PROCEEDINGS OFTHE CALIFORNIAACADEMYOFSCIENCES Volume 54, No. 4, pp. 65–79, 7 figs. March 14, 2003 Caryophyllidia-bearing Dorid Nudibranchs (Mollusca, Nudibranchia, Doridacea) from Costa Rica Yolanda E. Camacho-García1,2and Ángel Valdés3 1Department of Invertebrate Zoology and Geology, California Academy of Sciences, Golden Gate Park, San Francisco, California 9118, USA; 2Instituto Nacional de Biodiversidad (INBio), Sub-Programa de Malacología, Santo Domingo de Heredia, Costa Rica; 3Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, California 9007, USA The tropical eastern Pacific dorid nudibranch Taringa aivica Ev. Marcus and Er. Marcus, 1967 is redescribed based on the examination of specimens collected from the Pacific coast of Costa Rica. The differences between Taringa aivica timia Ev. Marcus and Er. Marcus, 1967 and Taringa aivica aivicaEv. Marcus and Er. Marcus, 1967 are not consistent and do not justify the existence of two subspecies of Taringa aivica. Examination of the type material of Peltodoris nayaritaOrtea and Llera 1981, anothereastern Pacific species, confirmed that it is a synonym of Peltodoris greeleyi MacFarland, 1909, originally described from Brazil. The study of Discodoris aurila Marcus, 1976 from Panama and Costa Rica, shows that this species is characterized by the absence of jaw elements, the presence of hamate and smooth radularlateral teeth, and the innermost teeth hamate, elongated, and lacking denticles. Peltodoris greeleyi and Discodoris aurila are transferred to the genus Diaulula based on the presence of caryophyllidia, low rhinophoral and branchial sheaths, a flattened prostate divided into two portions, penis and vagina unarmed, hamate radularteeth and smooth labial cuticle. The geographic range of Diaulula greeleyiis extended to Punta Uvita, Costa Rica and the geographic range of Diaulula aurilais extended from Mexico to Panama. RESUMEN La especie de dórido nudibranquio del Pacífico Este tropical Taringa aivica Ev. Marcus y Er. Marcus, 1967 es redescrita en base al estudio de especímenes recolec- tados en la costa Pacífica de Costa Rica. Las diferencias entre Taringa aivica timia Ev. Marcus y Er. Marcus, 1967 y Taringa aivica aivicaEv. Marcus y Er. Marcus, 1967 no son consistentes y no justifican la existencia de dos subespecies diferentes de Taringa aivica. El estudio del material tipo de Peltodoris nayaritaOrtea y Llera, 1981, otra especie del Pacífico Este, ha confirmado que ésta es un sinónimo de Peltodoris greeleyi MacFarland, 1909, que fue originalmente descrita de Brasil. El estudio de Discodoris aurilaMarcus, 1976 de Panamá y Costa Rica, muestra que esta especie se caracterizada por la ausencia de uncinos, y la presencia de dientes laterales de la rádula ganchudos y lisos, dientes centrales ganchudos, alargados y sin dentículos. Peltodoris greeleyiy Discodoris aurilason transferidas al género Diaululaen base a la presencia de cariofilídeos, vainas rinofóricas y branquiales no elevadas, una prós- tata aplanada dividida en dos regiones, pene y vagina lisos, dientes de la rádula en forma de gancho y cutícula labial lisa. La distribución geográfica de Diaulula gree- leyi es extendida hasta Punta Uvita, Costa Rica y la distribución geográfica de Diaulula aurilaes extendida desde México hasta Panamá. 65 66 PROCEEDINGS OF THE CALIFORNIAACADEMYOF SCIENCES Volume 54, No. 4 Intensive field work along the Pacific coast of Costa Rica has revealed the presence of three species of caryophyllidia-bearing dorids. The species, Taringa aivicaEv. Marcus and Er. Marcus, 1967, Peltodoris nayaritaOrtea and Llera, 1981 and Discodoris aurilaMarcus, 1976 have already been reported from other areas in the eastern Pacific, but their anatomy was poorly described and the presence of caryophyllidia had been overlooked. Valdés and Gosliner (2001) recently studied the phylogenetic relationships of the caryophyl- lidia-bearing dorids, which according to these authors are a monophyletic group. They also syn- onymized several genera previously considered as valid or regarded as uncertain. Therefore, the caryophyllidia-bearing dorid species from Costa Rica need to be re-examined in light of the new evidence. The objective of the present paper is to re-examine the three described species of the caryophyllidia-bearing dorids present in Costa Rica. The material examined is deposited at the Department of Invertebrate Zoology and Geology, California Acaemy of Sciences, San Francisco (CASIZ), Instituto Nacional de Biodiversidad, Costa Rica (INBio), the Natural History Museum of Los Angeles County (LACM), Muséum National d’Histoire Naturelle, Paris (MNHN), and the National Museum of Natural History (USNM). SPECIES DESCRIPTION Genus Taringa Er. Marcus, 1955 Type species: Taringa telopiaEr. Marcus, 1955 Taringa aivicaEv. Marcus and Er. Marcus, 1967 (Figs 1A–B, 2A–D, 3A–E) Taringa aivicaMarcus and Marcus, 1967:89–92, figs. 115–119. Taringa aivica timiaMarcus and Marcus, 1967:189–191, figs. 47–51; Behrens and Henderson, 1982:197–199, figs.1–4. MATERIALEXAMINED San Miguel, Cabo Blanco, Costa Rica, May 16, 1998, 1 specimen, 12 mm preserved length, 2 m depth, leg. A. Berrocal (INB0001496644); San Miguel Station, Cabo Blanco, Costa Rica, January 28, 1999, 2 specimens, 30–31 mm preserved length, intertidal, leg. F. Alvarado (INB0001496686); San Miguel Station, Cabo Blanco, Costa Rica, January 28, 1999, 11 specimens, 10–20 mm preserved length, intertidal, leg. F. Alvarado (INB0001496491); San Miguel Station, Cabo Blanco, Costa Rica, January 22, 1999, 18 specimens, 9–23 mm preserved length, intertidal, leg. F. Alvarado (INB0001496522); San Miguel Station, Cabo Blanco, Costa Rica, May 17, 1999, 1 specimen, 4 mm preserved length, 2 m depth, leg. S. Ávila (INB0001496524); Playa Coralito, Peñón del Coral, Puntarenas, Costa Rica, January 29, 1999, 1 specimen, 12 mm preserved length, intertidal, leg. F. Alvarado (INB0001496675); Punta Uvita, Puntarenas, Costa Rica, January 15, 2000, 9 specimens, 4–12 mm preserved length, intertidal, leg. M. Calderón (INB0001496174);San Pedrillo, Osa Peninsula, Costa Rica, January 19, 2000, 1 specimen, 6 mm preserved length, inter- tidal, leg. A. Berrocal (INB0001496548); San Pedrillo, Osa Peninsula, Costa Rica, January 15, 2000, 1 specimen, 16 mm preserved length, intertidal, leg. M. Calderón (INB0001495952); San Pedrillo, Osa Peninsula, Costa Rica, February 27, 1998, 3 specimens, 9–10 mm preserved length, FIGURE1. Living animals. A–B. Taringa aivica(INB0001496491); C. Diaulula greeleyi (INB0001496508); D. Diaulula aurila(INB0001495896). CAMACHO-GARCÍAAND VALDÉS: DORIDNUDIBRANCHS FROM COSTARICA 67 68 PROCEEDINGS OF THE CALIFORNIAACADEMYOF SCIENCES Volume 54, No. 4 intertidal, leg. A. Berrocal (INB000146490); San Pedrillo, Osa Peninsula, Costa Rica, February 27,1998, 1 specimen, 9 mm preserved length, intertidal, leg. A. Berrocal (INB0001496489); Playa Gallardo, Golfo Dulce, Costa Rica, February 12,1997, 1 specimen, 16 mm preserved length, inter- tidal, leg. S. Ávila (INB0001496523); Punta Larga, Golfo Dulce, Costa Rica, November 29,1997, 6 specimens, 5–16 mm preserved length, intertidal, leg. M. Madrigal (INB0001496484); Punta Larga, Golfo Dulce, Costa Rica, November 27, 1997, 2 specimens, 14–18 mm preserved length, intertidal, leg. A. Berrocal (INB0001496525). GEOGRAPHIC RANGE From Palos Verdes, California (Behens and Henderson, 1982) to Sonora, Mexico and the Canal Zone, Panama (Marcus and Marcus, 1967). EXTERNALMORPHOLOGY The body is oval to elongate (Fig. 1A–B). The dorsum is covered with caryophyllidia about 0.15 mm long (Fig. 2D).There are some larger, conical tubercles arranged in two rows on both sides of the visceral hump. The dorsal color is variable ranging from pale yellow to dark brown. There is no correlation between the size of the animal and the dorsal color. Normally specimens have irregularly distributed darker patches on the dorsum; patches may be more densely arranged on the center of the dorsum. The larger tubercles are white or cream white in most specimens. There is a row of white patches on both sides of the dorsal hump, around the larger tubercles, that may be absent in some specimens and may be larger in others, almost occupying the entire mantle margin. The rhinophores are dark gray or black with numerous white or cream white spots on the club. The rhinophores have 17 lamellae. Occasionally there are white spots surrounding the rhinophoral sheath. The rhinophoral apex is white or cream-white. The gill is composed of six tripinnate branchial leaves. The leaves are yellowish or cream-white with minute dark spots. Ventrally, the anterior border of the foot is grooved and notched (Fig. 3E). ANATOMY The labial cuticle is smooth. The radular formula is 32 ×(39.0.39) in a 26 mm preserved length specimen (INB0001496522). Rachidian teeth are absent (Fig. 2A). The innermost teeth are hamate with a wide base and denticles. The lateral teeth are hamate, having a narrow base and a very con- spicuous prolongation on the upper side (Fig 2B). There are four to nine denticles on each lateral tooth. These denticles decrease in number towards the central part of the radula. The lateral teeth increase in size gradually towards the medial portion of the half-row. There are three or four pecti- nate outermost teeth (Fig. 2C). The stomach is oval and connects distally to the long intestine that forms a loop and runs to the anal opening (Fig 3A). The ampulla is very long and convoluted in the middle portion (Fig. 3C). It enters the female glands near their nidamental opening. The deferent duct is long and convoluted, and enters the flat- tened prostate. The proximal end of the deferent duct opens into a common atrium with the vagi- na. The vagina is long and tubular in shape and almost as thick as the deferent duct. At its distal end, the vagina connects to the large and oval bursa copulatrix. Both, the duct that leads from the seminal receptacle to the bursa copulatrix and the vaginal duct, are joined. The pear-shaped semi- nal receptacle is smaller than the bursa copulatrix (Fig. 3D). It is connected to the bursa copulatrix by a long and coiled duct. The penial cuticle is conical or bell-shaped (Fig. 3B). CAMACHO-GARCÍAAND VALDÉS: DORIDNUDIBRANCHS FROM COSTARICA 69 C. m. µ 0 1 = ar b e al c s h, et e al t er at L B. m; µ 0 1 = ar b e al c s h, et e al t er at er l n Inm. A. 0µ hs. = 2 M photograpdia, scale bar 01496522), SED. Caryophylli 00m. (INB20 µ vicabar= 2. Taringa aial teeth, scale UREater FIGer l ut O 70 PROCEEDINGS OF THE CALIFORNIAACADEMYOF SCIENCES Volume 54, No. 4 FIGURE3. Anatomy of Taringa aivica(INB0001496522 ) A. Dorsal view of the internal organs, scale bar= 1mm; B. Penis, scale bar= 0.25 mm; C. Reproductive system, scale bar= 1mm; D. Detail of the reproductive system, scale bar=1mm; E. Ventral view of the mouth area, scale bar= 1mm. Abbreviations: am=ampulla; b=blood gland; bc=bursa copulatrix; dd=deferent duct; dg=digestive gland; fg=female gland; h=heart; i=intestine; ot=oral tube; pr=prostate; sh=syrinx; sr=sem- inal receptacle; st=stomach; t=oral tentacle; v=vagina. CAMACHO-GARCÍAAND VALDÉS: DORIDNUDIBRANCHS FROM COSTARICA 71 REMARKS The study of several specimens and the review of the original description confirms that the external and internal features of this species fit with those of the genus Taringa. The presence of a flattened prostate with two portions, an unarmed vagina, a penis armed with a cuticular structure, inner and mid-lateral hamate radular teeth and pectinated outermost teeth are characteristics of this genus (Valdés and Gosliner 2001). According to Marcus and Marcus (1967) the differences between Taringa aivica aivica and Taringa aivica timia are the presence of an outermost pectinated tooth with a broad spine in Taringa aivica timiathat is not present in T. aivica aivicaand the strong denticles of the lateral teeth in T. aivica aivica. Also, they found uniformly distributed caryophyllidia and sometimes bicuspid papillae in Taringa aivica timia, and very small caryophyllidia and conical papillae in Taringa aivi- ca. Behrens and Henderson (1982) reported Taringa aivica timia from Palos Verdes, California, and rovided additional anatomical details. In this study Behrens and Henderson found a bell-shaped papilla in the penial cuticle and 5 to 10 pointed denticles on the outer side of their cusp, but appar- ently the broad spine mentioned by Marcus and Marcus (1967) is missing. In the present study, we have found great variability in dorsal coloration as well as in the arrangement of the caryophyllidia and papillae (Figs. 1A–B). Aspine on the outermost pectinated teeth was not found in the material study and is also absent in the specimens assigned to Taringa aivica timia by Behrens and Henderson (1982). The presence or absence of this spine as well as the shape of the penial cuticle are most likely due to intraspecific variation. We consider that the features mentioned by Marcus and Marcus (1967) are not enough to justify the existence of two different subspecies and Taringa aivica timiaand Taringa aivica aivicashould be synonymized. Genus DiaululaBergh, 1878 Type species: Doris sandiegensisCooper, 1863 Diaulula greeleyi(MacFarland, 1909) (Figs. 1C, 4A–D, 5A–D) Peltodoris greeleyi MacFarland, 1909:84–88, pl.15, figs. 77–82; Marcus, 1955; Marcus and Marcus, 1967; Eyster, 1980:588. Peltodoris nayaritaOrtea and Llera, 1981:47–51, figs. 1–4 (also cited as Anisodoris). MATERIALEXAMINED HOLOTYPEof Peltodoris greeleyi: Alagoas, Riacho Doce, Brazil, July 28, 1899, 1 specimen, 9 mm preserved length, leg. A.W. Greeley. (CASIZ 21021). HOLOTYPE of Peltodoris nayarita: Isabel Island, Nayarit, Mexico (21º52′ N, 105º54′ W), 1 specimen, 22 mm preserved length, contracted and dissected (MNHN). ADDITIONALMATERIALEXAMINED San Miguel Station, Cabo Blanco, Costa Rica, May 17, 1998, 1 specimen, 10 mm preserved length, 2 m depth, leg S. Ávila (INB0001500647); San Miguel Station, Cabo Blanco, Costa Rica, January 26, 1999, 22 specimens, 3–13 mm preserved length, intertidal, leg. F. Alvarado (INB0001496509); San Miguel Station, Cabo Blanco, Costa Rica, January 22, 1999, 39 specimens, 2–16 mm preserved length, intertidal, leg. F. Alvarado (INB0001496508); Ballena Island, Uvita, 72 PROCEEDINGS OF THE CALIFORNIAACADEMYOF SCIENCES Volume 54, No. 4 m. µ 0 1 = ar b e al c s h, et e al t er at L B. m; µ 0 1 = ar b e al c s h, et e al t er at er l n Inm. A. 0µ hs. = 2 otograpcale bar hs M pdia, SEylli 6508), aryoph 9C 014D. 00m. Bµ N0 ula greeleyi(Ih, scale bar= 1 ulet ae 4. Dieral t FIGUREOuter lat C. CAMACHO-GARCÍAAND VALDÉS: DORIDNUDIBRANCHS FROM COSTARICA 73 Puntarenas, Costa Rica, January 16, 2000, 3 specimens, 2–6 mm preserved length, 6 m depth, leg. M. Calderón (INB0001496530); Punta Uvita, Puntarenas, Costa Rica, January 15, 2000, 7 speci- mens, 5–9 mm preserved length, intertidal, leg. M. Calderón (INB0001496515); Playa Ventanas, Puntarenas, Costa Rica, January 17, 2000, 5 specimens, 5–6 mm preserved length, intertidal, leg. M. Calderón (INB0001496529); San Pedrillo, Osa Peninsula, January 27, 1998, 1 specimen, 11 mm preserved length, intertidal, leg. A. Berrocal (INB0001496507); San Pedrillo, Osa Peninsula, Costa Rica, January 20, 2000, 2 specimens, 2–10 mm preserved length, intertidal, leg. M. Calderón (INB0001496521); San Pedrillo, Osa Peninsula, Costa Rica, January 19, 2000, 2 specimens, 10–11 mm preserved length, intertidal, leg. A. Berrocal (INB0001496516). GEOGRAPHIC RANGE This species is found in Florida (Marcus and Marcus 1967), Brazil (Marcus 1955), South Carolina (Eyster 1980), Nayarit, Mexico (Ortea and Llera 1981), Punta Eugenia, Baja California, México (Bertsch et al. 2000) and the Pacific coast of Costa Rica. EXTERNALMORPHOLOGY The body is oval to elongate (Fig. 1C). The dorsum is covered with long caryophyllidia, about 100 mm long (Fig. 4D). The body is pale yellow to orange. The dorsum is covered with a number of brown patches that may be darker in some specimens. These patches are more densely arranged near the mantle edge. On the mantle edge there are some large, opaque white patches. The rhinophoral sheaths are very inflated and pale cream white or white in color. The gill sheath is also pale or white and in some specimens it is edged by a thin brown line. The rhinophores are pale yel- low, with the club brown and the apex opaque white or pale yellow. There are 13 lamellae present in the rhinophores. The gill is composed of 12 unipinnate branchial leaves. They are yellow to dark brown. In the living animal the branchial leaves are oriented inwards. Ventrally the anterior border of the foot is grooved and notched. The oral tentacles are short and conical (Fig. 5D). ANATOMY The labial cuticle is smooth. The radular formula is 37 x (55.0.55) in a 10 mm preserved length specimen (INB0001496508). Rachidian teeth are absent (Fig. 4A). The lateral teeth are hamate, having a single cusp and lacking denticles (Fig 4B). The teeth increase in size gradually towards the medial portion of the half-row. The outermost teeth are very small and elongate, also lacking denticles (Fig. 4C). The esophagus is long and connects directly to the stomach (Fig. 5A). The ampulla is very long (Fig. 5B). It enters the female glands near their nidamental opening. The prostate is flattened and granular. It is divided into two different portions that are clearly dis- tinguishable by their different texture and coloration. The deferent duct is long, and expands into the wide ejaculatory portion. The deferent duct opens into a common atrium with the vagina. There are no penial hooks. The vagina is long and wide. At its distal end, the vagina connects to the large and rounded bursa copulatrix. Another duct, which connects to the seminal receptacle and the uter- ine duct, leads from the bursa copulatrix. The bursa copulatrix is about ten times larger than the seminal receptacle (Fig. 5B–C). REMARKS MacFarland (1909) described Peltodoris greeleyi from Brazil. Later, Marcus (1955) and Marcus (1967) redescribed this species from the same locality. According to these authors, the main 74 PROCEEDINGS OF THE CALIFORNIAACADEMYOF SCIENCES Volume 54, No. 4 FIGURE5. Anatomy of Diaulula greeleyi(INB0001496508). A. Dorsal view of the internal organs, scale bar= 1mm; B. Reproductive system, scale bar = 1mm; C. Detail of the reproductive system, scale bar= 1 mm; D. Ventral view of the mouth area, scale bar= 1mm. Abbreviations: am=ampulla; b=blood gland; bc=bursa copulatrix; dd=deferent duct; dg=digestive gland; fg=female gland; h=heart; i=intestine; ot=oral tube; pr=prostate; sh=syrinx; sr=seminal receptacle; st=stomach; t=oral tentacle; v=vagina. distinctive features of this species are the yellowish to orange color of the living animals with some small brown spots on the center and sides, the prominent branchial and rhinophoral sheaths, the smooth labial cuticle, the absence of rachidian teeth, the unipinnate gills, the outermost tooth small- er than the remaining teeth, the absence of denticles and the outermost, and midlateral teeth with cups. Ortea and Llera (1981) described the species Peltodoris nayarita from Nayarit, Mexico. Peltodoris nayaritais characterized by having a yellow mantle with small brown spots all over the dorsum and sometimes concentrated in the middle portion, high branchial and rhinophoral sheaths, smooth labial cuticle, unipinnate branchial leaves, outermost teeth smaller and outermost midlat- eral teeth with a cusp. Ortea and Llera (1981) placed this species in the genera Peltodoris and Anisodoris at the same time with no clear explanation. They also considered that Peltodoris and Anisodorisare synonyms. By studying the type material of Peltodoris greeleyi and Peltodoris nayarita, we found that both species share the presence of a smaller outermost tooth with a single cusp and no denticles, hamate lateral teeth with no denticles and a single cusp, and outermost teeth smaller than the