Diaulula greeleyi (MacFarland, 1909)

Alvim, Juliana & Pimenta, Alexandre Dias, 2013, Taxonomic review of the family Discodorididae (Mollusca: Gastropoda: Nudibranchia) from Brazil, with descriptions of two new species, Zootaxa 3745 (2), pp. 152-198 : 173-176

Diaulula greeleyi (MacFarland, 1909)

( Figures 1 F; 13–14)

Peltodoris greeleyi MacFarland, 1909: 84 , plt. XV, figs. 77–82; Er. Marcus (1955: 137, plt. 14, figs. 126–132); Ev. Marcus & Er. Marcus (1967a: 72, figs. 94–98); Eyster (1980: 588); Rios (2009: 427).

Diaulula greeleyi: Camacho-García & Valdés (2003: 71, figs. 1C, 4A–D, 5A–D); Valdés (2004b: 2, figs. 1A, 2, 3); Valdés et al. (2006: 188); García et al. (2008: 142); Padula et al. (2012: 9).

Type material. Holotype CASIZ 21021, 28 July 1899, 9.0 mm preserved length, A.W. Greeley leg.

Type locality. Riacho Doce, Alagoas state, Brazil.

Material examined. U.S.A.: Miami: MZSP 75313, 1971, E. Marcus coll. [2; one dissected]; Brazil: Pernambuco state: Praia de Suape: MZSP 86138, 19 /vii/2005, S. Almeida coll. [1]; Alagoas state, Saco da Pedra: MNRJ 13193, 08 /i/2008, V. Padula and J. Bahia colls. [2; two dissected]; Rio de Janeiro state: Búzios: Praia da Tartaruga: MNRJ 12310, 26 /vi/2005, V. Padula coll. [1]; MNRJ 12308, 22 /ii/2006, V. Padula coll. [5]; MNRJ 12311, 24 /iv/2005, V. Padula coll. [1]; MNRJ 14968, 25 /ix/2009, J. Alvim coll. [1]; MNRJ 10878, 21 /x/2006, V. Padula coll. [1]; Praia da Armação de Búzios: MZSP 25278, vii/1957, L.R.Tommasi coll. [1]; Cabo Frio: Canal de Itajurú: MNRJ 15034, 12 /x/2009, J. Alvim coll. [2; two dissected]; MNRJ 13784, 24 /v/2009, J. Alvim and T. Belmonte colls. [2]; MNRJ 13994, 05 /vii/2009, J. Alvim coll. [5; one dissected]; MNRJ 14974, 23 /viii/2009, J. Alvim coll. [2]; Praia das Conchas: MNRJ 13298, 21 /iv/2008, J. Bahia coll. [1]; MNRJ 12309, V. Padula coll. [1]; MNRJ 12307, 14 /x/2006, V. Padula coll. [2]; MNRJ 31367, 15 /iii/2013, J. Alvim coll. [2]; Arraial do Cabo: Praia do Forno: MNRJ 11059, 13 /iii/2007, F. Santos coll. [1]; MNRJ 12788, 16 /iii/2006, J. Alvim coll. [2]; Angra dos reis: Praia do Leste: MZSP 29732, 1958, E. Marcus coll. [1]; São Paulo state: São Sebastião: MZSP 25341, 1958, E. Marcus coll. [1]; Praia do Portinho: MZSP 92740, 18 /ix/2009, F. Santos [1]; without locality data: MZSP 37961 (ex-Marcus’s collection).

Geographical distribution. U.S.A.: South Carolina (Eyster, 1980); Florida (Ev. Marcus & Er. Marcus, 1967a; Valdés, 2004b); Bahamas (Valdés et al., 2006); Brazil: Pernambuco state: Praia do Suape (present study); Alagoas state: Riacho Doce (MacFarland, 1909); Rio de Janeiro state: Cabo Frio (Ev. Marcus & Er. Marcus, 1967a), Búzios (García et al., 2008), Arraial do Cabo, Angra dos Reis (present study); São Paulo state: Ubatatuba (Dayrat, 2010), Ilha de São Sebastião (Er. Marcus, 1955).

Description. External morphology ( Figures 1 F; 13E–F): body elliptical, slightly depressed, up to 14.0 mm long alive, with two times greater length than width. Mantle densely covered by equidistant caryophyllidia ranging in height from 72 µm to 120 µm. In each caryophyllidium six or seven spicules protrude around tubercle; tubercle apex presents a ciliary elongated tuft (tuft diameter: 14 µm to 19 µm). Rhinophoral and branchial sheaths prominent (approximately 0.3 mm high), densely covered by caryophyllia of same size as those through mantle. Rhinophores long, with cylindrical apex, 9 to 12 diagonals perfoliations and spiculated at base. Gill with 10–12 retractile, simple branchial leaves, arranged to form a closed circle around high anal cone. Foot narrower than mantle and, posteriorly may project beyond notum in a small rounded tail; anterior foot border notched on two “lips”. Conical and small oral tentacles. Living specimens presenting body predominantly yellow with some beige spots approximately circular, more concentrated on mantle edge, and other brown blotches more concentrated in middle of dorsum, not evident in juveniles; rhinophores and gill with yellow/orange pigment, darker than rest of mantle.

Labial cuticle and radula (Figures: 13A–D): labial cuticle smooth. Radula formula 28 x 33.0. 33 in preserved specimen measuring 9.0 mm in length and 38 x 60.0. 60 in specimen measuring 9.0 mm in length; lateral plates smooth and hook-shaped, without denticles; teeth more developed in center of rows; innermost lateral teeth smaller than others, and outer lateral teeth with rounded to triangular protuberance at convex portion of cusp.

Reproductive system ( Figure 14 ): hermaphrodite duct connecting to long and slightly convoluted ampulla. Postampullary gonoduct very short, connecting to oviduct and prostate. Prostate granular, divided into two parts; small, less dense and whitish part proximal and, denser and yellow at distal part. Distal portion of vas deferens, long, narrow, convoluted, enlarged near gonopore, opening in common atrium with vagina. Vagina elongated and narrow partially covered by prostate. Bursa serially arranged, non-convoluted vaginal duct connecting to rounded seminal receptacle; very short uterine duct. Receptacle with 1/3 to 1/4 bursa’s size.

Biology. Egg mass forms a spiral ribbon with crenulated border. Rosy ribbon with two turns in counterclockwise direction and contains numerous rows of many tiny eggs. There is one egg per capsule connected by translucent matrix.

Remarks. Diaulula greeleyi was originally described in the genus Peltodoris by MacFarland (1909) based on one preserved specimen, without any information about coloration. Er. Marcus (1955) re-described the species, and Camacho-García and Valdés (2003) re-allocated it to the genus Diaulula based on the presence of caryophyllidia, a penis or vagina not armed, a smooth labial cuticle, smooth teeth and prominent rhinophores and branchial sheaths. In addition, Camacho-García and Valdés (2003) synonymized Peltodoris nayarita Ortea & Llera, 1981 , from the Pacific coast of Costa Rica with D. greeleyi , emphasizing some similarities with regard to external coloration, labial armature, radula, and the reproductive system.

In fact, the micrographs of radula and an illustration of the reproductive system of the specimen of D. greeleyi from the Pacific coast of Costa Rica, studied by Camacho-García and Valdés (2003: Figs. 3–4 ), indicate a striking resemblance with the specimens from Brazil studied herein. However, there are significant differences in the dimensions of caryophyllidia between the specimens from the two regions. The specimens from Costa Rica present a caryophyllidium with an average length of 20 µm whereas in those from Brazil and Florida, it is much longer (72 µm–120 µm) ( Figs. 13 E–F). Additionally, the caryophyllidia diameter is larger in the specimens from Costa Rica (36 µm– 60 µm) than in specimens from Brazil and Florida (14 µm–20 µm) ( Figs. 13 E–F). In summary, in the western Atlantic specimens, the caryophyllidia are longer and thinner than in the east Pacific ones. Therefore, we consider that Diaulula nayarita is a valid species.

Diaulula farmersi Valdés, 2004 b is largely similar to Diaulula greeleyi , but these species are clearly distinguishable on the basis of external coloration. D. farmesi does not seem to be a color variation of D. greeleyi because certain characteristics in relation to color are invariable in both species. All D. greeleyi specimens studied here exhibit a predominantly yellow/pale orange body with some beige spots and brown blotches, whereas D. farmersi is yellowish gray. Another remarkable feature relates to the coloration of rhinophores and gills, as these structures have the same coloration and a darker pigmentation than the rest of the dorsum in D. greeleyi , whereas in D. farmersi the rhinophores are much darker than the rest of the mantle (dark brown with white apices) and the gill is white. In D. greeleyi , only specimens with a very dark mantle display rhinophores that are almost black because of the concentration of the blotches (as in Valdés, 2004: 2, fig 1A); thus, a specimen with a light mantle never exhibits dark rhinophores, and indeed, a white gill has never been observed in this species.

Valdés (2004b) described the general coloration of a specimen of D. greeleyi from Florida as pale yellow, orange or brown, although the photograph of the animal in vivo (Valdés, 2004b; Fig. 1 A) indicates a pattern of almost black coloration, due to a high concentration of dark spots on the dorsum. Based on the available images and descriptions of Diaulula greeleyi from several localities (Valdés et al., 2006; Camacho-García & Valdés, 2003; Ev. Marcus & Er. Marcus, 1967a), it can be concluded that Caribbean specimens have more pronounced and darker blotches than the specimens from Brazil ( Fig. 1 F).

Figures

FIGURE 1. Living specimens; A, Thordisa diuda (MNRJ 13195, 9 mm), photo: V. Padula; B, Hoplodoris hansrosaorum (MNRJ 12924, 22 mm); C, Geitodoris pusae (MNRJ 11712, 12 mm); D, Discodoris branneri (MNRJ 14922, 87 mm); E, Discodoris hummelincki (MNRJ 13997, 32 mm); F, Diaulula greeleyi (MNRJ 14974, 10 mm); G, Rostanga byga (MNRJ 12371, 5 mm); H, Jorunna spazzola (MNRJ 13196, 5 mm), photo: V. Padula.

FIGURE 3. Thordisa diuda, SEM photographs of the radula and dorsum; A, half rows of radula; B – C, innermost teeth; B, inner side; C, outer side, denticle indicated by white arrow; D, midlateral teeth; E, marginal teeth; F, tubercle of the dorsum. A – E (MNRJ 13195); F (MZSP 75298).

FIGURE 4. Thordisa diuda, A – B, general view of reproductive system; A (MZSP 75298); B, Juvenile (3 mm in length) (MNRJ 13195). Abbreviations: am, ampulla; ag, accessory gland; bc, bursa copulatrix; dd, deferent duct; f, female glands; go, gonopore; ov, oviduct; pr, prostate; s, seminal receptacle; u, uterine duct; va, vagina.

FIGURE 13. Diaulula greeleyi, SEM photographs; A, detail of the labial cuticle; B, innermost lateral teeth; C, midlateral teeth; D, marginal teeth; E, general view of the dorsum; F, detail of the caryophyllidium. A (MNRJ 13193); B – D (MNRJ 13994); E – F (MNRJ 12307).

FIGURE 14. Diaulula greeleyi (MNRJ 15034); A, general view of reproductive system; B, uterine duct and adjacent structures. Abbreviations: am, ampulla; bc, bursa copulatrix; dd, deferent duct; f, female glands; go, gonopore; ov, oviduct; pr, prostate; s, seminal receptacle; u, uterine duct; va, vagina.