Aplysia (Aplysia) nigra d'Orbigny 1837

Aplysia (Aplysia) nigra d’Orbigny, 1837 (Figs. 3–17) Aplysia nigra d’Orbigny, 1837: 209–210, pl. 18, figs. 1–2; Alamo & Valdivieso 1997: 84; Nakamura, 2006: 79; Uribe et al. 2013a: 47. ? Aplysia rangiana d’Orbigny, 1837: 210–211, pl. 17, figs. 11–13. Tethys nigra — Pilsbry, 1895: 85, pl. 22, figs. 10–11. ? Tethys rangiana — Pilsbry, 1895: 86, pl. 19, figs. 34–36. Aplysia (Aplysia) nigra — Eales, 1960: 369, text-figs. 46b, c, f; Paredes et al. 1999b: 31; Ramírez et al. 2003: 264. Type material. Probably lost, not found at MNHN, Paris (Engel & Eales 1957, Valdés & Héros 1998), nor at the NHMUK (A. Salvador pers. comm.) Neotype designation. In accordance with the International Code of Zoological Nomenclature (ICZN 1999, Art. 75.3), specimen IMARPE 04-001904 collected close to the type locality in San Lorenzo Island, Callao, Peru, on 21 July 2016 by Patricia Carbajal is here designated as neotype of Aplysia (Aplysia) nigra for the purpose of clarifying the status of the species (ICZN, Art. 75.3.1). The characters differentiating A. nigra from other species of the subgenus Aplysia are included in the anatomical redescription below (ICZN Art. 75.3.2), that ensures recognition of the selected neotype (ICZN Art. 75.3.3). Although a type specimen for A. nigra was not designated by d’Orbigny (1837), the relevant material was likely deposited at MNHN, but neither Engel & Eales (1957) nor Valdés & Héros (1998) found it, suggesting it is probably lost. Keen (1966) included this species in a list of types of d’Orbigny’s South American Collection deposited at NHMUK although she did not search for it. As no type material of A. nigra has been found in the NHMUK (A. Salvador pers. comm.) nor in the MNHN (Valdés & Héros 1998), no extant specimen can be connected to the original description (ICZN Art. 75.3.4). The specimen designated as neotype was selected to ensure consistency with the original description (ICZN Art. 75.3.5) and type locality (ICZN Art. 75.3.6). The specimen is part of the Colección Científica of the Instituto del Mar del Perú, one of the largest collections of marine specimens in Peru, with proper facilities for preserving the specimen (ICZN Art. 75.3.7). Type locality. San Lorenzo Island, Callao, Peru (d’Orbigny 1837). Material examined. PERU, Ancash: Chimbote (Isla Blanca), 2 specimens 105–113 mm length, 3.XI.2008, S. Castañeda col. (IMARPE 04-001903). PERU, Lima: Ancón, 1 specimen 181 mm length, 9.X.1977, C. Paredes col. (LaBSIM 15.06-0002.2), 1 specimen 75 mm length, 2017, O. Machuca col. (LaBSIM 15.06-0019), 1 specimen 85 mm length, 2. VI.2017 (LaBSIM 15.06-0020.2), 3 specimens 76–114 mm length; 2.VII.2017, F. Cardoso col. (LaBSIM 15.06-0023.1-3), 1 specimen 155 mm length; 19.XI.2017, P. Guardales and J. Leandro cols. (LaBSIM 15.06-0027.4), 1 specimen 196 mm length, 30.III.2018, A. Mendivil col. (LaBSIM 15.06-0035). PERU, Callao: San Lorenzo Island, 1 specimen 183 mm length, 21.VII.2016, P. Carbajal col. (IMARPE 04-001904). PERU, Lima: Chorrillos (Agua Dulce), 1 dry shell 70 mm length, 15.I.2018, A. Mendivil col.(LaBSIM 15.06-0033). PERU, Lima: Pucusana, 2 specimens 231–236 mm length, 16.XII.2017, A. Mendivil and A. Bravo cols. (LaBSIM 15.06- 0029.4-5), 2 specimens 211–246 mm length, 6.I.2018, A. Mendivil col. (LaBSIM 15.06-0030.3-4). PERU, Ica: Laguna Grande, 1 specimen 131 mm length, 24.XI.1998 (LaBSIM 15.06-0043.2). Description External morphology. Size ~ 300 mm in length. Color uniform deep purplish black, sometimes with fine white dots (Fig. 3). Body tough, robust, oval, flattened, narrowing gradually towards cephalic region (Fig. 4A). Cephalic tentacles short, thick, enrolled, with narrower bases, forming oral veil (Fig. 4A: tc). Oral lobes located on ventral surface of oral veil (Figs. 4B–C: lo). Rhinophores conical, thick, wide apart, with distal slit (Figs. 4A–B: ri). Foot sole wide, thick, with pair of lobes poorly differentiated in propodium, with very wide and rounded metapodium not developed in pedal sucker (Fig. 4C: mt). Parapodia relatively narrow, rigid, fused posteriorly, joined anteriorly with lobes slightly developed in anterior margin of parapodia (Figs. 4A–B: lpa). Visceral hump relatively large, oval, flattened, poorly differentiated, occupying more than 1/3 of body length (Fig. 4A). Mantle foramen small, oval, flattened, located near center of mantle (Figs. 4A: ma, 5A: arrow, 5D: arrow). Anal siphon relatively wide, very short, flattened, occupying ~1/4 of mantle length, enclosed within the reduced parapodial cavity (Fig. 6). Opaline gland simple, multiporous, with many very small openings occupying relatively large area on pallial cavity floor (Figs. 4A: oa, 5B–C: arrow, 5E–F: arrow). Opaline gland secretion milky white. Ink gland secretion white, scarce. Shell. Relatively large, shell length more than 1/3 of body length, width/length ratio about 2:3, slightly arched, oval to suboval, relatively narrow, wider close to anal sinus; on apertural view left margin slightly convex; right margin slightly convex or almost straight, narrowing abruptly towards apex; anal sinus wide, shallow and usually straight, sometimes slightly concave (Fig. 7). Protoconch in apex of calcified layer. Sculpture formed by very fine concentric lines. Haemocoel organs. Pericardium in anterodorsal portion of mantle, occupying ~1/10 of haemocoel volume. Buccal mass located anteriorly, occupying ~1/10 of haemocoel volume (Fig. 8). Penial sheath on right side of buccal mass, occupying ~1/10 of haemocoel volume. Nerve ring located posteriorly to buccal mass. Crop and gizzard located between buccal mass and visceral mass, together occupying ~1/6 of haemocoel volume (Fig. 8). Visceral mass in posterior portion of body, with digestive gland and intestine together occupying ~1/3 of haemocoel volume (Fig. 8). Hermaphrodite reproductive system on right side of visceral mass, occupying ~1/5 of haemocoel volume. Circulatory and excretory systems. Pericardium wider than long, about 1/3 of mantle length. Heart occupying most part of pericardial cavity. Auricle funnel-like, translucent, with delicate thin wall covered internally by interlacing strands of fibrous tissue (Figs. 9A–B: au). Ventricle smaller than auricle, opaque, with thick muscular wall covered internally by many longitudinal and transversal folds (Fig. 9B: ve). Connection between auricle and ventricle marked by auricle-ventricular valves, a pair of internal concentric flaps, width about half of ventricle width (Fig. 9B: av). Aortic crest about half of ventricle volume, flattened, with spongy wall covered internally by longitudinal folds (Figs. 9A–B: ao). Semilunar valve located at the entrance of ventricle to aortic crest, a semiconcentric dorsal flap, width about a third of aortic crest width (Fig. 9B: sv). Three major arterial vessels: (1) anterior aorta, irrigating reproductive system, nervous system, buccal mass and opaline gland; (2) gastric aorta, irrigating crop and gizzard; (3) posterior aorta, irrigating digestive gland and intestine. Kidney flattened, spongy walled, located on posterodorsal side of pericardium, occupying about same volume as aortic crest. Reno-pericardial duct not observed. Nephrostome located on bottom of pallial cavity, near base of gill. Digestive system. Oral tube short and muscular. Buccal mass piriform. Jaws thick, with longitudinal ridges well-developed, ~3 times wider than long, anterior and posterior borders strongly irregular (Figs. 10A, 13D), with elongated jaw elements, moderately curved toward distal end, tip thick, slitted (Figs. 10B–D). Dorsal surface of oral cavity with well-developed pair of dorsal folds (Figs. 10E: arrow, 13D: df), with dense elongated palatal elements, curved toward the distal end, tip with margin thickened (Figs. 10F–G). Odontophore spherical, occupying more than half of buccal mass volume. Odontophore muscles: mj, jaw and peribuccal muscles, originating on both sides of odontophore cartilages, extending along the buccal cavity, working as odontophore protractors (Figs. 11A–C); mc, buccal sphincter and circular muscles, well developed (Fig. 11G); m1d, pair of narrow jugal muscles, flattened, originating on anterodorsal surface of buccal mass, close to the median line, running dorsally, inserting on lateral surface of body (Figs. 11A, 11C); m1x, pair of auxiliary jugal muscles, ~8 times longer than wide, originating on anterodorsal surface of buccal mass posterior to m1d, running laterally, inserting on dorsal surface of body (Figs. 11A, 11C); m2, pair of strong retractor muscles of buccal mass, relatively thick, ~12 times longer than wide, originating on lateral side of odontophore, running posteriorly and inserting ventrally on dorsal portion of foot, near collumelar muscle (Figs. 11 A-F); m3, transversely thin muscle, wider than long, covering dorsally m4 (Figs. 11 B-C); m4, main pair of dorsal tensor muscles of radula, very thick and broad, originating on lateral region of odontophore cartilages, occupying most part of odontophore volume, inserting on ventral portion of subradular membrane and radular sac (Figs. 11 D-F); m5, pair of dorsal auxiliary tensor muscles of radula, ~4 times longer than wide, originating on lateral side of odontophore, running posteriorly and inserting on ventral side of subradular membrane, around radular sac (Figs. 11 D-F); m6, unpaired horizontal muscle, thin and narrow, connecting left and right odontophore cartilages (Fig. 11H); m7, pair of narrow and thin muscles, ~10 times longer than wide, originating on posterior region of odontophore cartilages and inserting on radular sac (Fig. 11H); m9, unpaired horizontal muscle, originating on posterior portion of m4, connecting pair of m4 (Fig. 11E); m10d, pair of dorsal protractor muscles of buccal mass, ~15 times longer than wide, originating on dorsal surface of odontophore, inserting on dorsal region of oral tube (Figs. 11A, 11C); m10v, pair of ventral protractor muscles of buccal mass, ~10 times longer than wide, originating on ventral surface of odontophore, inserting on ventral region of oral tube (Figs. 11A, 11C); m11, pair of ventral tensor muscles of radula, originating on ventral region of odontophore cartilages, running anteriorly, inserting on ventral side of subradular membrane (Fig. 11G). Pair of odontophore cartilages not delimited by a membrane, forming radular bolsters broad and flattened (Fig. 11H: oc). Radula longer than wide, yellowish; formula 42 x 1.21.1.21.1 (specimen length: 91 mm, LaBSIM 15.06-0023.2), to 111 x 2.59.1.59.2 (specimen length: 198 mm, LaBSIM 15.06-0035). Rachidian tooth bilaterally symmetrical, wider on base, with robust, triangular central cusp lacking denticles, 1 small lateral cusp on each side of central cusp, lacking secondary cusps (Fig. 12: black arrow). Lateral teeth asymmetrical, elongated, with large and triangular main cusp usually poorly serrated, 1 small secondary cusp distally (Fig. 12: white arrow). Marginal teeth small, with vestigial cusp. Pair of salivary glands ducts thick, flattened, wider in their median portion (Figs. 13A–B, 14H: sg). Esophagus with thick wall covered internally by longitudinal folds narrow and tall (Figs. 13A–B: es). Crop with thin wall covered internally by transverse and longitudinal folds broad and tall; subdivided in two chambers by a transverse girdle of circular fibers, anterior chamber larger than posterior chamber (Figs. 13A–B). Gizzard with thick wall, about 1/3 of crop volume (Fig. 13A: gz); presenting 10–11 large, pyramidal chitinous plates of rhombic base, distributed in 3 transverse rows occupying posterior region of gizzard (Figs. 13B, 14A–D); presenting ~50 small, conical chitinous plates of oval to circular base, distributed in several irregular rows occupying anterior region of gizzard (Figs. 13B, 14E–F). Filter chamber with thin wall, occupying half of gizzard volume (Fig. 13A: fc); presenting many small, conical gastric hooks of circular to oval base, distributed in many irregular transverse rows that cover almost entire surface of filter chamber (Figs. 13B, 14A, 14G). Stomach with thin wall, smaller than filter chamber; with pair of low gastric folds running longitudinally on lateral wall (Fig. 13B: gf). Digestive caecum with thin wall, about 1/3 of stomach width; running embedded within digestive gland along most of its length, tip coiled on right surface of digestive gland (Figs. 13A, 13C, 14I: ca); typhlosole extending internally along entire length of caecum, continuing into intestine for about half of stomach length (Fig. 13B: ty). Intestine with thin wall, convoluted, about 2/3 of caecum width, running 1 1/2 whorls around digestive gland, continuing posteriorly to gonad (Fig. 13C). Rectum passing through dorsal surface of haemocoel, leading to anus. Reproductive system. Penial sheath well differentiated into proximal penial canal and distal penial sac (Fig. 15A). Penial canal elongated, with muscular, thick wall, highly folded (Figs. 15B–C: pl). Penial sac bulbous, with thin wall, covered by small spiny warts slightly elevated, clustered in many longitudinal rows on opposite side to seminal groove (Figs. 15B–D, 16A: ws). Penis thick, spatulated, ~7 times longer than wide; covered by small spiny warts clustered in 3–4 longitudinal rows located in its proximal portion on opposite side to seminal groove, occupying ~1/4 of penis length (Figs. 15B–C, 16B: wp); with bilobed asymmetrical tip (Fig. 15E), seminal groove ending in shorter and rounded lobe, opposite lobe triangular (Figs. 15B–C). Pair of retractor muscles of penis thick, ~8 times longer than wide (Fig. 15A: mr). Protractor muscles of penis formed by many thin fibers (Fig. 15A: mp). Hermaphrodite reproductive system monaulic. Gonad embedded in posterior portion of visceral mass, yellowish, ~2 times wider than long. Preampullary duct relatively narrow, widening approaching ampulla, slightly curved. Ampulla thick, strongly convoluted, leading to a narrow postampullary duct (Fig. 15F: am). Nidamental gland oval, smaller than gonad, divided in three distinct glands: (1) albumen gland, (2) membrane gland, and (3) mucous gland. Large hermaphroditic duct wide, flattened, straight, ~3 times wider than ampulla, strongly attached to dorsal inner surface of haemocoel (Fig. 15F: lh). Seminal receptacle elongated, slightly wider at blind distal end. Bursa copulatrix spherical, with very thin wall, strongly attached to dorsal inner surface of haemocoel. Nervous system. Circumesophageal nerve ring made up of eight ganglia arranged in symmetrical pairs. Cerebral ganglia fused forming single mass, width about same pedal ganglion width (Figs. 17A–B: cg). Nerves leaving cerebral ganglia (Fig. 17E): c1, thick, branched, running anteriorly, inserting into dorsal wall of mouth; c2, bifurcating into 2 branches: c2a, inserting into cephalic tentacles, c2b, thicker than c2a, inserting into peribuccal region; c3, slender, running anteriorly, inserting into ventral wall of mouth; c4, thick, branched, inserting into rhinophores, giving off branch anastomosing with pedal nerve pd3; c5, thin, unbranched, inserting into eyes; c6, very slender, innervating statocyst. Cerebrobuccal connectives thick, longer than nerve ring length (Figs. 17A–B: ccb). Buccal ganglia oval, smaller than cerebral ganglia, joined by short commissure (Figs. 17A–B: bg). Nerves leaving buccal ganglia (Fig. 17C): b1, radular nerve, short, thick, inserting into ventral surface of radular sac; b2, thick, branched, anteriorly inserting into oral cavity and esophagus, posteriorly inserting into crop and gizzard; b3, very slender, inserting into salivary glands ducts; b4, slender, inserting into odontophore muscles, including retractor muscles of buccal mass; b5, slender, inserting laterally into odontophore; b6, slender, inserting dorsally into oral cavity. Cerebropedal connectives longer and thicker than cerebro-pleural connectives (Figs. 17A–B: cpd). Pedal ganglia oval, largest ganglia on nerve ring (Figs. 17A–B: pdg). Pedal commissure thick. Parapedal commissure thin, longer than pedal commissure. Nerves leaving pedal ganglia (Fig. 17D): pd1, slender, branched, running anteriorly, inserting into anterior portion of foot; pd2, very slender, branched, inserting into lateral anterior wall of haemocoel, on right side innerving retractor and protractor muscles of penis; pd3, very slender, anastomoses with cerebral nerve c4; pd4, slender, inserting into lateral anterior wall of haemocoel close to anterior origin of parapodia; pd5, slender, bifurcating into 3 branches: pd5a, branched, running posteriorly to mantle region, on right side anterior branch anastomoses with abdominal nerve a1 forming anterior opaline nerve (o1), also on right side posterior branch anastomoses with abdominal nerve a6 forming posterior opaline nerve (o2); pd5b, inserting into lateral anterior body; pd5c, anastomoses with pleural nerve pl1; pd6, slender, branched, inserting into anterior portion of parapodia; pd7, slender, running posteriorly, inserting into median portion of parapodia; pd8, thick, branched, inserting into median portion of foot; pd9, thick, inserting into posterior portion of foot and parapodia; pd10, very slender, unpaired, arising from parapedal commissure, running posteriorly, inserting into posterior region of foot. Cerebropleural connectives asymmetric, right connective longer than the left one, almost twice its length (Figs. 17A–B: ccl). Pleuropedal connectives short (Figs. 17A–B: clp). Pleural ganglia slightly asymmetric, left ganglion larger than right ganglion (Figs. 17A–B: plg). Nerves leaving pleural ganglia (Fig. 17D): pl1, slender, anastomoses with pedal nerve pd5c, inserting into dorsal wall of haemocoel; pl2, slender, only found on left side, running posteriorly, inserting into mantle region. Pleurovisceral connectives ~2 times longer than nerve ring length (Figs. 17A–B). Abdominal ganglia formed by two hemiganglia, with bulge on anterior end of each hemiganglion which represents reduced parietal ganglia (Figs. 17A–B: ag). Nerves leaving abdominal ganglia (Fig. 17F): a1, slender, inserting into mantle region, small branch anastomoses with pedal nerve pd5a forming anterior opaline nerve (o1); a2, thick, innerving osphradium and gill; a3, very slender, innerving bursa copulatrix; a4, inserting into pericardium; a5, slender, giving rise to genital ganglia, innerving hermaphrodite reproductive system; a6, slender, inserting into region around anal siphon, small branch anastomoses with pedal nerve pd5a forming posterior opaline nerve (o2). Geographic distribution. Máncora, Piura (4°S) to Laguna Grande, Ica (14°S), Peru. Habitat and ecology. Sandy bays, rocky blocks and rocky shores with algae; intertidal to subtidal. Mass mortality events relatively uncommon on sandy beaches. Remarks. D’Orbigny (1837) described A. nigra as a large animal, deeply black; with short parapodia posteriorly fused; and anal siphon short and flattened (Fig. 1C). The specimens examined in this work are consistent with the original description of A. nigra, although d’Orbigny (1837) stated the interior of parapodia could be a little pink, which we have not observed. Engel & Eales (1957) examined a specimen from Australia identified as A. nigra, finding it very similar to A. juliana, raising the question if A. nigra could be considered a melanic variety of A. juliana. Unfortunately, as they did not get access to Peruvian material of A. nigra, they could not recognize that the most notable difference between A. nigra and A. juliana is the development of parapodia; since in A. nigra they are rigid and narrow forming a reduced parapodial cavity (Fig. 3), whereas in A. juliana they are more widely open (Quoy & Gaimard 1832, Engel & Eales 1957, Eales 1960). Eales (1960) listed the southwest Pacific species Aplysia hyalina Sowerby II, 1869, Aplysia brunnea Hutton, 1875 and Aplysia hamiltoni Kirk, 1882 as junior synonyms of A. nigra, extending the range of the species from Peru to Australia, New Zealand and Brazil. Sowerby II (1869) introduced the name A. hyalina based on a dry shell from Port Jackson, Australia with the typical shape of the subgenus Aplysia. Allan (1932, 1941) described the living animals as large and black. Although Engel & Eales (1957) considered A. hyalina as a synonym of A. juliana, later Eales (1960) included it in the synonymy of A. nigra due to the color of the living animals. Bebbington (1977: fig. 14c) reported A. nigra for Australia, however the preserved specimens were described as having a pedal sucker and wide parapodia, more similar to A. juliana than to A. nigra. Nimbs et al. (2017a) concluded that the reports of A. nigra from eastern Australia are most likely to be A. juliana. Both A. brunnea and A. hamiltoni were described from dry shells from New Zealand. Suter (1913) considered both names conspecific and described the living animals as dark brown with fine irregular dark markings, with a shell very similar to that of A. hyalina. Engel & Eales (1957) included A. brunnea and A. hamiltoni as junior synonyms of A. juliana, but later Eales (1960) considered them as A. nigra, describing preserved specimens from New Zealand as having a lower fusion of the parapodia posteriorly and mantle foramen reduced to a small papilla, features not observed in A. nigra. After revising the Anaspidea from New Zealand, Willan (1979) concluded that A. nigra should probably be restricted to South America, since A. brunnea and A. hamiltoni are synonyms of A. juliana. Rudman (2003) also considered that the animals identified as A. brunnea or A. nigra brunnea in New Zealand should be considered A. juliana. This conclusion was followed by Nimbs et al. (2017a). Eales (1960) extended the range of