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(Decapoda), Euphausiacea, and Mysidacea (Crustacea): a Phylogenetic Interest

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(Decapoda), Euphausiacea, and Mysidacea (Crustacea): a Phylogenetic Interest Color profile: Disabled Composite Default screen 296 Carapace and mandibles ontogeny in the Dendrobranchiata (Decapoda), Euphausiacea, and Mysidacea (Crustacea): a phylogenetic interest Bernadette Casanova, Laetitia De Jong, and Xavier Moreau Abstract: The ontogeny of the carapace and the mandibles has been studied for one species of Dendrobranchiata (Decapoda), four species of Euphausiacea, and three species of Mysidacea (one species of Lophogastrida and two spe- cies of Mysida). The protocephalic origin of the carapace, which arises from the antennar tergite, is confirmed. During larval development the progressive dorsal insertion of the carapace leads to the opening of the tergites of both cephalic and thoracic segments. The opening of the eight thoracic segments (TS) occurs in Euphausiacea and Decapoda only, and is done in three steps (TS1; TS1–TS3 or TS1–TS4; TS1–TS8). In adult Mysidacea, the insertion of the carapace exhibits two levels of evolution (opening of TS1 in Gnathophausia species and of TS1–TS4 in the others). Thus, in the larvae of Euphausiacea and Decapoda, the most evolved taxa, the progressive insertion of the carapace corresponds to the carapace locations in the adults of the most ancient taxa, i.e., Mysidacea. The location of the internal musculature of the mandibles, which is known for certain to characterize the different parts of the arthropodial segment, and their development, shows that the gnathal part of each mandible is prolonged by a pleural part and half the residual tergite of the mandibular segment. Résumé : L’ontogénie de la carapace306 et des mandibules a été étudiée chez une espèce de décapode Dendrobranchiata, quatre espèces d’euphausiacés et trois espèces de mysidacés (un Lophogastrida et deux Mysida). L’origine protocépha- lique de la carapace, qui est issue du tergite antennaire, est confirmée. Au cours du développement larvaire, l’insertion dorsale progressive de la carapace entraîne l’ouverture des tergites céphaliques et thoraciques. L’ouverture des huit seg- ments thoraciques (TS) ne s’observe que chez les euphausiacés et les décapodes, où elle s’effectue en trois étapes (TS1; TS1–TS3 ou TS1–TS4; TS1–TS8). Chez les mysidacés adultes, l’insertion de la carapace montre deux niveaux d’évolution (ouverture de TS1 chez les espèces de Gnathophausia et de TS1–TS4 chez les autres). Ainsi, chez les lar- ves d’euphausiacés et de décapodes, taxons les plus évolués, l’insertion progressive de la carapace correspond à celles observées chez les adultes du taxon le plus ancien, i.e., celui des mysidacés. L’emplacement de la musculature interne des mandibles, qui définit de manière non équivoque les différentes parties du segment anthropodien, et leur développe- ment, montrent que la partie gnathale de chaque mandibule se prolonge par une partie pleurale et par la moitié du ter- gite résiduel du segment mandibulaire. Introduction Casanova etcies al. (Mysidacea, Euphausiacea, and Decapoda), the relations of the carapace with the eight thoracic segments are differ- In some adult specimens of Malacostraca it has previously ent. In the lower Lophogastrida, the primitive suborder of been demonstrated that the carapace has a protocephalic ori- the Mysidacea, the carapace covers all the segments, which, gin (Casanova 1987, 1991 and 1993). The podophthalmate nevertheless, remain free and distinct. In the other Lophogastrida Malacostraca (Stomatopoda, Mysidacea, Euphausiacea, Dendro- and the evolved suborder Mysida, the carapace is shorter; it branchiata (Decapoda)) are the sole crustaceans having a opens the thoracic segments 1–4, taking the place of the ter- segmented protocephalic area (Casanova 1993), which appears gites, which are pushed aside, the four other segments re- at the same time as the development of the stalked eyes. maining free and distinct. Finally, in adult Euphausiacea and This segmentation allows the formation of the carapace to be Decapoda, all the thoracic segments are open. In addition, understood. It appears that the carapace is formed by the de- the Lophogastrida are close to the ancestral stock from which velopment of the dorsal part (tergite) of the antennar seg- arise the Mysida, Euphausiacea, and Decapoda (Casanova et ment, which successively opens the cephalic tergites and, al. 1998; De Jong and Casanova 2001). The Euphausiacea depending on the taxon, a variable number of thoracic ones. and Decapoda, which constitute the superorder Eucarida, are Thus, in adult Malacostraca with a well-marked caridoid fa- considered as the most evolved crustaceans. The aim of this study was to describe the different steps Received 6 July 2001. Accepted 7 January 2002. Published of the setting of the carapace during larval development of on the NRC Research Press Web site at http://cjz.nrc.ca on 8 March 2002. Mysidacea, Euphausiacea, and Decapoda, and, hopefully, shed light on their phylogeny. The ontogeny of the mandi- B. Casanova, L. De Jong1 and X. Moreau. Equipe bles was also investigated because the mandibular segment d’Accueil n°2202 Biodiversité, Laboratoire de Biologie seems to be of phylogenetic interest. Indeed, it is the first animale (Plancton), Université de Provence, case 18, 3 place segment to be open by the time the carapace sets, and the Victor Hugo, 13331 Marseille CEDEX 3, France. mandibles are known to play a major role in the diversifica- 1Corresponding author (e-mail: [email protected]). tion of the Mandibulata (Arthropoda) (Manton 1977). Can. J. Zool. 80: 296–306 (2002) DOI: 10.1139/Z02-011 © 2002 NRC Canada J:\cjz\cjz80\cjz-02\Z02-011.vp Tuesday, March 05, 2002 9:54:33 AM Color profile: Disabled Composite Default screen Casanova et al. 297 Materials and methods setae and are located laterally and perpendicular to the sagittal plan of the larvae (Fig. 1c). The inner ramus (endopodite) is Materials transparent, since it is devoid of internal tissue. Larvae of the peneid decapod Penaeus indicus (H. Milne Edwards) were supplied by the Centre Océanologique de Zoea stages Bretagne in Brest, France. Larvae of the euphausiaceans At the first zoea stage the carapace is still rounded anteri- Nyctiphanes couchi Bell, 1853, Euphausia krohni Brandt, orly and extends forward to cover the ocular area and back- 1851, Nematoscelis megalops G.O. Sars, 1883, and Stylocheiron ward to cover the first two thoracic segments. These two abbreviatum G.O. Sars, 1883 were collected in the Gulf segments bear only appendages (Figs. 2a,2b). The posterior of Lion (Mediterranean Sea) by the RV Jean Charcot in suture on the carapace is observed at the level of the first March 1966. Larvae of the lophogastrid Gnathophausia zoea thoracic segment (Fig. 2b). The opening of the mouth is now Willemoës-Shum, 1873 and the mysids Praunus flexuosus effective and occurs between the inner fold of the labrum Müller, 1776 and Schistomysis ornata (G.O. Sars, 1864) and the mandibular sternite. Endites of the mandibles begin (Mysidacea) were removed from ovigerous females from the to bend and their internal sides exhibit two or three anterior Atlantic Ocean off the French coast. teeth followed by two smaller denticulations hidden by the labrum (Figs. 2c,2e). The mandibles have lost their rami Methods which remain as a small protuberance (Figs. 2d,2e). The mandibles appear to be mostly formed by the whole mandib- Animals were preserved in either 4% formalin or 70% ular segment (Fig. 2e). Indeed, the endites are fused with the ethanol. For scanning electron microscopy, fixed larvae were mandibular metamere and are linked by the sternite of the critical-point-dried, sputter-coated with gold and examined segment. Muscular insertions of both mandibles arise from with a Jeol JSM 35C scanning electron microscope (Service the left and right pleural parts of the segment, like the mus- commun de microscopie électronique de l’Université de Pro- cles of other appendages. However, they are linked by a vence, Marseille, France). transverse mandibular tendon, which couples the mandibles Penaeus indicus nauplii used for light microscopy were to allow synchronous movements (Fig. 2e). The mandibular fixed according to Arnaud et al. (1978), dehydrated, and em- segment is open dorsally at the tergite level (Fig. 2e) and is bedded in Epon. Semithin sections were cut using a LKB therefore devoid of a dorsal annulus. ultramicrotome and stained with Unna blue. At the zoea II stage, the aspect of the head changes, ow- The cuticle of whole larvae was also observed under light ing to the appearance of the stalked eyes under the rostrum, microscopy and underwent the following successive treat- which is now developed. The posterior suture on the carapace ments: (i) washing in 0.5% sodium hypochlorite solution; is always located at the beginning of the thorax (Fig. 3a). (ii) washing in 50% ethanol solution with 1.5% lactic acid; The annuli of the eight thoracic segments are well marked; and (iii) staining with chlorazol black in 50% ethanol solu- the first two possess biramous appendages and the last six tion at 40°C (Casanova et al. 1993). exhibit only traces of appendages, which appear as buds that become more prominent from the anterior to the posterior Results thoracic segments (Fig. 3b). These appendages appear simul- taneously at the subsequent zoea III stage, but are not yet Decapoda fully developed because they are uniramous (Fig. 3c). Penaeus indicus Mysis stages By the mysis I stage the appendages of the last six tho- Nauplius stage N6 racic appendages are biramous; buds prefiguring the five At the last nauplius stage (N6), a dorsal fold correspond- pairs of pleopods appear (Fig. 3d). The posterior suture on ing to the carapace appears at the antennar level and extends the carapace still occurs at the beginning of the thorax (Fig. 3d). dorsally along the mandibles, maxillules, and maxilles At the mysis II stage the posterior suture on the carapace (Fig. 1a). Semithin sections reveal that this fold arises from reaches the fourth thoracic segment, which exhibits a par- the cephalic dorsal tegument (Fig.
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