Doris granulosa, PEASE, 1860

Valdés, Ángel, 2002, A phylogenetic analysis and systematic revision of the cryptobranch dorids (Mollusca, Nudibranchia, Anthobranchia), Zoological Journal of the Linnean Society 136 (4), pp. 535-636 : 554-560

DORIS GRANULOSA PEASE, 1860 ( FIGS 4C , 9 , 10 )

Doriopsis granulosa Pease, 1860: 32–33 .

Doriopsis scabra Pease, 1871a: 300 , pl. 19, fig. 2A- C.

Doris ? flabellifera Cheeseman, 1881: 222–223 .

Doris (Ctenodoris) aurantiaca Eliot, 1913: 5–7 , pl. 1, fig. 1.

Guyonia flava Risbec, 1928: 103–104 , pl. 3, fig. 6, text fig. 21.

Type material

The type specimens of Doriopsis granulosa and Doriopsis scabra are untraceable; the type material of Doris flabellifera , as well as that of other nudibranchs described by Cheeseman, is lost (Bruce Marshall, pers. comm.). SYNTYPE of Guyonia flava Pease : New Caledonia, date unknown, one specimen, leg. J. Risbec ( MNHN).

Additional material

Small island south of the strait between Île Saint Marie and Île aux Nattes, Madagascar, 5 April 1990, one specimen, 12 mm preserved length, leg. T . M. Gosliner ( CASIZ 073536 ) .

External morphology

The background colour of the living animals is yelloworange. There is a number of small brown dots scattered on the surface, more densely arranged around the dorsal tubercles ( Fig. 4C ). The rhinophores and gill are also yellow-orange. The whole dorsum is covered with rounded, simple tubercles, all of them similar in size ( Fig. 9D ). The largest tubercles are those situated in the central region of the body. The rhinophoral and branchial sheaths have a few tubercles, similar to the rest of the dorsal tubercles. There are six tripinnate branchial leaves, arranged horizontally. The anal papilla is small, situated in the centre of the branchial circle of leaves. The rhinophores are elongate, having 12 lamellae in a 12-mm preserved length specimen.

Ventrally there are no oral tentacles, but two blunt prolongations on each side of the mouth opening ( Fig. 10F ). 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. 10D ) which attach to the body wall. The oval, muscular buccal bulb has two additional muscles attached. Two short salivary glands connect with the buccal bulb at each side of the oesophageal junction. The buccal bulb is shorter than the glandular portion of the oral tube. The labial cuticle is smooth. The radular formula is 47 ¥ 47.0. 47 in a 12-mm long specimen. Rachidian teeth are absent. The lateral teeth are narrow and elongate, having a single cusp and lacking denticles ( Fig. 9A ). The teeth from the middle portion of the half-row are larger than those closer to the medial portion of the radula ( Fig. 9B ). The outermost teeth are smaller and also smooth ( Fig. 9C ). The oesophagus is short and connects directly to the stomach ( Fig. 10A ).

The ampulla is long and convoluted, and branches into a short oviduct and the prostate ( Fig. 10B ). The oviduct enters the female gland mass near to its centre. The prostate is tubular, short, folded and granular. It connects with a short duct that narrows and expands again into the ejaculatory portion of the deferent duct. The muscular deferent duct opens into a common atrium with the vagina. The vagina is long. Near to its proximal end it joins the bursa copulatrix and the seminal receptacle. The uterine duct also leads from the vagina. The bursa copulatrix is oval in shape, about as large as the seminal receptacle.

In the central nervous system ( Fig. 10D ) the cerebral and pleural ganglia are fused and distinct from the pedal ganglia. There are three cerebral nerves leading from each cerebral ganglion and two pleural nerves leading from each pleural ganglion. 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 three nerves leading from the left ganglion and four from the right. The pedal and parapedal commissures are enveloped together with the visceral loop.

The circulatory system ( Fig. 10A ) consists of a large heart and a small blood gland situated in front of the central nervous system.

Remarks

Baba & Hamatani (1961) redescribed this species, under the name Doriopsis aurantiaca ( Eliot, 1913) , based on specimens collected from Japan. Kay & Young (1969) reported this species from Hawaii, this time under the name Doriopsis granulosa Pease, 1860 , and figured its reproductive system and the radula for the first time. They also suggested that Doris aurantiaca , Doriopsis scabra Pease, 1871 , Guyonia flava Risbec, 1928 and Doris flabellifera Cheeseman, 1881 could be synonyms.

Edmunds (1971) studied specimens from Tanzania which are similar to those from Hawaii, and confirmed the list of synonyms suggested by Kay & Young (1969). In contrast, Willan & Coleman (1984) considered that Doriopsis flabellifera is a distinct species, although they provided no anatomical evidence.

DORIS KERGUELENENSIS (BERGH, 1884)

( FIGS 11 , 12 )

Archidoris kerguelenensis Bergh, 1884b: 85–89 , pl. 1, figs 1–12.

Archidoris australis Bergh, 1884b: 89–91 , pl. 1, figs 13–18, pl. 2, fig. 13.

Archidoris rubescens Bergh 1898: 501–503 , pl. 29, figs 17–20.

Austrodoris michaelseni Odhner, 1926: 68–71 , pl. 2, figs 30-32, text figs 47-50.

Austrodoris crenulata Odhner, 1926: 75–76 , pl. 2, figs 38, 39, text fig. 54.

Austrodoris macmurdensis Odhner, 1934: 260–263 , pl. 2, figs 21–23, text figs 25-27.

Austrodoris tomentosa Odhner, 1934: 265–267 , pl. 2, figs 19, 20, text fig. 32.

Austrodoris nivium Odhner, 1934: 267–269 , pl. 2 figs 21–23, text figs 33-35.

Austrodoris mishu Marcus, 1985: 219–222 , figs 1–12.

Austrodoris vicentei Marcus, 1985: 214 , 217.

Austrodoris georgiensis García et al. 1993: 417–421 , figs 1–8.

Type material

For a list of the extant type material of the nominal species included in the genus Austrodoris see Wägele (1990).

Additional material

North-west of Explorer’s Cove , New Harbor, west side of McMurdo Sound, Antarctica, 17 December 1985, two specimens, 54–66 mm preserved length, leg. K. A. Miller ( CASIZ 087312 ) .

External morphology

The external morphology of this species has been described in detail by Wägele (1990). My specimens were preserved, so no data on the living animals are available.

The general colour of the living animals is uniformly white ( Wägele, 1990). The rhinophores and gill are also white. The whole dorsum is covered with rounded and simple tubercles varying in size and shape ( Fig. 11D ). The largest tubercles are situated in the central region of the body. The rhinophoral and branchial sheath are surrounded by tubercles similar to the rest of the dorsal tubercles. There are 7–9 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 32 lamellae in a 66-mm preserved length specimen.

Ventrally there are no oral tentacles, but two blunt prolongations on each side of the mouth opening ( Fig. 12F ). 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. 12D ) which attach to the body wall. The oval, muscular buccal bulb has two additional muscles attached; two long and wide salivary glands connect with it at each side of the oesophageal junction. The buccal bulb is twice as long as the glandular portion of the oral tube. The labial cuticle is smooth. The radular formula is 24 ¥ 37.0. 37 in a 54-mm long specimen. Rachidian teeth are absent. The lateral teeth are narrow and elongate, having a single cusp and lacking denticles ( Fig. 11A ). The teeth from the middle portion of the half-row are larger than those closer to the medial portion of the radula ( Fig. 11B ). The outermost teeth are smaller and also lack denticles ( Fig. 11C ). The oesophagus is short and connects directly to the stomach ( Fig. 12A ).

The ampulla is very long and convoluted. It branches into a short oviduct and the prostate ( Fig. 12B ). The oviduct enters the female gland mass near to its centre. The prostate is tubular, very long and folded ( Fig. 12B ). It connects with a long duct that narrows and expands again into the large ejaculatory portion of the deferent duct. The muscular deferent duct opens into a short common atrium with the vagina. The vagina is short and wide. Near to its proximal end it joins the bursa copulatrix and the seminal receptacle. The uterine duct also leads from this duct. The bursa copulatrix is irregular in shape, about as large as the seminal receptacle ( Fig. 12C ).

In the central nervous system ( Fig. 12E ) the cerebral and pleural ganglia are fused and distinct from the pedal ganglia. There are three cerebral nerves leading from each cerebral ganglion and three pleural nerves leading from each pleural ganglion. There is a separate abdominal ganglion on the right side of the visceral loop. This ganglion appears to have several distinctive portions and one of them seems to be the genital ganglion. The buccal ganglia are near to the rest of the central nervous system, joined to the cerebral ganglia by two relatively short nerves. Gastrooesophageal, rhinophoral and optical ganglia are present. The pedal ganglia are clearly separated, having three nerves leading from the left ganglion and two from the right one. The pedal and parapedal commissures are enveloped together with the visceral loop.

The circulatory system ( Fig. 12A ) consists of a large heart and a single large blood gland situated in front of the central nervous system.

Remarks

Wägele (1990) revised the genus Austrodoris and concluded that all the Antarctic species previously assigned to it are synonyms of Austrodoris kerguelensis (Bergh, 1884) . She also described in detail the anatomy and external morphology of this species.

More recently García et al. (1993) described the new species Austrodoris georgiensis , which is also a synonym of Austrodoris kerguelensis . García et al. (1993) based Austrodoris georgiensis on a single specimen collected from South Georgia, in the Atlantic Antarctic sector. The only difference between A. georgiensis and A. kerguelenensis is the presence of an elongate bursa copulatrix in the former. As other features of both nominal species (e.g. external morphology, radula, other reproductive organs), are identical, it is likely that the single specimen assigned to A. georgiensis is just an aberrant specimen of A. kerguelenensis . Another possibility is that the bursa copulatrix is more variable than assumed until now.

Figures

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.

Figure 9. Doris granulosa (CASIZ 073536), SEM images of the radula and dorsal tubercles. A, inner lateral teeth; scale bar = 30 Mm. B, mid-lateral teeth; scale bar = 30 Mm. C, outer lateral teeth; scale bar = 25 Mm. D, dorsal tubercles; scale bar = 420 Mm.

Figure 10. Doris granulosa (CASIZ 073536). A, general view of the anatomy; scale bar = 1 mm. B, reproductive system; scale bar = 1 mm. C, detail of the bursa copulatrix and seminal receptacle; scale bar = 1 mm. D, lateral view of the buccal bulb; scale bar = 1 mm. E, central nervous system; scale bar = 0.5 mm. F, ventral view of the mouth area; scale bar = 2 mm.

Figure 11. Doris kerguelenensis (CASIZ 087312), SEM images of the radula and dorsal tubercles. A, inner lateral teeth; scale bar = 200 Mm. B, mid-lateral teeth; scale bar = 150 Mm. C, outer lateral teeth; scale bar = 100 Mm. D, dorsal tubercles; scale bar = 1 mm.

Figure 12. Doris kerguelenensis (CASIZ 087312). A, general view of the anatomy; scale bar = 2 mm. B, reproductive system; scale bar = 2 mm. C, detail of the bursa copulatrix and seminal receptacle; scale bar = 2 mm. D, lateral view of the buccal bulb; scale bar = 2 mm. E, central nervous system; scale bar = 1 mm. F, ventral view of the mouth area; scale bar = 2 mm.