Discodoris branneri 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 : 166-170

Discodoris branneri MacFarland, 1909

( Figures 1 D; 9–10)

Doris (Dendrodoris crucis ) Orsted in Mörch, 1863: 33 (partially; according to Dayrat, 2010).

Discodoris notha Bergh, 1877: 530 , plt. LXI–LXII, figs. 3–9; 29–30; Bergh (1884b: 92); Bergh (1904: 53, plt. IV, figs. 7–14) (partially; according to Dayrat, 2010).

Discodoris branneri MacFarland, 1909: 66 , plt. XII, figs. 58–65; Rios (2009: 426); Padula et al. (2012: 6).

Carminodoris branneri: Perrone & Duneddu (1997: 52) .

Discodoris evelinae Er. Marcus, 1955: 143, figs. 141–150; Ev. Marcus & Er. Marcus (1967a: 75); Ev. Marcus & Er. Marcus (1969: 13); Ev. Marcus (1971: 944, fig. 43); Ev. Marcus (1972: 79); Ev. Marcus & Hughes (1974: 520, fig. 41); Ev. Marcus (1976b: 139); Bertsch (1976: 117, figs. 1–7, tbl. 1–2); Humann (1992: 241); Redfern (2001: 175, fig. 726, plt. 119); Valdés et al. (2006: 174) (in part); Debelius & Kuiter (2007: 250); García et al. (2008: 137); Rios (2009: 426).

Discodoris hedgpethi Ev. Marcus & Er. Marcus (1960: 254, figs. 7–11); Ev. Marcus & Er. Marcus (1967a: 75, figs. 98A– 98E); Er. Marcus & Ev. Marcus (1971: 49, figs. 111– 114).

Discodoris spetteda Ev. Marcus & Er. Marcus (1966: 181) Nomen nudum.

“ Montereina branneri ”: Dayrat (2010: 234, figs. 241–257).

Type material. Holotype: ZMA CASIZ 0 20019, 1899, 32.0 mm preserved length, A.W. Greeley leg.

Type locality. Riacho doce, Alagoas state, Brazil.

Material examined. Barbados: MZSP 37949; Brazil: Alagoas state: Recife do Francês: MNRJ 12931, 23 /xi/ 2007 [1]; Saco da Pedra: MNRJ 12942, 11 /i/2008, colls. J. Bahia & V. Padula [4; two dissected]; MNRJ 13102, 08 / i/2008, coll. Anderson [1]; MNRJ 13103, 22 /x/2006, coll. M. Dorigo [1]; MNRJ 13173, 11 /i/2008, colls. J. Bahia & V. Padula [1]; Riacho Doce: MNRJ 13174, 31 /i/2006 [1, one dissected]; Piscina dos Amores: MNRJ 12930, 02 / iv/2007 [1]; Ponta Verde: MNRJ 13175, 18 /iii/1992 [1]; Bahia state, Salvador: HSL MNRJ 7422 [1]; Rio de Janeiro state: Búzios, Praia da Tartaruga: MNRJ 15001, 09 /vi/2009, coll. T. Belmonte [1]; MNRJ 14934, 25 /xi/ 2009, coll. J. Alvim [1; one dissected]; Cabo Frio, Canal de Itajurú: MNRJ 10662, ix/1980, coll. L. R. Tostes [1; one dissected]; MNRJ 13199, 18 /v/2008, coll. V. Padula [1; one dissected]; MNRJ 14922, 22 /vii/2009, coll. J. Alvim [2]; Arraial do Cabo, Prainha: MNRJ 13172, ii/1984, colls. G.W. Nunan & M. R. Sá [1]; Praia do Forno: MNRJ 10669, ii/1983, coll. G. Nunan [2]; São Paulo state: Ilhabela: MZSP 41639 [1] and MZSP 41803[2], 07/v/ 2004, colls. L.R.Simone, C. M. Cunha, Gonçalves & Rosier; MZSP 41801, 06 /v/2004, colls. L.R.Simone, C. M. Cunha, Gonçalves & Rosier [2].

Geographical distribution. U.S.A.: Florida, Palm Beach (Ev. Marcus & Er. Marcus, 1967a); Texas, Port Arkansas (Ev. Marcus & Er. Marcus, 1960); Bahamas, Cayman Islands (according to Dayrat (2010) this distribution is still uncertain), Honduras, Jamaica, Puerto Rico, Barbados, Guadeloupe, Martinique, St. Lucia, St. Vincent and the Grenadines, Costa Rica, Panama, Colombia, Santa Marta, Venezuela (Valdés et al., 2006); Virgin Islands (Dayrat, 2010); Brazil: Pernambuco state: Suape (Ev. Marcus, 1971); Alagoas state (Padula et al., 2012): Recife do Francês, Saco de Pedra, Piscina dos amores (present study), Riacho Doce (MacFarland, 1909); Bahia state (present study); Rio de Janeiro state: Búzios (García et al., 2008), Cabo Frio and Arraial do Cabo (present study); São Paulo state: Ilha de São Sebastião (Er. Marcus, 1955).

Description. External morphology ( Figures 1 D; 9D–E): body oval, slightly depressed, up to 87 mm long alive, with 1.5 to 2.5 times greater length than width. Mantle densely covered by somewhat conical tubercles of different sizes (diameter 37 µm to 273 µm), irregularly disposed; tubercles can be more or less conical with five to 12 spicules that protrude outside; ciliary tuft at apex of tubercles, normally lost during fixation. Rhinophoral and branchial sheaths prominent and irregular, covered by tubercles; rhinophores long with 19 to 26 diagonal perfoliations and cylindrical apex. Gill with six retractile, tripinnate or tetrapinnate branchial leaves, symmetrically positioned along longitudinal axis of body; anal cone high, located between two most posterior branchial leaves. Foot narrower than mantle; anteriorly bilabiated and notched on upper “lip”. Oral tentacles conical. Color of living specimens predominantly brownish, with several brown and white blotches on dorsum of irregular sizes and arrangement, usually with four to 10 dark brown circular blotches larger in diameter and well defined (in some cases almost black); ventrally, white to cream; foot with brown blotches smaller and at higher density than ventral part of mantle; rhinophores with basal region of same brown tone as mantle, with some whitish spots, laminated part yellowish-brown, with white spots on perfoliations, apical part white; branchial leaves cream/beige with numerous tiny brownish spots.

Labial cuticle and radula ( Figures 9 A–C): labial cuticle with yellow lateral plates with numerous elongated elements; elements approximately rectangular, long and filiform on outer margin and, low and short on inner margin. Radula formula 31 x 46.0. 46 in dry preserved specimen measuring 27.0 mm in length and 32 x 62.0. 62 in preserved specimen measuring 53.0 mm in length; lateral teeth hook-shaped, smooth, larger and more developed in center of rows; marginal teeth thinner and less curved, with a protuberance on convex surface of base of cusp.

Reproductive system ( Figures 9 F–I; 10A): hermaphrodite duct connecting to long and convolute ampulla. Postampullary gonoduct short, connecting to oviduct and prostate. Prostate granular, divided into two parts, approximately of same size, less dense part proximal, denser distal part. Deferent duct elongated and enlarged on distal portion. Penis of 3.3 mm to 8.0 mm length, covered by penial hooks; there is one spine more developed than others attached on base of penis; distal part smooth, without penial hooks. Vagina elongated and convoluted, 2x to 3x thicker than deferent duct, opening into rounded bursa copulatrix. Bursa serially arranged, vaginal duct convoluted connecting to short-stalked seminal receptacle; uterine duct very short.

Biology ( Figures 10 B–C): egg mass usually forming a spiral ribbon of 45.0 mm to 49.0 mm diameter, with white eggs and crenulated border; ribbon with around six whorls in counterclockwise direction and with numerous rows of many tiny eggs; only in one case the same specimen deposited one egg mass with white eggs in its natural habitat, and another one coloured violet (deep purple) in aquarium. Some specimens autotomized parts of mantle margin when disturbed.

Remarks. The specimens studied here fits largely in the genus Discodoris Bergh, 1877 , because this species presents all the diagnostic features of the genus, including the dorsum covered with simple tubercles, stiffened by integumentary spicules ( Figs. 9 D–E); anterior border of the foot grooved and notched; labial cuticle armature with rodlets ( Fig. 9 A); radula composed of simple, hamate teeth ( Figs. 9 B–C); reproductive system with a flattened, granular prostate, having two well differentiated regions ( Fig. 10 A); vestibular or accessory glands absent ( Fig. 10 A) (Valdés, 2002). Valdés (2002) pointed in the diagnostic features of the genus Discodoris that the penis devoid hooks, while we find hooks on the penis of D. branneri . Still we place this species into Discodoris .

The oldest valid Discodoris from Brazil is Discodoris branneri . The latter was described based on a single specimen, without data on external morphology and coloration in vivo, resulting in inconclusive evidence of possible intraspecific variation. This led some authors to describe new species from Brazil and the Caribbean Sea, without appropriate comparison with D. branneri .

For example, Er. Marcus (1955) described Discodoris evelinae and distinguished this species from Discodoris branneri based on differences in the size of the nidamedal complex and prostate gland, yet he emphasized that these differences could be due to changes related to the successive stages of male and female maturation. MacFarland (1909) also noted that in D. branneri , the diminutive size of the complex nidamedal gland could be related to the reproductive period. Er. Marcus (1955) considered D. evelinae to be highly similar to D. branneri , particularly in the penial hooks, cylindrical-conical tubercles on the dorsum, and shape and number of rows of radular teeth; however, he separated the two species because he thought it was difficult to judge the differences in the size of the female gland and prostate. Dayrat (2010) considered Discodoris evelinae Er. Marcus, 1955 to be a junior synonym of D. branneri . According to him, the best diagnostic feature is the penis, which is similar in both descriptions. Indeed, both reproductive systems are compatible, despite small differences.

We observed that one specimen measuring 43.0 mm in length, from the type locality of D. branneri , has a small female gland similar to the specimen studied by MacFarland (1909), which was 55.0 mm long. Er. Marcus (1955), on the other hand, examined specimens of 100.0 mm in length. Additional specimens from Alagoas state were examined, and these showed a correlation between the size of the female gland and body length. Thus, we conclude that differences between the two species are due to sexual maturation, and agree with the synonymy introduced by Dayrat (2010).

Discodoris hedgpethi Ev. Marcus & Er. Marcus, 1960, a species described from the Gulf of Mexico, was distinct from D. evelinae with respect to the number of teeth per row of the radula. Ev. Marcus (1971) studied one specimen from Puerto Rico that presents an intermediate number of teeth per row, so the author established the synonymy between species. Ev. Marcus and Er. Marcus (1960, fig. 9) described a denticle in the innermost lateral tooth in Discodoris hedgpethi , but their drawing of the denticle is not clear, so it is difficult to evaluate the true state of the innermost lateral tooth. We would like to emphasize that the presence of a denticle on the cusp of the innermost lateral tooth of Discodoris hedgpethi has never been reported for D. branneri (or D. evelinae ), and, in line with this, the feature was not observed in D. branneri specimens studied in this work. A second difference may relate to the penis of D. hedgpethi . Dayrat (2010: 239, fig. 243) described the penises of two syntypes of D. hedgpethi as presenting several large penial hooks on the anterior portion; however, the micrographs of the penises do not show where the more prominent spine is, and Ev. Marcus and Er. Marcus (1960) did not describe the anterior portion of the penis. The penis in the six specimens dissected in the present study is slightly different, in that it only has one penial hook that is more evident than the others penial hooks in the anterior part of the penis ( Figs. 9 F–G). These two differences are difficult to evaluate without analyzing the syntypes or other specimens from the type locality, thus we believe that the two species cannot be distinguished on the basis of these features. However, we would like to emphasize these differences for further studies.

As a result of a revision of the basal discodorids, Dayrat (2010) concluded that this taxon was part of a metaphyletic group at the base of the Discodorididae , which could not be diagnosed because its members present all plesiomorphic characteristics associated with Discodorididae . He named this taxon as " Montereina " branneri or Discodorididae branneri , as an attempt to follow simultaneously the International Code of Zoological Nomenclature (ICZN, 1999) and International Code of Phylogenetic Nomenclature (Cantino & de Queiroz, 2010). Since the phylogeny of this family is not well established, we prefer to use a conservative approach.

Examination of several specimens, including those from the type locality, indicated that, despite large intraspecific variation in coloration, the rounded dark-brown blotches (sometimes almost black) on the dorsum are always present ( Fig. 1 D). In most cases, however, these blotches are distributed along the sides of the mantle. Valdés et al. (2006: 174) is considered only “in part” in the synonymic list because of this color characteristic: the picture that shows the light specimen from Martinique does not represent Discodoris branneri . In addition, ventral spots are always present, and these are smaller and present at a higher density on the foot than in the ventral part of the mantle.

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 9. Discodoris branneri, SEM photographs; A, labial cuticle; B, inner lateral teeth; C, marginal teeth; D – E, tubercles of the dorsum; F – I, penis; G, detail of the apical and more developed spine of the penis; H, detail of the spines in the middle of the penis; I. smooth portion of the penis. A – C (MNRJ 13172); D (MNRJ 10669); E (MNRJ 12942); F (MNRJ 13199); G – I (MNRJ 10662).

FIGURE 10. Discodoris branneri; A, general view of reproductive system (MNRJ 14934); B, purple egg mass deposited inside the aquarium (MNRJ 15001); C, usual egg mass white (MNRJ 14922). Abbreviations: am, ampulla; bc, bursa copulatrix; dd, deferent duct; f, female glands; ov, oviduct; pr, prostate; s, seminal receptacle; u, uterine duct; va, vagina.