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28 Phoronida OUP-SECOND UNCORRECTED PROOF, October 22, 2015 28 PHORONIDA Elena Temereva INTRODUCTION organization (Silén 1952, Emig 1982, Temereva and Malakhov 2001). Most phoronids have a head region, anterior and poster- Phoronids are marine invertebrates with biphasic life cycles. he ior portions of the trunk, and the ampulla (Fig. 28.1A). Adult group includes eleven accepted species (Temereva and Neretina phoronids have an unusual body plan: the dorsal side between 2013, Hirose et al. 2014) belonging to two genera: Phoronis the mouth and anus is extremely short, whereas the ventral side Wright, 1856 and Phoronopsis Gilchrist, 1907. According to is long (Fig. 28.1F). As a result, the digestive tract is U-shaped comparative anatomy and embryology, phoronids and other and both branches can be observed in the cross-section of the lophophorates (Bryozoa and Brachiopoda) were regarded as body (Fig. 28.1G). All phoronids have a very complex circu- archimeric and very close to the Deuterostomia (Masterman latory system and red blood (Selys-Longchamps 1907, Emig 1898, Siewing 1980, Nielsen 2002). Phoronids, however, have 1977, Temereva and Malakhov 2004a, b) (Fig. 28.1A). been recently regarded as trochozoans (Giribet et al. 2009), Most phoronid species have planktotrophic larvae nested within the brachiopods (Cohen 2013). Because the tro- (Fig. 28.1E), only P. ovalis has lecithotrophic, creeping lar- chozoan ailiation of phoronids is not clearly supported by com- vae. In some species, embryos and young larvae develop in parative anatomy and embryology, their phylogenetic position the lophophoral cavity; advanced larval stages live and feed in among the Bilateria remains uncertain. plankton. Planktotrophic phoronid larvae have a characteristic he benthic and worm-like adult phoronids live in their organization, which includes the preoral lobe (hood) with pre- own tubes embedded in soft or hard substrata (Fig. 28.1A, B). oral ciliated band, the collar with tentacles and postoral ciliated Adults may number > 100,000 m–2 (Emig 1982, Vyshkvartzev band, and the trunk with a terminal telotroch (Fig. 28.1E). In et al. 1990). Adult body length usually depends on the substra- advanced larvae, the ventral invagination (the metasomal sac) tum and ranges from several millimetres in burrowing phoro- of the epidermis arises under the tentacles, at the midline of the nids (Phoronis ovalis Wright, 1856) to 45 cm in phoronids living trunk. he metasomal sac grows with age and occupies the entire in soft substratum (Phoronopsis californica Hilton, 1930). he trunk coelom in competent larva (Zimmer 1964, Herrmann anterior body part is extended into the water and bears a lopho- 1979, Bartolomaeus 2001). phore with a double row of tentacles, which are covered by cilia Metamorphosis begins with a great contraction of special- and used to capture food (Temereva and Malakhov 2010). Inner ized larval muscles (Temereva and Tsitrin 2013), which gener- and external rows of tentacles surround the mouth and arrange ates pressure in the trunk coelom resulting in the eversion of the along a horseshoe line (Temereva and Malakhov 2009a). his metasomal sac (Zimmer 1964; Siewing 1974, Herrmann 1979, arrangement of tentacles gives rise to the name of all phoronids— Temereva 2010). he larval preoral lobe, tentacles, and telotroch ‘horseshoe worms’. he lophophore also functions in the brood- are partly or completely consumed, and the internal organ sys- ing of embryos and young larvae, in gas exchange, and in sensa- tems including the nervous system change substantially. tion that is provided by laterofrontal sensory cells (Fig. 28.1C). he organization of lophophore varies in diferent species and can be very complex (helicoidal lophohpore in P. californica) INVESTIGATIONS (Fig. 28.1B). In Phoronopsis spp., the lophophore base is sur- OF THE NERVOUS SYSTEM rounded by an epidermal fold (the ‘collar’) (Fig. 28.1D). Phoronis spp. lack a collar. he body is subdivided into several parts, he nervous system of adult phoronids has been investigated which difer in diameter, thickness of epidermis, and muscle largely with histological methods. he irst attempt to represent Structure and Evolution of Invertebrate Nervous Systems Edited by Andreas Schmidt-Rhaesa, Stefen Harzsch and Günter Purschke © Oxford University Press 2015. Published in 2015 by Oxford University Press. 351 47-Schmidt-Rhaesa-Chap47.indb 351 22/10/15 11:39 AM OUP-SECOND UNCORRECTED PROOF, October 22, 2015 STRUCTURE AND EVOLUTION OF INVERTEBRATE NERVOUS SYSTEMS Fig. 28.1. Peculiarities of phoronid morphology. A: D–G, Phoronopsis tentacle; ah: anal hill; am: ampulla; ap: anterior portion of the trunk; bc: harmeri. B. Phoronopsis californica. C. Phoronis australis. A: Live animal blood capillaries; bl: basal lamina; bm: blood masses; c: collar; c2: tentacu- extracted from the tube and viewed from the anal side. B: Lophophore lar coelom; c3: trunk coelom; db: descending branch of the digestive tract; of live animal from South China Sea. Photograph is copyrighted by Oleg dg: dorsal ganglion; ds: dorsal side of the body; e: erythrocyte; es: oesopha- Savinkin (Russia). C: Cross-section of the tentacle. Long microvilli of lat- gus; f: frontal side of the tentacle; gf: giant nerve ibre; hr: head region; lph: erofrontal cell are shown by double arrowhead. D: Head region and the lophophore; lv: lophophoral blood vessel; m: mouth; ms: metasomal sack; lophophore viewed from the anal side. E: Precompetent larva of Phoronopsis mv: median blood vessel; n :channel of nephridium; nh: nephridial hill; pl: harmeri viewed from the left side. Apical organ is to the top, ventral side is preoral lobe (hood); pp: posterior portion of the trunk; st: stomach; t: ten- to the left. F: Sagittal histological section of the head region. he oral side tacle; tnr: tentacular nerve ring; tt: telotroch; vs: ventral side of the body. A, is to the right; the anal side is to the left. G: Portion of cross-section of the B, E photographs of live animals. C semithin sections, stained with methyl- head region. he anal side is to the top; the oral side is to the bottom. a: ene blue. D scanning electron microscopy (SEM). F, G histological sections anus; ab: ascending branch of the digestive tract; af: abfrontal side of the stained with Caracci hematoxylin. the scheme of a phoronid deinitive nervous system was made by he phoronid nervous system has been investigated in greater Hilton (1922) who used histological methods including stain- detail for larvae than for adults. he irst detailed description of ing with methylene blue. he most detailed description of the the larval nervous system was made with histological methods adult phoronid nervous system was based entirely on histological (Zimmer 1964). he ultrastructure of the nervous system has data (Silén 1954) and was in all of the textbooks (Hyman 1959, been described in young larvae of Phoronis ijimai Oka, 1897 Bullock and Horridge 1965, Herrmann 1997). Transmission (Lacalli 1990) and advanced larvae of Phoronis muelleri Selys- electron micrographs (TEM) have been obtained for three Longchamps, 1903 (Hay-Schmidt 1989). TEM concerning the Phoronis species (Fernández et al. 1996) and one Phoronopsis organization of the nerve elements in the hood were obtained species (Temereva and Malakhov 2009b). TEM describing for competent larvae of P. pallida Silén, 1952 (Santagata 2002). innervation of phoronid tentacles were provided by Pardos he irst immunocytochemical study of P. harmeri larvae was and colleagues (1991, 1993). Neurites containing both clear made by Nezlin (1989), who investigated the development and dense-core vesicles occur in the basiepithelial nerve plexus of monoamine-reactive neurons. Comprehensive results on of Phoronis psammophila Cori, 1889 (Fernández et al. 1991). the distribution of catecholamine-containing, serotonin-like, he method of intravital staining with methylene blue allowed and neuropeptide FMRFamide-like immunoreactive elements description of several types of neurons in the trunk plexus of were obtained for advanced larvae of P. muelleri (Hay-Schmidt Phoronopsis harmeri Pixell, 1912 (Lagutenko 1996, 1997, 1998). 1990a). Santagata and Zimmer (2002) described two types of Apart from our preliminary investigations, immunocytochem- larval nervous system organization. Recent results revealed the istry has not been applied to adult phoronids. presence of the ventral nerve cord in young larvae of P. harmeri 352 47-Schmidt-Rhaesa-Chap47.indb 352 22/10/15 11:39 AM OUP-SECOND UNCORRECTED PROOF, October 22, 2015 PHORONIDA (Temereva 2012) and both deuterostome- and trochozoan-like he thickness of the trunk nerve plexus depends on the body features of nervous system organization during P. harmeri devel- part (Fig. 28.3A). he plexus is the thickest in the anterior por- opment (Temereva and Wanninger 2012). Only two publica- tion of the trunk (Fig. 28.1C). Here it consists of numerous tions include brief data about the remodelling of the phoronid longitudinal and transversal projections, which are associated nervous system during metamorphosis (Nezlin 1989, Santagata with numerous perikarya of diferent types. hese projections 2002). and perikarya form a continuous envelope around the basal membrane of the anterior body part. his area contains many neuromuscular junctions in the basal membrane (Fig. 28.2G). ARCHITECTURE In the posterior portion of the trunk, the plexus is represented by OF THE NERVOUS SYSTEM separate neurite bundles, each of which is formed by a few neu- rites. In the ampulla that is the terminal portion of the trunk, Gross anatomy of the adult nervous system the nerve plexus is organized as in the anterior body part, but is thinner (Fig. 28.2A). In adult phoronids, the nervous system is represented by the Innervation of the internal organs in adult phoronids has intraepithelial nerve plexus, which is thickened in several been inadequately investigated. Examinations at ultrastructural areas that are regarded as the main nervous system elements level revealed longitudinal and transversal neurite bundles in (Fig. 28.1F, G, 28.2A, B, 28.3A, B). he nervous system in adult the digestive tract epithelium (Fernández et al.
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