea. They also described the The background color ofliving animals is a uniform color ofthe living animal as "light gray with scattered gray blue with two black spots (Figure IB) located roundish or irregularly shaped blackish brown patches. almost halfway between the rhinophores and the It is finely tuberculated, large tubercles occurringin the branchial leaves; however, there are also some small centre of the black patches and surrounded by more