History and Revised Classification of the Order Cyclomyaria (Tunicata, Thaliacea, Doliolida)
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I I BULLETIN DE L'INSTITUT ROYAL DES SCIENCES NATURELLES DE BELG IQUE, BIOLOG IE, 73: 191-222, 2003 BULLETIN VAN HET KONINKLIJK BELGISCH INSTITUUT VOOR NATUURWETENSCHAPPEN, BIOLOGIE, 73: 191 -222, 2003 History and revised classification of the order Cyclomyaria (Tunicata, Thaliacea, Doliolida) by Jean E.A. GODEAUX Abstract The genus Doliolum, with the species Doliolum mediter raneum, was created in 1823 by A.W. OTTO who described a The history of the successive investi gations done on the Order ban·el-shaped structure inhabited by a female amphipod of Doliolida is summarized and a revised classification of the Order is the genus Phronima. That "species " and those created later presented including all the species belonging or not to the fa mily ( 1830) by DELLE CHIAJE (D. papillosum and D. sulcatum) do Doliolidae. New fami lies are defined. Geographical distribution of not exist, as they onl y represent artefacts made by a crusta the species is given. cean parasiting a colony of Pyrosoma (P atlanticum?). Key-words: Fami lies Doliolidae, Doliopsoidae, Doliopsidae, QUOY & GAIMARD (Astrolable Expedition 1826-1 829) Paradoli opsidae, Doliopsoidesatlanticwn, Doliopsisbahamensis named Doliolum denticulum a kind of barrel ("barrilet nov. sp., Paradoliopsis harbisoni. denticule") first observed in Amboina roads (Indonesia) ( 1835, pl. 89, fig. 25-26) and later on off Vanikoro Island (Melanesia), and described as "Doliolum co1pore minima, Resume hyalino, cylindrico-ovato, subtruncato in Lttroque apice pelforato, antice crenulata, circulis octonis salientibus" L' hi storique des recherches successi ves menees sur I 'Ordre des Doliolida est presente avec une revision de sa classificati on incor (Length : 4.5 mm). The authors also emphasized the presence porant toutes les especes appartenant ou non a Ia famille des of a dorsal vessel (in fact the ventral endostyle), of the heart Doli olidae. De nouvelles families ant ete introduites. La distribu and of a gill composed of two sheets. The eight salient rings tion geographique des especes est presentee. represent eight muscle hoops and expose the blastozooid. The description of the animal is correct, and genus and spe Mots-clefs: Families Dolioli dae, Doliopsoidae, Doliopsidae, cies (now named Doliolum denticulatum QUOY & GAIMARD Paradoli opsidae, Doliopsoidesatlanticum, Doliopsisbahamensis nov. sp., Paradoliopsis harbisoni. 1835 after HUXLEY 185 1b ) are still accepted (Fig.! a) . From Amboina roads QUOY & GAIMARD named Doliolum caudatwn ("barri let a queue") ~ second species "Doliolum, Historical introduction co1p ore cylindrico, elongato, octonis circulis cincto, postice caudato, oribus terminalis, length 18-22.5 mm" cylindrical, The phylum Tunicata LAMARCK 1816 is divided into three elongated, 4 to 5 times longer than the other species, bearing cl asses, the benthic Ascidiacea, and the pelagic Thaliacea eight circles (muscles ?) and a tail (1835, pl.89, fig. 29-30). and Appendicul aria. The class Thaliacea consists of three After scrutening the drawings and correction of the orienta Orders: Cyclomyaria, Pyrosomatida and Salpida, the affini tion of the body (Fig. ! b), that doliolid seems to be an ties of which are still disputed (GODEAUX 1998). oozooid deprived of its viscera= nurse (the "ventral tail" be The Order Cyclomyaria CLAUS 1862 (Doli olida DELAGE & ing the dorsal spur); one may suggest that it belongs to the HEROUARD 1898) is the last Thaliacean order to be identi genus Dolioletta. QUOY & GAIMARD (loc.cit.) also stressed fi ed, probably owing to the tiny size and the transparency the relationshi ps between Doliolum and salps. (thinness) of the tissues of the animals. Up to now, that order Descriptions of the doliolid anatomy and of the life cycle comprises the single family Doliolidae (BRONN 186 1) the were initiated by HUXLEY ( l85 lb) and especially by KROHN systemati cs of which were established by GA RSTANG in his ( 1852) who gave the first correct position of the body of the classical memoir (1933). Although several genera and spe animals and recogni zed their relationshi ps with the cies have been descri bed since that ti me, no real attempt was Ascidiacea. He also observed both the tailed larva and the done to improve the systematics of the order until the paper gonozooid of Doliolum denticulatum and the oozooid and by GODEAUX ( 1996). the gonozooid of a new species named Doliolum muelleri. I I 192 JEAN E.A. GODEAUX zooids) and phorozooids, and the hermaphroditie sexual gonozooids; the dorsal spur (cadophore) of the oozooid is just an organ carrying on the developing buds. ULJANIN (1884) and NEUMANN (1906, 1913) also proved that the gonozooids are not budded by the phorozooids but that they represent a third generation of buds resulting of the strobili zation of a pro bud issued from the stolon of the oozooid and carried by the phorozooids. The phorozooid and gonozooid are fully similar as the sole difference is either the absence or the presence of the gonads. The same authors divided the ge nus Doliolwn into two subgenera, Doliolwn and Dolioletta. Therefore the life cycle of a doliolum is especially compli cated as the same species is represented by six successive stages: tadpole or larva (L), fullgrown oozooid (Ooz), degen erated (eviscerated) oozooid or nurse (N, Fig. 2 a), all three issued from the egg, and three blastozooids: trophozooid or gastrozooid (TZ), phorozooid (PZ) and gonozooid (GZ, Fig.2 b). That cycle has just been described in three species, Fig. 1. a. blastozooid of Doliolwn denticulum (now D. especially thanks to rearing of eggs and larvae (BRACONNOT denticulatum) after QUOY & GAIM ARD 1835. b. Doliolwn 1970 a,b). Moreover the oozooids and nurses of the different caudatum (nurse of Doliolella sp?, after QUOY & species of a genus are so similar that they cannot be separated GAIM ARD 1835). (cryptic species as suggested by GODEAUX 1961). The cur rent systematics (GARSTANG 1933) is based on the anatomi cal structure of the phorozooids and gonozooids and recog KROHN concluded in favor of a simple alternation of genera nizes four genera and some twenty species. tions (metagenesis) as already known in salps. Beside of the Doliolidae, several doliolum-Iike types have Further researches by GEGENBAUR (1855), KEFERSTEIN & been progressively discovered and described. EHLERS (1861), GROBBEN (1882), ULJANIN (1884) and In 1835, RATHKE, after papers left by ESCHSCHOLTZ, named NEUMANN (1906, 1913) progressively cleared up the com plexity of the life cycle of the doliolum: the sterile oozooid buds thanks to its ventral stolon three successive generations of blastozooids, namely the sterile .trophozooids (=gastro- Fig. 3. Doliopsis sp.: gonozooid (after BARROIS I 885, modified). Anchinia savign.iana a second type of Doliolid di scovered in the northern Atlantic Ocean ( 48° N-16° W). NEUMANN (1913b), after GEGENBAUR, GROBBEN and ULJANIN , consid ered that this species does not exist and is just a doliolum Fig. 2. Doliolina muelleri: a: oozooid, b: gonozooid. nurse with its dorsal spur. Later on a meditenanean species, - 1 II Systematics of Doliolida 193 considered as close to Anchinia, was successively named Hermaphroditism of the gonozooids. Doliopsis rubescens (VOGT, 1852, Fig.3) andAnchinia rubra (VOGT 1854, KOWALEVSKY & BARROIS 1883, BARROIS 1885). GROBBEN (1882) recognized two species: A. - Differentiation of the four types savigniana and A. rubra, while KROGER (1939) called Doliopsis savigniana specimens mainly collected in the The four types of Doliolids can be distributed into four fami southern Atlantic Ocean. Numerous specimens mainly li es thanks to diverse characters: length of the endostyle, caught in the Bahamas seem to belong to another species, shape of the digestive tube, number (5 , 8 or 9) and disposi Doliopsis bahamensis (GODEAUX, 1996). The relationship tion of the muscle hoops, position of the vibratile organ with with Doliolum has been early on suggested by HUXLEY regards to brain and M III, shape of the branchial septum, (l85la), VOGT (1852), GROBBEN (1882) and NEUM ANN number of gill slits, position of the gonads, shape of the testis ( 1913b). The life cycle of these animals remains practically (in gonozooid), presence of pigmented areas. unknown (see below). Metagenesis is probable, but only blastozooids have been described up to now. In 1939, KROGER described a third type of doliolid species Subdivisions of the Order Doliolida (Cyclomyaria) called Doliopsoides meteori and collected in the southern Atlantic Ocean, mostly below 400m depth. The barrel According to these different characters, a division of the or shaped body evokes that of the doliolum. Another species, der Doliolida in two suborders and four families is proposed: Doliopsoides horizoni has been described from the eastern tropical Pacific Ocean by TOKIOKA & BERNER (1958a,b). Suborder Doliolidina with two families: Doliopsoides atlanticum GODEAUX 1996 is a third species of the same genus from the north western Atlantic Ocean a) Doliolidae with four genera and about twenty species. (GODEAUX 1996, GODEAUX & HARBISON in press). Nothing is known about their life cycle, although metagenesis seems b) Doliopsoididae with one genus and three species. probable. In 1996, GODEAUX created the species Paradoliopsis The common characters are: barrel-shaped body, siphons at harbisoni (GODEAUX & HARB ISON in press) after two mature both ends of the main axis, thinness of the tunic, number of individuals and four developing buds still undescribed and the muscle hoops