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Chaetal Loss and Replacement in Pseudopotamilla Reniformis (Sabellida, Annelida)

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Chaetal Loss and Replacement in Pseudopotamilla Reniformis (Sabellida, Annelida) Invertebrate Biology 133(3): 261–273. © 2014, The American Microscopical Society, Inc. DOI: 10.1111/ivb.12061 Chaetal loss and replacement in Pseudopotamilla reniformis (Sabellida, Annelida) Glafira D. Kolbasova,1,a Alexander B. Tzetlin,2 and Elena K. Kupriyanova3 1 Department of Invertebrate Zoology, Moscow State University, Moscow 119991, Russia 2 Pertsov White Sea Biological Station, Moscow State University, Moscow 119991, Russia 3 The Australian Museum, Sydney, New South Wales 2010, Australia Abstract. Chaetae are continually being replaced during the life of a polychaete, but the process of chaetal degeneration during replacement is still poorly known. Chaetal loss occurs either one at a time through special degenerative sites, or all chaetae in a chaetal sac are lost simultaneously in the absence of degenerative sites. Old chaetae can be either resorbed inside the coelom or shed. This study describes chaetal degradation, loss, and sub- sequent replacement during experimentally induced regeneration in the sabellid polychaete Pseudopotamilla reniformis. During post-traumatic regeneration in P. reniformis, abdominal- type chaetae fall from the chaetal sac simultaneously without degenerative sites, and are replaced by thoracic-type chaetae. Chaetal sac degradation occurs in three main stages: (1) formation of numerous lysosomes and small electron-transparent vesicles in follicle cell cytoplasm; (2) disintegration of follicular cell membranes; and (3) disintegration of follicular cell cytoplasm. Description of changes during parapodial transformation allows identifica- tion of signs of degradation that can serve as histological indicators of chaetal degeneration in a wide range of polychaetes. Our study suggests that chaetal degeneration and loss in polychaetes can occur either with degenerative sites or without them, depending on the type of chaetal replacement. Additional key words: chaetal sac, chaetal degeneration, chaetogenesis, morphallaxis, uncini Chaetae, epidermal extracellular structures that replaced by those of another, as shown for, e.g., lent their name to the now-defunct taxon Polychae- Lumbrineris fragilis (O.F. MULLER€ 1766) by Tzetlin ta, play an important role in life of these annelid (1990), Scolelepis squamata (MULLER€ 1806) by worms (Woodin & Merz 1987). Chaetal morphology Hausen & Bartolomaeus (1998), and Dipolydora and functions are extremely variable: in different concharum (VERRILL 1880) by Radashevsky & species, chaetae are used for defense, crawling, Fauchald (2000). In large polychaetes that grow dra- swimming, burrowing, and body anchoring within matically in their lifetime, small juvenile chaetae are tubes (Woodin & Merz 1987; Fitzhugh 1991; Merz replaced by larger adult chaetae (Pilgrim 1977; & Woodin 2006). In spite of the functional impor- Bhaud 1988; Duchene & Bhaud 1988). In addition, tance of chaetae, many aspects of chaetal develop- worn-out and broken adult chaetae are replaced by ment are still unclear. new chaetae (Hausen 2005). Annelid chaetae are continually and routinely There are, however, two unusual types of chaetal replaced during the life of a worm. During settle- replacement. Probably the most remarkable of them ment and metamorphosis, larval chaetae are is epitoky, metamorphosis of an immature worm replaced by juvenile chaetae (Eckelbarger 1975, into a sexually mature reproductive form. Epitokous 1976, 1977; Amieva & Reed 1987; Eeckhaut et al. transformation results in atokous chaetae of benthic 2003; Gibson & Gibson 2004; Gibson & Smith 2004; worms being replaced by modified epitokous swim- Pernet & McArthur 2006; Smart & von Dassow ming chaetae (see, e.g., Clark 1961; Simpson 1962; 2009; Budaeva & Fauchald 2010). As juveniles Hofmann 1974; Daly 1975; Kuper & Westheide grow, chaetae of one morphological type may be 1998; Petersen 1999; Chatelain et al. 2008). Another unusual type of chaetal replacement takes place dur- aAuthor for correspondence. ing regeneration of Sabellidae and Serpulidae. The E-mail: [email protected] body of these worms is subdivided into thorax and 262 Kolbasova, Tzetlin, & Kupriyanova abdomen, and the thoracic chaetal arrangement dif- tion in this species can be easily induced artificially fers from the abdominal one. A part of an abdomen (Kolbasova et al. 2013). Such experimentally can regenerate into a complete worm; during regen- induced regeneration provides a convenient experi- eration, anterior abdominal parapodia are trans- mental system not only for studies of chaetal regen- formed into thoracic ones by losing their old eration (Berrill 1977, 1978; Murray 2010; Licciano abdominal-type chaetae and replacing them with et al. 2012), but also for examination of degenera- thoracic-type chaetae (Berrill 1931, 1977, 1978; tive sites. Berrill & Mees 1936a,b; Pernet 2001; Murray 2010; Licciano et al. 2012). Methods Each chaeta develops from an individual epider- mal follicle. Several follicles are usually organized in The adult body length of Pseudopotamilla renifor- one or several rows situated inside a common chae- mis is 50–70 mm. The thorax consists of 7–14 (typi- tal sac, an invagination of epithelial basal lamina cally 8–9) segments, and the abdomen consists of (Bartolomaeus 1995; Hausen 2005; Kieselbach & 80–120 chaetigers. Both thoracic and abdominal Hausen 2008). Usually one parapodium has two parapodia are illustrated in Fig. 1A–D. The first chaetal sacs, the notopodial sac and the neuropodial (collar) segment lacks neuropodia, while the subse- one (Mettam 1967; O’Clair & Cloney 1974). Accord- quent thoracic segments bear dorsal notopodia and ing to a widely accepted general model of chaetal ventral neuropodia (Fig. 1A). The thoracic notopo- replacement, formation of new chaetae occurs at a dium bears two clusters of capillary chaetae: a single special formative site at one end of the chaetal row, semicircle of 8–10 narrowly hooded capillary chae- while degeneration takes place at a degenerative site tae in the superior (dorsalmost) cluster, and two located at the opposite end of the row (Pilgrim parallel transverse rows of 10–12 paleate capillary 1977; Duchene & Bhaud 1988; Hausen 2005; Hoff- chaetae in the inferior (ventralmost) cluster mann & Hausen 2007). Newly formed chaetae enter (Fig. 1A,C) (note that all chaetal terminology used the row and push the older ones toward the other is sensu Fitzhugh 1989). Each thoracic neuropodium end; the oldest chaetae are either gradually resorbed bears two parallel tori with 19–28 acicular uncini in (Thomas 1930; Pilgrim 1977) or are shed (Duchene the anterior row and 18–24 avicular uncini in the & Bhaud 1988; Hausen 2005). posterior row (Fig. 1A,C). Each abdominal notopo- The outlined chaetal replacement model implies dium bears one transverse row of 15–20 avicular un- that each chaetal row should contain both formative cini, and each neuropodium bears two parallel and degenerative sites. Formative sites are easy to transverse rows, each consisting of 7–12 broadly find, and chaetal formation (chaetogenesis) in anne- hooded capillary chaetae (Fig. 1B,D). lids has been extensively studied by both light Adults of P. reniformis were collected by scuba and electron microscopies (Bartolomaeus 1995; divers in June 2010 from Kandalaksha Bay near the Meyer & Bartolomaeus 1996; Bartolomaeus & Meyer White Sea Biological Station (66°340 N, 33°080 E). 1997; Hausen & Bartolomaeus 1998; Hausam & Worms were cut into 2–4 pieces with scissors and Bartolomaeus 2001; Bartolomaeus 2002; Hausen placed into aquaria with running seawater to allow 2005). However, degenerative sites have been regeneration. During regeneration, the branchial described only for Clymenella torquata (LEIDY 1855) crown, pygidium, and the first two thoracic chaeti- by Pilgrim (1977), Capitella capitata (FABRICIUS 1780) gers are formed de novo from the apical blastema, by Schweigkofler et al. (1998), and Owenia fusiformis while the remaining thoracic segments (typically DELLE CHIAJE 1844 by Meyer & Bartolomaeus (1996). 6–7) transform from the nearest 6–7 abdominal seg- It is not clear why degenerative sites are so elu- ments (a phenomenon known as morphallaxis). The sive. One possible explanation is that degenerative transforming segments lose abdominal-type chaetae, sites are difficult to observe because chaetae are lost which are replaced by new thoracic-type chaetae so quickly that observing degeneration of an indi- (Figs. 2, 3A–F). The reorganization takes about vidual chaeta is nearly impossible. Alternatively, the 100 d (Kolbasova et al. 2013). To establish the chaetal replacement model may not be universal, course of morphogenetic events following the para- and in some species, chaetal degenerative sites might podial reorganization, every 3–5d,5–8 worms were not form at all. To address this question, we exam- photographed and fixed for further examination ined morphogenetic events during chaetal degenera- using both scanning and transmission electron tion and replacement in the sabellid polychaete microscopy (Kolbasova et al. 2013). For scanning Pseudopotamilla reniformis (BRUGIERE 1789). Chaetal electron microscopy (SEM), the animals were fixed replacement as a result of thoracic region regenera- in 2.5% glutaraldehyde in PBS buffer with 1% Invertebrate Biology vol. 133, no. 3, September 2014 Chaetal loss in polychaetes 263 Fig. 2. Schematic illustration of parapodial reorganiza- tion in Pseudopotamilla reniformis. A. Intact abdominal parapodium. B. At the 10th day after fragmentation, abdominal notopodia lose their uncini, and formative
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