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28 PHOROnidA

Elena Temereva

intROdUctiOn organization (Silén 1952, Emig 1982, temereva and Malakhov 2001). Most 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 (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 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. . 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.

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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 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 . 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 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

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(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. 1996), excretory phoronids has two main elements: the tentacular nerve ring and organs (Fernández et al. 1996, temereva and Malakhov 2004c), the dorsal ganglion (Silén 1954, Fernández et al. 1996, temereva and blood vessels (temereva and Malakhov 2004b). and Malakhov 2009b). he dorsal ganglion and tentacular nerve ring are connected and pass each other at the dorsal side between Cytoarchitecture of the adult nervous system the mouth and anus (Fig. 28.1G, 3B). in addition, there is also the nerve plexus, which extends along the entire body, and the in adult phoronids, all neuronal elements have a similar cyto- giant nerve ibres (Fig. 28.2c, d). logical organization and stratiied structure that is related to the he tentacular nerve ring passes along the external side of the cellular layers (Fig. 28.2H, 28.3E–G). he internal layer con- lophophore base (Fig. 28.2B). it connects with thin neurite bun- tacts the basal lamina and is formed by numerous nerve ibres dles, which pass along each tentacle and contact sensory cells surrounded by the glial cell processes. in the neuropil of the of the postoral ciliated band. he tentacular nerve ring mostly dorsal ganglion, most neurites have large diameters and electron consists of numerous transversal neurites, which are associated light cytoplasm, whereas in the tentacular nerve ring neuropil with multipolar perikarya. Each tentacle contains two groups most neurites have small diameters and dense cytoplasm. he of neurite bundles: frontal and abfrontal (Pardos et al 1991, bodies of glial cells constitute the second layer (Fig. 28.2H). temereva and Malakhov 2009b) or two laterofrontal neurite he third layer consists of perikarya overarched by the bodies bundles, which connect the sensory cells of the tentacles and of epidermal cells. his stratiied structure is penetrated by basal tentacular nerve ring (Silén 1954). Although in the cross-section projections of epidermal cells, which contain thick bundles of of each tentacle groups of several frontal and abfrontal neurite tonoilaments (Fig. 28.2H). bundles can be found, there are always one mediofrontal, two laterofrontal, one medioabfrontal, and two lateroabfrontal neu- Fine organization of the nerve elements in adults rite bundles (Fig. 28.3d). he latter bundles are usually asso- ciated with large gland cells, whereas the laterofrontal bundles According to ultrastructural investigations by Fernandéz and are located near sensory laterofrontal cells. hese cells have eight colleagues (1996), four types of perikarya can be distinguished thick and long microvilli surrounding a cilium, and a long basal based mostly on vesicle characteristics: with dense content, process, which passes to the tentacular nerve ring (Fernández dense core vesicles, electron lucent vesicles, and electron light et al. 1996). Except laterofrontal sensory cells, each tentacle vesicles. According to other results, however, several kinds of contains perykarya, which do not contact the epidermis sur- vesicles can be found in one neurite, and it is impossible to dis- face and are scattered along the frontal and laterofrontal sides tinguish specialized types of perikarya (temereva and Malakhov (Fig. 28.3d). 2009b). Moreover, intravital staining of the phoronid trunk he dorsal ganglion is the concentration of nerve cells and nerve plexus with methylene blue revealed the presence of 24 processes on the dorsal side (Fig. 28.1F). it is located at the types of sensory neurons (Lagutenko 1996), eight types of epistome base and formed by two ends of the tentacular nerve motoneurones (Lagutenko 1997), and 15 types of interneur- ring (Fig. 28.1G). he ganglion largely consists of large motor ones (Lagutenko 1998). neurons were deined according to perikarya and their projections (Fig. 28.2E). their morphology and location in the epidermis. in the dorsal in all phoronids, the giant nerve ibres start from the dor- ganglion and tentacular nerve ring, numerous large perikarya sal ganglion and extend to the abfrontal side between the anus with electron light cytoplasm are present (Fig. 28.2E, H, J). and left and right nephridiopores (Fig. 28.1F, 28.2A, 28.3B). hese perikarya are 7–9 µm in diameter and do not contact hey run basiepithelially through the length of the anterior the surface of the epidermis. he nucleus contains a nucleolus body part and are always associated with lateral mesenteries and mostly lacks peripheral chromatin. he cytoplasm is illed (Fig. 28.2F, G). with many small mitochondria, rough endoplasmic reticulum,

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Fig. 28.2. details of the nervous system organization. A–F: H–L: cross-section of the giant nerve ibre. E: Longitudinal section of the dorsal Phoronopsis harmeri. G. Phoronis australis. A: Sagittal section of the head ganglion. he anal side is to the right; the oral side is to the left. F: cross- region; the dorsal ganglion looks like a large aggregation of nerve ibres. section of the epidermis and giant nerve ibre. G: he left giant nerve ibre B: Sagittal section of the head region; tentacular nerve ring is represented with several envelope cells (ec). he rupture of the basal lamina (bl) is shown by numerous nerve ibres and covered by an epidermal fold—collar (c). by straight arrowhead. H: Longitudinal section of the tentacular nerve ring. C: A portion of the nerve plexus in the anterior part of the trunk. D: he he collar (c), which covers the tentacular nerve ring, is to the right. he

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Fig. 28.2. Continued stratiied cytoarchitecture of the nerve plexus is clearly visible. I: A portion of (epidermal cells); G: Golgi apparatus; gf: giant nerve ibre; gc: glial cells; ld: the giant nerve ibre with several envelope cells (ec). J: A typical perikaryon of lipid droplet; llm: left lateral mesentery; lm: longitudinal muscles; mi: micro- the dorsal ganglion. K: Several neurites in the tentacular neurite bundle. he villi; mt: mitochondria; mv: median blood vessel; n: nucleus; np: neuropil; synaptic contacts are indicated by open arrowheads. L: Optical cross-section nu: nucleolus; p: perikaryon; to: tonoilaments; v: vesicles. A–D scanning of the anterior body part combined with Z-projection of 30 slides from 5-Ht electron microscopy (SEM). E,H semithin sections, stained with methylene channel. ab: ascending branch of the digestive tract; bl: basal lamina; c: collar; blue; some perikarya are indicated by arrows. F,G histological sections stained cm: circular muscles; c2: tentacular coelom; c3: trunk coelom; d: diaphragm; with caracci hematoxylin. I–K thin sections (transmission electron micros- db: descending branch of the digestive tract; ec: envelope cells; ep: epidermis copy). L immunocytochemical staining against 5-Ht.

granules of glycogen, and lipid droplets. in some perikarya, the FMRFamide-like immunoreactivity occur in the nerve tracts centriole associated with the Golgi apparatus is located near of the tentacle, tentacular nerve ring, dorsal ganglion, trunk the nucleus. nerve plexus, and oesophagus (Fig. 28.2L). he giant nerve Glial cells with characteristic polymorphic, dense granules are ibre exhibits neither serotonin-like nor FMRFamide-like abundant in all elements of the nervous system where they are immunoreactivity. intermingled with nerve ibres (Fernández et al. 1996, temereva Researchers have used antibodies to detect transmitter sub- and Malakhov 2009b). in all phoronids studied to date, the stances in phoronid larvae. he distribution of neurotransmitters cytoplasm of glial cells contains one or two centrioles closely and presence of some nerve elements were used to distinguish located to the Golgi complex. two types of nervous systems in phoronid larvae (Santagata and he giant nerve ibres are huge axons of one (in P. harmeri) Zimmer 2002). or several (in P. psammophila) perikarya (Silén 1954). hese axons are accompanied by some enveloping cells (Fig. 28.2F, G, i). P. psammophila contains specialized enveloping cells, which nEUROGEnESiS form a myelin-like envelope around the single axon (Fernández et al. 1996). in contrast, the two giant axons of both P. aus- Phoronid neurogenesis has been studied in two species difering tralis (Haswell 1883) and P. hippocrepia (Wright 1856) lack a in development: P. ijimai, which broods embryos and young lar- myelin-like sheath, and the enveloping glial cells do not com- vae (Hay-Schmidt 1990b), and P. harmeri, which has holopelagic pletely surround the axon, thereby leaving a small axonal area development (temereva and Wanninger 2012). in both species, in close apposition to the epidermal basal lamina (Fernández the irst step in neurogenesis is the appearance of serotonin-like et al. 1996). in P. harmeri, the single axon lacks a specialized immunoreactive perikarya on the anterior pole of the embryo. envelope and contacts the basal lamina only in the head region; he neurite bundle, which is associated with the postoral cili- in the rest of the body, the axon is surrounded by epidermal cells, ated band, is the irst serotonin-like immunoreactive nerve tract which form a complete multilayer myelin-like sheath (temereva to appear. in P. ijimai larvae, the minor nerve ring extending and Malakhov 2009b). he cytoplasm of the giant ibre con- above the tentacles appears irst, whereas in P. harmeri larvae, the tains small mitochondria, large vacuoles with light content, and main nerve ring passing below the tentacles appears irst. in both lucent vesicles (Fig. 28.2i). he giant nerve ibre forms efector species, the neurite bundle underlying the preoral ciliated band branches (collaterals), which pass around the body and innervate develops next. After the trunk is formed, the telotroch nerve ring the longitudinal muscle (Silén 1954, Lagutenko 1997). develops (temereva and Wanninger 2012). neurites, which form the innermost layer of the nerve plexus, FMRFamide immunoreactivity irst appears in the epi- can be divided into those with light cytoplasm and those with thelium of the apical plate and then in the neurites under the dense cytoplasm. heir diameter is usually greater for neurites preoral ciliated band, before the FMRFamide-like immunoreac- with light rather than dense cytoplasm. Both types of neurites tive tentacular neurite bundle develops. two FMRFamide-like contain diferent kinds of synaptic vesicles and cannot be cat- immunoreactive perikarya are located near the apical plate in egorized according to this feature. neurites swell where the early larvae of both species. hese perikarya are absent in the synapses form (Fig. 28.2K). All phoronids contain neuromuscu- young larvae of P. ijimai (Hay-Schmidt 1990b), but are present lar synapses (Fig. 28.3H). cells of longitudinal muscles usually in those of P. harmeri; many new perikarya appear in the epider- form the basal processes, which penetrate the basal lamina and mis of the hood, the oral ield, and the midgut (temereva and contact neurites (Fernández et al. 1996). hese penetrations are Wanninger 2012). evident in histological sections and look like a rupture of the basal lamina (Fig. 28.1G). he neurite sometimes contacts the muscular process embedded in the basal lamina (temereva and ORGAniZAtiOn OF tHE Malakhov 2009b). nERVOUS SyStEM in LARVAE

According to immunocytochemistry (Santagata and Zimmer nEUROtRAnSMittERS 2002), two types of nervous system organization are evident in competent (= ready for metamorphosis) phoronid larvae. For According to our preliminary observations of adult P. harmeri, both types, several main nerve elements can be recognized with neurites and perikarya that demonstrate serotonin- and immunocytochemistry. hese are the complex apical organ, the

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Fig. 28.3. he schemes of organization of phoronid nervous system. is to the right. he distal portion of the scheme is represented by longitudinal nervous elements are shown by diferent colours. Although the homology section of the epidermis, which contains several types of neurons described by between larval and adult nervous elements is still uncertain, some nervous Lagutenko (1996, 1997, 1998). he border of neurites aggregation is shown elements, which adults certainly inherit from larvae, are indicated by the same by dots. he clear spaces around the giant nerve ibre correspond to envelope colours in adult and in larva. A: he thickness of nerve plexus in diferent parts cells. C: Organization of the nervous system in competent larva of P. harmeri; of body; the scheme of sagittal section: the oral side is to the left, the anal side this picture is based on temereva and tsitrin 2014b. Ventral side is to the left, is to the right (based on temereva and Malakhov 2009). B: Organization of dorsal side is to the right. D: he location of neurite bundles in the tentacle the nervous system in the head region of adult P. harmeri. he scheme is based of adult phoronids; the scheme of cross-section of tentacle. E,F: cytological on own unpublished results, which were obtained with tEM and immunocy- organization of the dorsal ganglion (E) and tentacular nerve ring (F). Perikarya tochemical staining. he lophophore is simpliied; tentacles of the left side are are indicated by yellow, glial cells, by magenta. G: Scheme of the giant nerve removed; the collar is not shown completely. Oral side is to the left, anal side ibre of P. harmeri. H: he scheme of typical neuromuscular synapse. a: anus;

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Fig. 28.3. Continued af: abfrontal zone of the tentacle; afb: abfrontal neurite bundle; am: ampulla; gf: giant nerve ibre; hr: head region; in: interneurone (pale pink); lab: latero- amn: anterior marginal neurite bundle; an: aggregation of neurites; anr: anal abfrontal neurite bundle; lat: lateral zone of the tentacle; lfc: laterofrontal cell; nerve ring; ao: apical organ; ap: anterior portion of the trunk; ab: ascending lfb: laterofrontal neurite bundle; lm: longitudinal muscles; m: mouth; mg: branch of the digestive tract; bl: basal lamina; c: collar; cm: circular muscles; midgut; mgp: midgut perikarya; mn: motor neuron (pale blue); mnr: minor c2: tentacular coelom; db: descending branch of the digestive tract; dg: dor- nerve ring; msn: metasomal sack neurites and perikarya; n: duct of nephrid- sal ganglion; dlp: dorsolateral group of perikarya; e: erythrocyte; ec: envelope ium; nf: nerve ibre; pp: posterior portion of the trunk; sf: sensory ield; sn: cells; ep: epidermis (epidermal cells); epi: epistome; f: frontal zone of the ten- sensory neuron (magenta); t: tentacle; tn: trunk neurites and perikarya; tnr: tacle; fb: frontal neurite bundle; fc: frontal cilia of tentacle; fo: frontal organ; tentacular nerve ring; to: tonoilaments; ttn: telotroch nerve ring.

frontal organ, the tentacular neurite bundle (the main nerve ring), the primary simplicity of the nervous system of a common ances- the minor nerve ring, the marginal and median neurite bundles tor of the Bilateria (Mamkaev 1962, Lagutenko 1998). On the of the hood, the longitudinal neurite bundles in each tentacle, the other hand, the simplicity of the phoronid nervous system may be neurites, and the perikary of the metasomal sac (Santagata and considered a secondary condition resulting from a sessile lifestyle. Zimmer 2002). he combination of tEM and immunostain- Because phoronid larvae have a very complex organization of ing against serotonin, FMRFamide, and alpha-tubulin revealed the nervous system, which consists of numerous elements and the complex organization of the nervous system in competent P. exhibits some deuterostome-like features, it is more plausible to harmeri larvae (temereva and tsitrin 2014b). in addition to the suggest that this pattern of the nervous system was inherited from nerve elements listed above, competent P. harmeri larvae contain the last common bilaterian ancestor and then underwent simpli- the posterior marginal neurite bundle of the preoral lobe, two ication, correlated with a sessile lifestyle of adult phoronids. dorsolateral groups of perikarya associated with the main nerve ring, the perikarya and neurites of the trunk, and two circular AcKnOWLEdGEMEntS neurite bundles of the telotroch (Fig. 28.3c). he nerve net sur- rounds the oesophagus and cardiac sphincter of P. harmeri larvae, his research was supported in part by grants from the Russian which have numerous FMRFamide-like immunoreactive cells in Foundation for Basic Research (#14-04-00238), Russian their midguts (temereva 2010, temereva and tsitrin 2014b). Scientiic Found (# 14-14-00262), and a Grant of the President of Russia (# Md-5812.2015.4). VARiAtiOn OF tHE nERVOUS REFEREncES

SyStEM WitHin tHE tAxOn Bartolomaeus, t. (2001). Ultrastructure and formation of the body cavity lining in Phoronis muelleri (Phoronida, ). in Phoronopsis spp., the tentacular nerve ring is surrounded by Zoomorphology, 120, 135–148. the epidermal fold (Fig. 28.2B), whereas the collar is absent in Bullock, t.H. and Horridge, G.A. (1965). Structure and Function in the Phoronis spp. Among phoronids there are species with one or nervous System of invertebrates. W.H. Freeman and company. San with two giant nerve ibres. Large species usually have one giant Francisco. ibre, which is always on the left side and which can reach 80 cohen, B.L. (2013). Rerooting the rdnA gene tree reveals phoronids µm in diameter (Fig. 28.2F), while small species usually contain to be ‘brachiopods without shells’; dangers of wide taxon samples two giant ibres (left and right) with diameters of 1 to 10 µm in metazoan phylogenetics (Phoronida; Brachiopoda). Zoological (Fig. 28.2G). Journal of the Linnean Society, 167, 82–92. According to our observations of four-day-old juvenile P. cori, c.J. (1889). Beitrag zur Anatomie der Phoronis. inaug.-diss. Prague, 48pp. Univ. Leipzig. harmeri, the lophophore nervous system exhibits a regular Emig, c.c. (1977). Sur la structure des parois de l’appareil circula- alternation of intertentacular and abfrontal neurite bundles tore de Phoronis psammophila cori (Phoronida, Lophophorata). (temereva and tsitrin 2014a). in each tentacle, these bundles Zoomorphologie, 87, 147–153. pass through the corresponding lateroabfrontal and abfrontal Emig, c.c. (1982). he biology of Phoronida. Advances in Marine sides and connect with the tentacular nerve ring. he juveniles Biology, 19, 2–90. also have the minor nerve ring, which passes along the internal Fernández, i., Aguirre, A., Pardos, F., Roldan, c., Benito, J., and side of the lophophore base (Fig. 28.3B). it is shaped like a Emig, c. (1991). he epidermis of Phoronis psammophila cori horseshoe, the ends of which probably contact the dorsal gan- (Phoronida, Lophophorata): an ultrastructural and histochemical glion. he minor nerve ring connects the frontal neurite bun- study. Canadian Journal of Zoology, 69, 2414–2422. dles, which extend through each tentacle. he minor nerve ring Fernández, i., Pardos, F., Benito, J., and Roldan, c. (1996). consists of a few transversal nerve projections and cannot be Ultrastructural observation on the phoronid nervous system. Journal of Morphology, 230, 265–281. easily detected in histological sections, but can be detected by Giribet, G., dunn, c.W., Edgecombe, G.d., Hejnol, A., Martindale, staining against alpha-tubulin. he laterofrontal neurite bundles M.Q., and Rouse, G.W. (2009). Assembling the spiralian tree of do not contact the minor nerve ring. hey apparently skirt the life. in M.J. telford and d.t.J. Littlewood, eds. Animal Evolution, tentacle laterally and connect the tentacular nerve ring. pp. 52–64. Oxford University Press. new york. On the one hand, the simplicity of the general organization Haswell, W.A. (1883). Preliminary note on an Australian species of of the adult phoronid nervous system has traditionally been used Phoronis (Gephyrea tubicola). Proceedings of the Linnean Society of as evidence that phoronids are ‘lower’ Bilateria that have retained New South Wales, 7, 606–608.

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Hay-Schmidt, A. (1989). he nervous system of the actinotroch larva of Santagata, S. (2002). Structure and metamorphic remodeling of the lar- Phoronis muelleri (Phoronida). Zoomorphology, 108, 333–351. val nervous system and musculature of Phoronis pallida (Phoronida). Hay-Schmidt, A. (1990a). distribution of catecholamine containing, Evolution and Development, 4, 28–42. serotonin-like and neuropeptide FMRFamide-like immunoreactive Santagata, S. and Zimmer, R.L. (2002). comparison of the neuromus- neurons and processes in the nervous system of the actinotroch larva cular system among actinotroch larvae: systematic and evolutionary of Phoronis muelleri (Phoronida). Cell &Tissue Research, 259, 105–118. implication. Evolution and Development, 4, 43–54. Hay-Schmidt, A. (1990b). catecholamine-containing, serotonin-lake Selys-Longchamps, M. (1903). Über Phoronis und Actinotrocha bei and FMRFamide-like immunoreactive neurons and processes in the Helgoland. Wissenschaftliche Meeresuntersuchungen, Helgoland, 6, 1–55. nervous system of the early actinotroch larva of Phoronis vancouver- Selys-Longchamps, M. (1907). Phoronis. Fauna und Flora des Golfes von ensis (Phoronida): distribution and development. Canadian Journal Neapel, 30, 1–280. of Zoology, 68, 1525–1536. Siewing, R. (1974). Morphologische Untersuchungen zum Herrmann, K. (1979). Larvalentwicklung und Metamorphose von Archicoelomatenproblem. die Körpergliederung bei Phoronis muel- Phoronis psammophila (Phoronida, tentaculata). Helgoländer leri de Selys-Longchamps (Phoronidea): Ontogenese—Larve— Wissenschaftliche Meeresuntersuchungen, 32, 550–581. Metamorphose—Adultus. Zoologisches Jahrbücher Abteilung Herrmann, K. (1997). Phoronida. in F.W. Harrison and R.M. Woollacott Anatomie, 92, 275–318. eds. Microscopic Anatomy of Invertebrates. Vol. 13. Lophophorates, Siewing, R. (1980). das Archicoelomatenkonzept. Zoologisches Entoprocta, and cycliophora, pp. 207–235. Willey-Liss, new york. Jahrbücher Abteilung Anatomie und Ontogenie, 103, 439–482. Hilton, W.A. (1922). he nervous system of phoronida. Journal of Silén, L. (1952). Researches on Phoronidea of the Gullmar Fiord area Comparative Neurology, 34, 381–389. (West coast of Sweden). Arkiv för Zoologi, 4, 95–140. Hilton, W.A. (1930). A new Phoronopsis from california. Transactions of Silén, L. (1954). On the nervous system of Phoronis. Arkiv for Zoologi, the American Microscopical Society, 49, 154–159. 6, 1–40. Hirose, M. Fukiage, R. Katoh, t. Kajihara, H. (2014). description temereva, E.n. (2010). he digestive tract of actinotroch larvae and molecular phylogeny of a new species of Phoronis (Phoronida) (Lophotrochozoa, Phoronida): anatomy, ultrastructure, innerva- from Japan, with a redescription of topotypes of P. ijimai Oka, 1897. tions, and some observations of metamorphosis. Canadian Journal ZooKeys, 398, 1–31. of Zoology, 88, 1149–1168. Hyman, L.H. (1959). he lophophorate coelomates— Phoronida. temereva, E.n. (2012). Ventral nerve cord in Phoronopsis harmeri lar- in E.J. Boell, ed. he Invertebrates. Vol. 5. Smaller coelomate Groups, vae. Journal of Experimental Zoology (Molecular and Developmental pp. 228–274. McGraw-Hill, new york. Evolution), 318B, 26–34. Lacalli, t.c. (1990). Structure and organization of the nervous system in the temereva, E.n. and Malakhov, V.V. (2001). he morphology of the actinotroch larva of Phoronis vancouverensis. Philosophical Transactions of Phoronid Phoronopsis harmeri. Russian Journal of Marine Biology, the Royal Society of London B Biological Sciences, 327, 655–685. 27, 21–30. Lagutenko, y.P. (1996). cellular structure for the aferent link of the skin temereva, E.n. and Malakhov, V.V. (2004a). Ultrastructure of the nervous plexus of Phoronids (tentaculata, Phoronoidea) metasome. blood system in Phoronid Phoronopsis harmeri Pixell, 1912: 1. Zhurnal Evolutsionnoi Biokhimii I Fiziologii, 32, 448–459. [in Russian] capillaries. Russian Journal of Marine Biology, 30, 28–36. Lagutenko, y.P. (1997). System of motoneurones in the epidermal temereva, E.n. and Malakhov, V.V. (2004b). Ultrastructure of the nerve plexus of phoronids (tentaculata, Phoronoidea). Zhurnal blood system in Phoronid Phoronopsis harmeri Pixell, 1912: 2. Main Evolutsionnoi Biokhimii I Fiziologii, 33, 218–227. [in Russian] vessels. Russian Journal of Marine Biology, 30, 101–112. Lagutenko, y.P. (1998). System of interneurones in the epidermal nerve temereva, E.n. and Malakhov, V.V. (2004c). distinctive features of plexus in phoronids (tentaculata, Phoronoidea) and problem of the microscopical anatomy and ultrastructure of the metanephridia origin of associative link in lower Bilateria. Zhurnal Evolutsionnoi Phoronopsis harmeri, Pixell, 1912 (Phoronida, Lophophorata). Biokhimii I Fiziologii, 34, 64–75. [in Russian] Invertebrate Zoology, 1, 93–103. Mamkaev, y.V. (1962). About phoronids of far eastern seas. 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Acta Zoologica, 72, 81–90. morphic remodeling of the nervous system in juveniles of Phoronopsis Pixell, H. (1912). two new species of the Phoronidea from Vancouver harmeri (Phoronida): insights into evolution of the bilaterian ner- island. Quarterly Journal of Microscopical Science, 58, 257–284. vous system. Frontiers in Zoology, 11, 35.

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temereva E.n. and tsitrin E.B. (2014b). development and Wright, S. (1856). description of two tubicolar animals. Edinburgh organization of the larval nervous system in Phoronopsis harmeri: New Philosophical Journal, 4, 3–13. new insights into phoronid phylogeny. Frontiers in Zoology, Vyshkvartzev, d.i., Lebedev, E.B., and Kalashnikov, V.Z. (1990). 11, 3. consequences of the typhoon ‘Vera’: casting of invertebrates on temereva, E. and Wanninger, A. (2012). development of the nervous a sandy spit in Possjet Bay of the Sea of Japan. Russian Journal of system in Phoronopsis harmeri (Lophotrochozoa, Phoronida) reveals Marine Biology, 5, 78–80. both deuterostome- and trochozoan-like features. BMC Evolutionary Zimmer, R.L. (1964). Reproductive Biology and Development of Biology, 12, doi:10.1186/1471–2148–12–121 Phoronida, 416pp. University Microilm, Ann Arbor.

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