Zoosyst. Evol. 94 (2) 2018, 237-246 | DOI! 10.3897/zse.94.14518 > PENSUFT. bi Neti ‘2? NATURKUNDE BERLIN Complementary anatomy of Actinocyclus verrucosus (Nudibranchia, Doridoidea, Actinocyclidae) from Indo-Pacific Patricia Oristanio V. Lima!, Luiz Ricardo L. Simone? 1 Museu de Zoologia da Universidade de Sdo Paulo 2 Postal address: Cx. Postal 42494: CEP 04299-970 Sdo Paulo, SP, Brazil http://zoobank. org/E3893503-97D3-419D-8B4E-592BC4C2B238 Corresponding author: Patricia Oristanio V. Lima (patylima84@gmail.com) Abstract Received 13 June 2017 Accepted 28 February 2018 Published 15 March 2018 The last review of the genus Actinocyclus consider only two valid species for the genus: Actinocyclus verrucosus Ehrenberg, 1831 (type species of the genus) and Actinocyclus papillatus (Bergh, 1878), both with a geographical distribution in the Indo-Pacific. The anatomy of these species is still unknown, except for some scanty anatomical informa- Academic editor: Matthias Glaubrecht tion. A detailed anatomical study of Actinocyclus verrucosus is performed, including in- edited structures such as digestive system, odontophore muscles and circulatory system, beyond complementary information on the commonly studied structures, in order to clar- Key Words Actinocyclidae Actinocyclus verrucosus comparative morphology systematics Indo-Pacific Introduction The family Actinocyclidae comprises two genera, Actino- cyclus Ehrenberg, 1831 [type species: Actinocyclus ver- rucosus Ehrenberg, 1831, by subsequent designation of Gray (1847)], with two valid species: the type species and A. papillatus (Bergh, 1878) (Rosenberg 2010); and Hal- laxa Eliot, 1909 with 15 valid species (Bouchet 2011). The current systematics of this family is mainly based on Gosliner and Johnson (1994) who studied the phylogenetic relationship of the WHallaxa, and hypothesized Actinocyclus as its sister taxa, considered only these two genera as members of Actinocyclidae, and this family as sister taxon of Chromodorididae (Valdés 2002). The last review of Actinocyclus was based on some traditional characters, such as the external morphology, the reproductive system and radular data (Valdés 2002). As have been seen in recent papers (e.g., DaCosta et al. 2007, Simone 2011, Lima and Simone 2015), the scenario of the morphological characters is an effective tool to ify the taxonomy and distribution. better understanding the relationship among species and has been useful to clarify and refine their taxonomy. In this paper the morphological data of Actinocyclus ver- rucosus are described in more details, including previously unexplored structures, such as digestive tubes, odontophore muscles and circulatory system, and builds a conceptual scenario for comparative characters in future analysis. Material and methods The studied material belongs to museum collections, con- sisting of specimens preserved in 70% ethanol; a complete information follows description. Dissections were per- formed under a stereomicroscope by standard techniques (Simone 2004, 2011). The initial steps of the anatomical investigation were done through a longitudinal cut on the integument covering the dorsal visceral mass. Digestive, circulatory, excretory, reproductive and central nervous systems were investigated in detail. The terminology used Copyright Patricia Oristanio V. Lima, Luiz Ricardo L. Simone. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 238 Lima, P O. V. & Simone, L. R .L.: Complementary anatomy of Actinocyclus verrucosus... for odontophore muscles was based on Ponder et al. (2008), Simone (2011) and Lima and Simone (2015). Drawings were done with the aid of a camera lucida. Scanning elec- tron microscopy (SEM) was used to examine details of the radula at the Laboratorio de Microscopia Eletrénica of Mu- seu de Zoologia da Universidade de Sao Paulo (MZSP). The following abbreviations are used herein: aa: an- terior aorta; ab: afferent branchial vein; am: ampulla; an: anus; ap: posterior aorta; au: auricle; at: aortic trunk; be: bursa copulatrix; bg: blood gland; bl: branchial leaves; bs: buccal sphincter; cb: buccal commissure; ce: cerebral ganglia; cl: pleural commissure; cp: pedal commissure; cu: caecum; dd: duct of digestive gland; dg: digestive gland; dt: digitiform tentacle; eb: efferent branchial vein; es: oesophagus; ey: eye; fg: female gland; ft: foot; gb: buc- cal ganglia; ge: gill circle; ge: gonopore; gg: gastro-oe- sophageal ganglia; gp: pedal ganglia; hg: hermaphrodite gland; il: inner lip; in: intestine; mo: mouth; ms: medial si- nus; m2 —m10: odontophore muscles; mt: oral tube mus- cle; ne: nephrostome; oc: odontophore cartilage; ol: outer lip; ot: oral tube; ov: oviduct; pe: pericardium; pe: penis; pl: pleural ganglia; pr: prostate; ra: radula; ri: rhino- phore; rg: rhinophoral ganglia; rm: gill retractor muscle; rn: rinophoral nerve; rp: reproductive system; rs: radular sac; rv: renal vesicle; sg: salivar gland: sm: subradular membrane; sn: nervous system; sr: seminal receptacle; st: stomach; sy: statocysts; tu: dorsal tubercles; ud: uterine duct; va: vagina; vd: vas deferent; ve: ventricle. Institutional abbreviation AUS Australian Museum Research Institute, Sydney CASIZ Invertebrate Zoology and Geology of the Cali- fornia Academy of Science, San Francisco MHUB- Museum fir Naturkunde der Humboldt-Uni- versitat zu Berlim ZMUC_ _ Zoologisk Museum, Kobenhavns Universitet, Copenhagen MNHN Muséum National d’ Histoire Naturalle, Paris Results Family Actinocyclidae O’ Donoghue, 1929 Genus Actinocyclus Ehrenberg, 1831 Type species. Actinocyclus verrucosus Ehrenberg, 1831, by subsequent designation of J. E. Gray (1847) Actinocyclus verrucosus Ehrenberg, 1831 Figs 1-31 Actinocyclus verrucosus Ehrenberg, 1831: 28. Sphaerodoris punctata Bergh, 1877: 66 (nomen nudum), Bergh 1878: 587, pl. 65, figs 1-5. Sphaerodoris laevis Bergh, 1890: 925, pl. 88, figs 3-12; Odhner 1919: 40. Sphaerodoris japonica Eliot, 1913: 23. Aldisa nhatrangensis Risbec, 1956: 14, pl. 20, fig. 109, pl. 22. zse.pensoft.net Type material. See Valdés (2002). Type locality. Massawa, Eritrea. Material examined. AUSTRALIA, Coral Sea, North East Herald Cay, AUS 333868.001, 2 specimens (M. Pre- ker, coll., 24/vi/1997, beach rock, SE side of cay, LT at dusk). VANUATU, Espiritu Santo Island, Palikulo Pen- insula (15°28.90’S 167°15.50’E (DDM)), CAS 179791, 1 specimen (M. Pola-Perez, Y. Camacho-Garcia et al. Coll., 15/ix/2006, intertidal, soft bottom). Diagnosis. Body of grayish color, with some black dots and some tubercles. Anterior border of foot concave and not bilabiate nor longitudinally notched. Presence of m7a odontophore muscles and pleural commissure. Redescription. External morphology (Figs 1-9): Size, ~12mm length, ~10mm width. Color grayish with some black dots in preserved specimen. Body rounded, oval, almost as long as wide; elevated dorsum with some sever- al simple dorsal tubercles scattered irregularly (Figs 1-3). Mantle smooth without spicules. Rhinophores with ~17 transverse lamellae (preserved specimen with ~12mm- long CASIZ 179791) (Figs 5-7); rhinophoral sheaths smooth. Gill circle composed of 16-19 unipinnate bran- chial leaves surrounding anus (preserved specimen with ~12mm-long) (Figs 8—9); branchial sheaths smooth. Mouth opening in anterior ventral region, between anter1- or region of notum and foot (Fig. 2). Digitiform tentacles very small, one on each side of mouth (Fig. 4). Anterior border of foot concave, not bilabiate, nor longitudinally notched (Fig. 4). Foot not exceeding notum in a preserved specimen (Fig. 2). Haemocoel organs (Figs 11—12): pericardium and pos- terior half of visceral mass occupying ~40 % of haemo- coel volume. Buccal mass located anteriorly, occupying ~20 % of haemocoel volume. Nervous system dorsal to buccal mass, covered by blood gland, occupying ~10 % of haemocoel volume. Genital system on right side; oc- cupying ~20 % of haemocoel volume. Stomach internal to digestive gland, intestine with small curve at anterior portion, both occupying ~10 % of haemocoel volume. Circulatory and excretory systems (Figs 8-11): peri- cardial cavity dorsal and posterior to digestive gland, anterior to gill circle. Afferent and efferent veins located at edge of each branchial leaves (Fig. 9). Gill retractor muscle divided in two fibers originating from base of gill circle, running lateral to haemocoel longitudinally up to half of foot level, inserting into dorsal surface of foot (Fig. 8). Auricle funnel-like (wider anteriorly) with thin walls (Fig. 10). Ventricle slightly taller than wide, with thick muscular walls (Fig. 10). Aortic trunk anterior to pericardium, connected to anterior ventricular region (Figs 10-11); posterior artery branched into anterior ar- tery irrigating reproductive system, buccal mass, odonto- phore and nervous system inserting on blood gland; ante- rior artery irrigating stomach, caecum and digestive gland Zoosyst. Evol. 94 (2) 2018, 237-246 239 Figures 1—4. External morphology of Actinocyclus verrucosus. 1. Whole dorsal view, scale: 5 mm. 2. Whole ventral view, scale: 5 mm. 3. Whole right lateral view, scale: 5 mm. 4. Detail of anterior border of foot, ventral view, scale: 2 mm. zse.pensoft.net 240 Lima, PR O. V.& Simone, L. R .L.: Complementary anatomy of Actinocyclus verrucosus... — ““. Te a Figures 5—12. Anatomical details of Actinocyclus verrucosus. 5. Rhinophore extracted, ventral view, scale: 0.5 mm. 6. Same dorsal view, scale: 0.5 mm. 7. Same, transverse section, scale: 0.5 mm. 8. Gill circle with retractor muscle, dorsal view, scale: 1 mm. 9. Detail of gill filament, scale: 1 mm. 10. Detail of circulatory system (structures of pericardium), ventral view, scale: 2 mm. 11. Ex- tracted visceral mass, dorsal view, scale: 2 mm. 12. Same, ventral view, scale: 2 mm. zse.pensoft.net Zoosyst. Evol. 94 (2) 2018, 237-246 241 14 7" Pian ot IT IT; ca ae | / | j ae re? i lg | O | | = - = wn = NG 4 / fay <= > |! | GU1He Raita \ Wh mat —_ Vg oF | =e re ax Figures 13—21. Actinocyclus verrucosus details of digestive system. 13. Foregut and nerve ring, ventral view, some adjacent struc- tures also shown as in situ, scale: 1 mm. 14. Same dorsal view, scale: 1 mm. 15. Same, longitudinally sectioned, showing internal oral tube, dorsal view, scale: 1 mm. 16-20. Odontophore anatomy, scales: 1 mm. 16. Whole ventral view, sphincter removed. 17. Whole dorsal view, esophagus removed. 18. Dorsal view, radula removed, each cartilage slightly deflected. 19. Whole right view. 20. Ventral view, m4 and m5 folded down to expose odontophore cartilage; m7 and m7a removed. 21. Midgut as in situ, dorsal view, scale: 2 mm. zse.pensoft.net 242 Lima, P O. V. & Simone, L. R .L.: Complementary anatomy of Actinocyclus verrucosus... gg Figures 22—27. Actinocyclus verrucosus reproductive system. 22. Dorsal whole view, most structures uncoiled, scale: 1 mm. 23. Same, ventral view, scale: 1 mm. 24. Detail of uncoiled female structures, dorsal view, scale: 1 mm. 25-27. Central nervous system. 25. Dor- sal view, scale: 1 mm. 26. Ventral view, scale: 1 mm. 27. Detail of buccal and gastroesophageal ganglia, ventral view, scale: 0.5 mm. zse.pensoft.net Zoosyst. Evol. 94 (2) 2018, 237-246 243 Table 1. Comparative table of some features between Actinocyclus verrucosus, Hallaxa apefae and Chromodoris magnifica (all these features of the three species was analyzed in Lima 2016). Anterior Ducts of Pedal border of foot Foot MEP HESS tenes pats ates digestive gland Pecan commissure Actinocyclus Concave, not Not projected Readil verrucOSsus bilabiate nor beyond the pirated Present | Present 3 Present Present Ehrenberg, 1831 notched notum Convex, Pointed, poserior : malaean Cae bilabiated not | projected beyond Nene y Absent | Absent Absent Absent Marcus, 1957 apparent notched the notum Chromodoris Convex, Pointed, poserior Readil magnifica (Quoy & | bilabiated not | projected beyond eee Absent | Absent Absent Absent Gaimard, 1832) notched the notum (Fig. 11). Auricular vessels connecting lateral cavities of integument to auricle (Fig. 10). Medial sinus connected to afferent branchial ring, irrigating entire digestive gland. Renal vesicle located on right dorsal side of pericardium, near base of auricle, connected to inner surface of peri- cardium; renal chamber elliptical, with longitudinal folds, ~1/4 of size of ventricle (Fig. 10). Renal chamber extend- ing from dorsal to medial sinus, previously connected to renal vesicle, extending posteriorly to center of gill circle and opening in nephrostome, next to anus pore (Fig. 8). Blood gland undivided (Fig. 11). Digestive system (Figs 8, 13-21, 28-31): Oral tube composed of outer lip, with pleats lengthwise; inner lip with transverse fold; mt, two pairs of retractor muscles of buccal mass, originating on oral tube, running dorsally and ventrally to oral tube, inserting on body side, about three times as wide and twice as long as m10 (Fig. 15). Odontophore oval, connected to oral tube by several fine longitudinal dorsal and ventrolateral protractors muscles of buccal sphincter, originating in anterior region of odon- tophore, inserting in posterior region of integument, close to oral tube (m10) (Fig. 14); Buccal sphincter surrounding chitinous part of oral tube. Odontophore muscles: m2, pair of strong retractor muscles of buccal mass, six times lon- ger than wide, originating on anterior dorsal odontophore, running laterally to m4 and inserting ventrally on dorsal portion of foot; m3, two times wider than long, transverse fibers between esophagus and odontophore (Figs 15-16); m4, pair of dorsal tensor muscles of radula, strong and broad, 1/2 winder than long, covering externally 2/3 of cartilage, inserting on ventral portion of subradular mem- brane; m5, pair of dorsal auxiliary tensor muscles of rad- ula, twice as long as wide, originating on most posterior region of odontophore cartilages, covering ~1/3 of poste- rior cavity of odontophore, as long as, but with ~1/3 of m4 width, inserting on ventral side of subradular membrane, around radular sac; m6, unpaired horizontal muscle, with transverse fibers connecting anterior surfaces of left and right odontophore cartilages, as long as wide, about same length and half as wide as m4 (Fig. 20); m7, pair of thin muscles originating each into an odontophore cartilages and inserting on m7a passing ventrally by m5, and on rad- ular sac (Fig. 19); m7a, originating on posterior region of odontophore cartilage and inserting on radular sac, m7’ auxiliary (Fig. 19). Pair of odontophore cartilages slen- der, elliptical. Subradular membrane thin, strong, translu- cent (Fig. 18). Radular sac ~1/6 of odontophore (Fig. 16). Jaw elements not analyzed. Radular teeth (Figs 28-31): rachidian teeth absent; formula 50 x 17.0.17 (preserved specimen, ~15 mm-long, AUS C333868001). Innermost lateral teeth broad and thick, with large and rounded cusp and about six to eight cusps along inner edge (Fig. 31). Mid-lateral teeth narrow basally and elongated, with api- cal cusp larger than other, twenty-one lateral cusps (Fig. 30). Outermost teeth shorter than middles laterals, about sixteen to eighteen cusps (Fig. 29). Pair of salivary glands long, tubular, about same length as esophagus; duct insert- ing in anterior region of esophagus, extending posteriorly to anterior region of digestive gland (Fig. 14). Esophagus simple, originating dorsally to odontophore, inserting directly in anterior region of stomach, internal longitu- dinal folds with same diameter along entire length (Figs 14-15). Stomach internal to digestive gland, oval, close to anterior region of intestine, with distinct digestive ducts (Fig. 21). Intestine with longitudinal folds along its entire length, diameter same as esophagus diameter. Caecum as an elongated sac, located ventrally to stomach, opening on anterior portion of stomach (Fig. 21), close to esophageal insertion, ~/2 length and ~1/2 of width of stomach. Diges- tive gland dark brown, internal to hermaphrodite gland, cone-shaped; inner face of gland sponge-like, bearing three ducts (Fig. 21). Anus opening into pore at center of gill circle (Fig. 8); anal papilla absent. Genital system (Figs 2, 11-12, 22—24): located between buccal mass and digestive gland, mainly on right and dor- sal sides. Hermaphrodite gland around digestive gland, dark beige in color (Figs 11-12). Hermaphrodite duct thin, long located posterior end of ampulla (Figs 22—23). Ampulla located on female gland, elongated and tubular, about same length as oviduct, inserting distally at junction of oviduct and prostate (Fig. 23). Prostate glandular, con- nected to female gland, ~1/2 of ampulla’s length. Vas def- erens and penis muscular, cylindrical, elongated, ~1/2 of prostate’s width (Fig. 22). Female gland well-developed, rounded, occupying ~40% of reproductive system vol- ume, about same length and twice width as oviduct (Figs 22-23). Oviduct occupying ~1/3 of female gland volume (Figs 22—23). Uterine duct located at base of bursa cop- zse.pensoft.net f >. Z ae Figures 28-31. Actinocyclus verrucosus, radula in SEM. 28. Panoramic view, scale: 100 um. 29. higher magnification in central region, scale: 40 um. 30. Outer lateral teeth, scale: 10 um. 31. Detail of marginal teeth tip, scale: 10 um. ulatrix and seminal receptacle, inserted in female gland near oviduct, relatively short, ~1/10 of vagina’s length and same diameter as vagina (Figs 22, 24). Seminal receptacle pyriform, as large as bursa copulatrix, connected to vagina near uterine duct through short stalk (Figs 22, 24). Bur- sa copulatrix rounded, connected to vagina after seminal receptacle, length ~1/6 of vagina’s length, also through stalk three times longer than uterine duct (Figs 22, 24). Vagina cylindrical, elongated, same width and four times longer than penis, followed ventrally by prostate and lo- cated parallel to penis on gonopore (Fig. 24). Gonopore on right side, located in anterior fifth of length of animal from head, between foot and notum (Fig. 2). Central nervous system (Figs 25—27): located dorsally to odontophore, mostly covered by blood gland. Pair of cerebral and pleural ganglia fused with each other dor- sally and ventrally. Pedal ganglia fused with cerebral and pleural ganglia ventrally, not fused among themselves, connected by long and thin pleural commissure. Pedal commissure simple, 2 of length of pleural commissure, both surrounding esophagus and salivary glands (Fig. 26). Buccal ganglia short, located ventrally to odontophore, between radular sac and anterior portion of esophagus, connected to cerebral ganglia through long and slender connective tissue, united to gastro-esophageal ganglia by short connective tissue. Gastro-esophageal ganglia with length ~1/4 of buccal ganglia length, spherical (Fig. 27). Rhinophoral ganglia bulb-shaped, connected to anterior portion of cerebral ganglia (Fig. 25). Dorsal eyes located on cerebral ganglia with short stalk, pedunculated. Sta- tocysts small and iridescent, located ventrally between pedal and pleural ganglia (Fig. 25). zse.pensoft.net Distribution. West and Central Indo Pacific [Red Sea (Ehrenberg 1831), Philippines, and Indonesia (Ber- gh 1878, 1890), East Africa, Malaysia and Japan (Eliot 1904, 1913), Vietnam (Ribesc 1956), Hawaii (Kay and Young 1969), Queensland (Willan and Coleman 1984), Western Australia (Wells and Bryce 1993), Madagascar and Marshall Island (Valdés 2002)]. Discussion The presence of a short pair of digitiform tentacles around the mouth (Fig. 4) 1s noteworthy, they were also reported by Gosliner and Johnson (1994). However, these digitiform tentacles have been reported as absent by Kay and Young (1969) and Valdés (2002). The most external differences of A. verrucosus, when compared to other Doridoidea, for example Hallaxa apefae, Chromodoris magnifica and Doris verrucosa (Tab. 1), is the presence of an anterior border of foot concave, not convex and not grooved, nor notched (Figs 2, 4). The rhinophores have 17 lamellae instead of 20 described by Valdés (2002), and the number of branchial leaves rang- es from 16 to 19, instead of only 16. Regarding the color of the body, no alive specimens have been analyzed. In the circulatory system, interesting features were found in the position in relation to gill circle, the affer- ent and efferent vessels, the gill retractor muscle, medial sinus, renal chamber and nephrostome. Despite some of these features have already used in phylogenetics ana- lyzes (Lima 2016), because of lack of further informa- tion, a deeper analysis is still difficult. Zoosyst. Evol. 94 (2) 2018, 237-246 The oral tube is composed of a pair of retractor muscles, which attaches to the body wall (mt), in_4. verrucosus there are two pairs of mt, while in Hallaxa apefae, and the most species of Doridoidea, present three pairs (Lima 2016). A buccal sphincter and the m3 (transverse muscle) involve the odontophore (Figs 15—16) that have a pair of long re- tractor muscles (m2) (Figs 15—17). A group of muscles are described for the first time (m4, m5, m6, m7) (Figs 16—20), with similar functions of their counterparts in other het- erobranchs (Simone 2011). The odontophore cartilage is well-developed (Fig. 18) like in other nudibranchs as, e.g., Doris verrucosa Linnaeus, 1758 (Lima and Simone 2015). However, some differences are visible between A. verru- cosus and D. verrucosa as following: m5 pair originates on the middle region of the odontophore cartilages in A. verrucosus (Figs 19-20) instead on the posterior region in D. verrucosa (Lima and Simone 2015, fig. 8B); m6 located more anteriorly in A. verrucosus (Fig. 20), whereas in D. verrucosa the m6 connects the both odontophore cartilag- es anteriorly and posteriorly (Lima and Simone 2015, Figs 8A-B). However, the most significant difference of odon- tophore muscles of A. verrucosus and others Doridoidea Species appears to be the presence of the pair m7a. The reproductive system seems to be similar to those de- scribed by Valdés (2002), but it has some different features from the interpretation by Kay and Young (1969) that de- scribed the prostate without the glandular portion, which was not observed in the present studied samples (Figs 23-24). In the central nervous system, the abdominal gangli- on described by Valdés (2002) was not observed, but a pleural commissure (Figs 25—26), that is not mentioned by him, was found. This last feature was uncovered as au- tapomorphy in a recent phylogenetic study (Lima 2016) as well as the presence of m7a — originating on posterior region of odontophore cartilage and inserting on radular sac, probably m7’s auxiliary. In the same recent phylogenetic study (Lima 2016) Hallaxa apefae appears more related to Chromodorididae (Tab. 1) clade and could be considered as sister group based on the posterior projection of the foot beyond the notum and the absence of integumentary spicules. In the same analysis, A. verrucosus resulted as sister group of a Clade that united Dorididae and Discodorididae with two characters: radula with many lateral teeth and buccal commissure readily visible. The present complementary anatomical investigation improved the species delimitation of A. verrucosus. In addition, allowed to evaluate the characters usually used in taxonomy and phylogenetic studies, as well as the dis- covery of new characters with phylogenetic signal and provided more bases for the synonymies. The evalua- tion of new morphological characters will improve the knowledge of the Actinocyclus evolutionary history, or even Doridoidea. 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