A phylogenetic analysis and systematic revision of the cryptobranch dorids (Mollusca, Nudibranchia, Anthobranchia) Author Valdés, Ángel text Zoological Journal of the Linnean Society 2002 2002-12-31 136 4 535 636 https://academic.oup.com/zoolinnean/article-lookup/doi/10.1046/j.1096-3642.2002.00039.x journal article 5419 10.1046/j.1096-3642.2002.00039.x 8acc9095-eaff-47d7-b3da-91b6c2fb636e 0024-4082 4634200 DORIS PSEUDOARGUS RAPP, 1827 ( FIGS 4A , 5 , 6 ) Doris pseudoargus Rapp, 1827: 519 . Doris flavipes Leuckart, 1828: 14 . Doris leuckartii Delle Chiaje, 1841: 19 , pl. 40, fig. 3. Doris schembrii Verany, 1846: 21–22 . Type material Doris pseudoargus Rapp , the type material, collected from Le Havre, France , is untraceable. NEOTYPE (here designated): Locmariaquer, France , 13 April 1972 , one specimen, 22 mm preserved length, leg. P. Bouchet ( MNHN ). Doris flavipes Leuckart , the type material collected from the Mediterranean Sea is untraceable. Doris leuckartii Delle Chiaje , the type material collected from Nice, France , is untraceable. Doris schembrii Verany , SYNTYPES : Gulf of Geneva, Italy , two specimens ( MNHN ). The type material of Doris britannica Leach could not be located at BMNH and is probably lost. Additional material Las Llanas Beach , Muros de Nalón , Asturias , Spain , 16 August 1987 , one specimen , 17 mm preserved length, leg. A. Valdés ( CASIZ 121105 ). Naples , Italy 1902–03, one specimen , 33 mm preserved length, leg. F. M. MacFarland ( CASIZ 081871 ). Figure 4. Living animals. A, Doris pseudoargus (CASIZ 121105). B, Doris immonda (CASIZ 089023), photo by T. M. Gosliner. C, Doris granulosa (CASIZ 073536), photo by T. M. Gosliner. D, Discodoris boholiensis (CASIZ 083654), photo by T. M. Gosliner. E, Discodoris ketos , San Pedrillo , Puntarenas, Costa Rica, photo by T. M. Gosliner. F, Thordisa rubescens (CASIZ 015860), photo by T. M. Gosliner. G, Aphelodoris antillensis (CASIZ 077289), photo by T. M. Gosliner. H, Peltodoris atromaculata (CASIZ 119474). I, Peltodoris nobilis , Monterey Bay, California, photo by A. Smith. External morphology The general colour of the living animals varies from yellowish to pale brown, with pale purple, whitish, green, dark brown or reddish irregular patches on the dorsum ( Fig. 4A ). In some specimens there are only dark brown patches. The rhinophores and the gill are yellowish to pale brown. The whole dorsum is covered with rounded and simple tubercles, all of them similar in size ( Fig. 5D ). The largest tubercles are those situated in the central region of the body. The rhinophoral and branchial sheaths have several tubercles which are slightly stalked but otherwise similar to the rest of the dorsal tubercles. There are 8–9 tripinnate branchial leaves, forming a circle. The anal papilla is prominent, situated in the centre of the branchial circle of leaves. The rhinophores are elongate, having 14 lamellae in a 17-mm preserved length specimen. Ventrally, there are no oral tentacles, but two blunt prolongations on each side of the mouth opening ( Fig. 6E ). The anterior border of the foot is grooved but not notched. Anatomy The posterior end of the glandular portion of the oral tube has six strong retractor muscles ( Fig. 6D ) which attach to the body wall. Two long salivary glands connect with the buccal bulb at each side of the oesophageal junction. The buccal bulb is several times longer than the glandular portion of the oral tube. The labial cuticle is smooth. The radular formula is 41 ¥ 73.0. 73 in a 33-mm long specimen. Rachidian teeth are absent. The lateral teeth are narrow and elongate, having a single cusp and lacking denticles ( Fig. 5A ). The teeth from the middle portion of the half-row are larger than those closer to the medial portion of the radula ( Fig. 5B ). The outermost teeth are smaller and have a number of thin denticles ( Fig. 5C ). The oesophagus is short and connects directly to the stomach ( Fig. 5A ). Figure 5. Doris pseudoargus (CASIZ 081871), SEM images of the radula and dorsal tubercles. A, inner lateral teeth; scale bar = 75 Mm. B, mid-lateral teeth; scale bar = 75 Mm. C, outer lateral teeth; scale bar = 43 Mm. D, dorsal tubercles; scale bar = 750 Mm. Figure 6. Doris pseudoargus (CASIZ 081871). A, general view of the anatomy; scale bar = 2 mm. B, reproductive system; scale bar = 2 mm. C, detail of several reproductive organs; scale bar = 2 mm. D, lateral view of the buccal bulb; scale bar = 2 mm. E, ventral view of the mouth area; scale bar = 5 mm. E, central nervous system; scale bar = 1 mm. The ampulla is convoluted and branches into a short oviduct and the prostate ( Fig. 6C ). The oviduct enters the female gland mass near to its centre. The prostate is tubular, very long, folded and granular ( Fig. 6B ). It connects with a long duct that narrows and expands again into the huge ejaculatory portion of the deferent duct. The muscular deferent duct opens into a short common atrium with the vagina. The vagina is long and wide. Near to its proximal end it joins the duct connecting the bursa copulatrix and the seminal receptacle. The uterine duct also leads from this duct. The bursa copulatrix is irregular in shape, about 10 times larger than the seminal receptacle ( Fig. 6C ). In the central nervous system ( Fig. 6F ) the cerebral and pleural ganglia are fused and distinct from the pedal ganglia. There are four cerebral nerves leading from each cerebral ganglion, and three pleural nerves leading from the left pleural ganglion and two from the right one. There is no separate abdominal ganglion on the right side of the visceral loop. The buccal ganglia are near to the rest of the central nervous system, joined to the cerebral ganglia by two relatively short nerves. Gastro-oesophageal, rhinophoral and optical ganglia are present. The pedal ganglia are clearly separated, having five nerves leading from the left ganglion and four from the right one. The pedal and parapedal commissures are enveloped together with the visceral loop. The circulatory system ( Fig. 6A ) consists of a large heart and a single large blood gland situated over the central nervous system. Remarks Doris tuberculata Müller, 1778 was described on the basis of an undetermined number of specimens collected from Norway . Müller (1778) described the animals as golden, patelliform, with the dorsum covered with numerous hair-like yellowish tubercles. The description of the animals clearly represents a species of phanerobranch dorid, probably a member of the genera Acanthodoris J.E. Gray, 1850 , Adalaria Bergh, 1878 or Onchidoris Blainville, 1816 . Years later, Cuvier (1804) reported Doris tuberculata Müller, 1778 from the Atlantic coast of France based on two newly collected specimens, but indicating that his material was clearly different from Müller’s (1778) . The animals described by Cuvier are large cryptobranch dorids with the dorsum covered with rounded tubercles. Rapp (1827) described Doris pseudoargus from Le Havre, France , with the same characteristics of the specimens studied by Cuvier (1804) : ‘ash colour with dull reddish spots’, and therefore this is the first valid introduction of a name for this species. Johnston (1838) introduced the names D. britannica and D. montagui , without a description and in the synonymy of D. Tuberculata . Therefore they are nomina nuda and if they have not been used as valid before 1961 they are also not available ( ICZN, 1999 ). In the following years most authors referred to this species as Doris tuberculata , but with authorship of Cuvier. Examples include Delle Chiaje (1841) , Bergh (1878b) , Eliot (1910) , Vayssière (1913) O’Donoghue (1929) , Pruvot-Fol (1935) , Odhner (1939) . The scientific influence of Cuvier’s papers probably explains why subsequently many authors applied the name Doris tuberculata to this cryptobranch dorid species. The usage of the name Doris tuberculata for this species was challenged by the British School. Early on, Iredale & O’Donoghue (1923) for some unexplained reason decided that the animals named Doris tuberculata by Cuvier are a different species from specimens identified as such by Alder & Hancock and Eliot; they used the unavailable name Doris britannica , combined with the genus name Archidoris , for the latter. On the other hand, Pruvot-Fol (1931) argued that all these animals belonged to the same species - Doris tuberculata with authorship of Cuvier the valid name. The name Doris britannica very rarely appears in the literature. Thompson (1966) reintroduced the usage of the name Doris pseudoargus , also combined with Archidoris , but without a justification. Both Doris pseudoargus and Doris tuberculata have been equally used in modern literature, usually combined with the genus name Archidoris . Examples of the former in taxonomic papers include Schmekel & Portmann (1982) , Thompson & Brown (1984) , Cattaneo-Vietti et al . (1990) , Picton & Morrow (1994) ; examples of the latter include Ros (1975) , Barletta (1981) , Swennen & Dekker (1987) , Sabelli, Giannuzzi-Savelli & Bedulli (1990) . In addition, most papers on physiology, ecology or histology of this species have used the former ( Thompson, 1966 ; Rose, 1971 ; Potts, 1983 ; Jonas, 1986 ), whereas biochemistry papers have used the latter ( Cimino et al . 1993 ). In no cases did authors specify their reasons for using one or the other name, which increased the general confusion. Because both names are currently in use, the maintenance of the usage of the valid name for this species, Doris pseudoargus , would certainly not cause a larger disruption than the validation of the name Doris tuberculata . Doris pseudoargus is a well-known species that ranges from Nordkapp ( Norway ), Iceland and the Faroes to the Mediterranean Sea ( Thompson & Brown, 1984 ). The name D. tuberculata has been used for specimens that occur beyond the geographical range of this species. Savigny (1817) reported this species from the Red Sea, Bergh (1894) from the North Pacific and Lemche (1929) from the Gulf of Mexico. These three records are probably misidentifications (see Pruvot-Fol, 1935 and Thompson & Brown, 1984 , who have also listed several other synonyms for this species discussed here). Doris schembrii Verany, 1846 was originally described with the same external features of A. pseudoargus (see Verany, 1846 ), and the re-examination of its type material confirmed that these names are synonyms. Also, the original descriptions of Doris flavipes (see Leuckart, 1828 ) and Doris leuckartii (see Delle Chiaje, 1841 ) clearly show that they should be regarded as junior synonyms of A. pseudoargus . Doris flammea Alder & Hancock, 1844 and Doris mera Alder & Hancock, 1844 have been regarded as synonyms of D. pseudoargus (see Thompson & Brown, 1984 ). However, the original description of these species ( Alder & Hancock, 1845 -55) shows that they are externally very different from D. pseudoargus . Doris flammea is a bright orange-scarlet species, occasionally blotched with purple. The dorsum is covered with short, obtuse, spiculose tubercles. The rhinophores are large, tapering, orange with 10 or 11 scarlet lamellae. There are nine scarlet branchial leaves. This description resembles Rostanga rubra Risso, 1818 , but whether these two names are synonyms requires further investigation. Doris mera was described as a white species, ‘rather broad and elevated on the back’. This is very different from D. pseudoargus , which is a brownish species. Also, the dorsal tubercles of D. mera were described as being moderately sized, unequal and round. This is very similar to Aldisa zetlandica ( Alder & Hancock, 1854 ) , for which D. mera could be a synonym.