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The social feather duster worm Bispira brunnea (Polychaeta: Sabellidae): aggregations, morphology and reproduction

The fan worm Bispira brunnea is one of the most attractive sabellid polychaetes from Caribbean coral reef areas and it is exploited for ornamental purposes. An understanding of the structure of its aggregations, morphology and reproductive biology
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  Full Terms & Conditions of access and use can be found at Download by:  [UNAM Ciudad Universitaria] Date:  26 June 2017, At: 11:51 Marine Biology Research ISSN: 1745-1000 (Print) 1745-1019 (Online) Journal homepage: The social feather duster worm Bispirabrunnea (Polychaeta: Sabellidae): aggregations,morphology and reproduction Yasmín Dávila-Jiménez , María Ana Tovar-Hernández & Nuno Simōes To cite this article:  Yasmín Dávila-Jiménez , María Ana Tovar-Hernández & Nuno Simōes(2017): The social feather duster worm Bispira brunnea (Polychaeta: Sabellidae): aggregations,morphology and reproduction, Marine Biology Research, DOI: 10.1080/17451000.2017.1280608 To link to this article: Published online: 26 Jun 2017.Submit your article to this journal View related articles View Crossmark data  ORIGINAL ARTICLE The social feather duster worm  Bispira brunnea  (Polychaeta: Sabellidae):aggregations, morphology and reproduction Yasmín Dávila-Jiménez  a , María Ana Tovar-Hernández b and Nuno Sim ō es c a Posgrado en Ciencias del Mar y Limnología, Unidad Académica Sisal, Universidad Nacional Autónoma de México, Sisal, Yucatán, Mexico; b Facultad de Ciencias Biológicas, Laboratorio de Biosistemática, Universidad Autónoma de Nuevo León, San Nicolás de los Garza, NuevoLeón, Mexico;  c Facultad de Ciencias, Unidad Académica Sisal, Universidad Nacional Autónoma de México, Sisal, Yucatán, Mexico ABSTRACT The fan worm  Bispira brunnea  is one of the most attractive sabellid polychaetes from Caribbeancoral reef areas and it is exploited for ornamental purposes. An understanding of the structureof its aggregations, morphology and reproductive biology will provide information required tofacilitate artificial propagation of this species. Ten aggregations were collected in October 2013,February and March 2014 in the Majahual reef lagoon, Mexican Caribbean. Whole aggregationswere examined under light microscopy and scanning electron microscopy and the histology of oogenesis was determined. Aggregations were composed of 24 – 56 individuals and included juveniles and adults. The adults (5 – 20 mm) did not display any noticeable form of sexualdimorphism. In  B. brunnea  both sexual (hermaphroditism or gonochorism) and asexualreproduction occurred at the same time within the population: 92.71% reproduced sexuallyand 52% by architomy. The buds produced by architomy were inside the parental tube, atthree regenerative stages. The sex ratio was 36.75% males, 33.11% females, 22.84%hermaphrodites and 7.28% unknown (gametes not seen). Gametes were distributed in thelast thoracic segments and throughout the abdomen. Oogenesis was extra-ovarian,development followed four discrete stages and the oocytes were small and asynchronous(60.97  μ m in diameter). Sperm morphology was adapted to external fertilization in the watercolumn. Sequential (protandrous) hermaphroditism is suggested to occur in  B. brunnea . Thepyramidellid ectosymbiont mollusc  Odostomia  ( Eulimastoma )  caniculatum  is recorded herefor the first time as being associated with a sabellid worm. ARTICLE HISTORY Received 3 February 2016Accepted 6 January 2017 RESPONSIBLE EDITOR Danny Eibye-Jacobsen KEYWORDS Cluster duster; gonochorism;hermaphroditism; architomy;regeneration; oogenesis Introduction Tubicolous polychaetes belonging to the family Sabel-lidae Latreille, 1825, popularly known as  ‘ sea flowers ’ , ‘ feather dusters ’  or  ‘ fan worms ’ , are among the 10most imported ornamental invertebrates (Wabnitzet al. 2003). These organisms are popular because of the delicate appearance and attractive coloration of their branchial crown (Olivotto et al. 2011).In the Caribbean Sea, the sabellid polychaete worm Bispira brunnea  (Treadwell, 1917) is one of the mostphotographed invertebrates (Tovar-Hernández &Pineda-Vera 2008). Each worm inhabits an elastictube covered by fine sand (Nicol 1931; Bonar 1972). It is gregarious, hosting more than 100 worms in asingle aggregation, and is sometimes known as thecluster duster worm; it inhabits cracks and crevices incoral reefs, which makes its collection a challengingtask (Tovar-Hernández & Pineda-Vera 2008). It is oneof the most exploited invertebrates in terms of ornamental trading and is a common species inpopular aquarium and reef forums (Murray et al. 2012).Reproductive studies of ornamental tube wormsand their life cycle are important for the establishmentof suitable culture protocols. Culturing tube worms incaptivity may help decrease fishing pressure on wildpopulations and contribute to the preservation of coral reefs by avoiding the use of destructive collectingpractices (Bybee et al. 2006).The Sabellidae are among the best-understoodpolychaete families in terms of reproduction (McEuenet al. 1983; Rouse & Fitzhugh 1994; Giangrande 1997; Rouse et al. 2006). Sabellids display a range of sexualreproductive modes, from broadcast spawning to ovo-viviparity. They are mainly gonochoric, but some taxashow simultaneous or protandric hermaphroditism(Rouse et al. 2006). Brooding of larvae is present insome sabellids, either intratubular or extratubular,although the former is the most common within the © 2017 Informa UK Limited, trading as Taylor & Francis Group CONTACT  Yasmín Dávila-Jiménez Posgrado en Ciencias del Mar y Limnología, Unidad Académica Sisal, Universidad NacionalAutónoma de México, Puerto de Abrigo, Sisal, Yucatán, Mexico MARINE BIOLOGY RESEARCH, 2017  group (Rouse & Fitzhugh 1994). Asexual reproductionhas been reported frequently in sabellids, and takesthe form of architomy (spontaneous fission followedby subsequent regeneration). Natural fission from theposterior end, as opposed to regeneration followingdamage or autotomy, has been recorded in at least14 sabellid species grouped into nine genera (Tovar-Hernández & Dean 2014).Within the sabellid genus  Bispira  Krøyer, 1856, thereis information about reproduction in  Bispira volutacor-nis  (Montagu, 1804), a cold-water species distributedaround Ireland, which is dioecious and polythelic, sur-viving spawning and releasing all gametes in a singlebatch; sexual dimorphism is evident in this species(Nash & Keegan 2003). For  B. manicata  (Grube, 1878),an Australian tropical species, the sole reproductiveinformation is a report of asexual reproduction (Capa2008).The only published record of reproduction in B. brunnea  reported both sexual (dioecious) andasexual reproduction (Tovar-Hernández & Pineda-Vera2008), but gave no details of the structure (diameterand length of tubes, presence of offspring, associatedfauna) and composition of aggregations. The presentstudy describes the structure of aggregations, thedetailed body morphology in the juvenile and adultstages (descriptions available in the literature do notspecify whether they were based on adult or juvenilestages), allometry, reproductive modes, gamete mor-phology, distribution of gametes within body regionsand oogenesis. Such information will assist in theculture of   B. brunnea. Material and methods Aggregations of   Bispira brunnea  were collected inOctober 2013 (aggregations I – V), February (aggrega-tions VI – VIII) and March 2014 (aggregations IX – X) inthe reef lagoon of Majahual, Quintana Roo, MexicanCaribbean: 18°42 ′ 35.7 ′′ N, 87°42 ′ 44.7 ′′ W. Whole aggre-gations were fixed in 10% formalin – seawater for aperiod of 72 hours, and then transferred to 70%ethanol for preservation. Structure of aggregations Epibionts found among aggregations were removedfor identification. Each individual sabellid worm wasseparated carefully from its aggregation, labelled andplaced in an individual vial. The number of individualsper aggregation was noted. The diameter and length of 80 tubes were measured and all tubes were removedwith forceps. The presence of offspring inside thetube was recorded, as well as any evidence of regeneration. Morphology and morphometrics Terminology in this study follows Fitzhugh (1989).Measurements of body length (peristomium to pygi-dium), branchial crown length, thorax width andnumber of thoracic and abdominal segments wererecorded as mean±SD (range; number of individuals).The number of thoracic and abdominal segments andtheir respective standard deviations were rounded tothe nearest integer. Correlations of these measure-ments (232 individuals: 28 juveniles and 204 adults)were obtained on the basis of log-transformed dataand a power regression model to analyse growth andrelationship to the different maturity categories. Reproductive modes A longitudinal section throughout the body length of each sabellid worm was prepared to assess maturation(juvenile, adult) and sex (male, female, hermaphrodite).Methyl green was used to distinguish the gametes:sperm tissue stains blue whereas oocytes do not.When gametes were detected, a sample of gametetissue was placed in ethanol – glycerol on a slide andexamined by compound microscopy. Specimens werestained with Shirlastain A to compare the external mor-phology of adults, juveniles and fragments undergoingregeneration. Gamete distribution and morphology  In order to determine oogenesis, 15 individuals col-lected in March 2014 were processed for histology.They were embedded in paraplast (56 – 58°C meltingpoint), and serial sections were taken from spacedintervals along the thorax and abdomen (7  μ m) andstained with haematoxylin – eosin; slides weremounted permanently in synthetic resin (Sheehan &Hrapchak  1980; Bell & Lightner 1988; Austin & Austin 1989). A Nikon Eclipse E600 optical microscope wasused for observations and the diameter of 100oocytes was measured with a stage micrometer. Repro-ductive stages were categorized according to Bybeeet al. (2007): (1) no evidence of reproductive activityin the coelom (sex cannot be determined), (2) only coe-lomocytes present in the coelom (sex cannot be deter-mined), (3) some gametes present in the coelom (sexcan be determined), (4) coelom densely packed withgametes (sex can be determined). 2 Y. DÁVILA-JIMÉNEZ ET AL.  Juveniles, regenerating fragments and maturespecimens were observed by scanning electronmicroscopy. To determine distribution, size and mor-phology of gametes and to check for hermaphroditism,longitudinal sections from mature worms were dehy-drated in two changes of 100% ethanol. Specimenswere critical point-dried in CO 2 , then mounted onstubs with platinum tape and coated with gold(200 Å thickness). They were viewed under a Cam-bridge 250 scanning electron microscope and digitalimages were captured. Results Structure of aggregations Tube diameter was 1.74±0.43 mm (1 – 2.8 mm;  n =80)and tube length was 40±11 mm (25 – 60 mm;  n =80).In a single aggregation 24 – 56 worms were found,and basal tube parts were semitransparent, gluedtogether to form a dense plexus of entangled tubes.These aggregations were attached to dead or livingcoralline substratum, or to rocks among patches of brown algae; among the tubes were found crustaceans(decorator crab), echinoderms (ophiurans), nematodes,encrusting sponges, syllid polychaetes and molluscs( Cerithium litteratum  (Born, 1778),  Turbo castanea Gmelin, 1791,  Olivella rosolina  (Duclos, 1835), and  Euli-mastoma canaliculatum  (C.B. Adams, 1850)). Nema-todes were common in the sediments but were alsofound as endoparasites in the coelomic cavity of sixadults (one parasite per worm) and could not be ident-ified because they were in the early stages of develop-ment. The proximal parts of the sabellid tubes werefree and straight, covered by sand grains. Within eachaggregation, there were both juveniles (2 – 9 individ-uals) and adult forms (19 – 51 individuals). Morphology and morphometrics  Adult stage Of the 355 specimens examined, 302 (85.07%) wereadults. In adults, branchial crown as long as bodylength 12.4±3.13 mm (5 – 20 mm;  n =204) with 24±2radioles (18 – 28;  n =204) arranged in two semicircles(Figure 1G), not involuted mid-ventrally, basally joinedby a low palmate membrane. Dorsalmost radiolar pairwith a broad flange basally, as long as palmate mem-brane. Narrow radiolar flanges extending along radiolarlength, after palmate membrane. Longest pinnuleslocatedatmid-radiolarlength.Radiolartipslongandfili-form. Dorsal lips erect, triangular, with radiolar appen-dages (Figure 1G), extending beyond palmatemembrane. Ventral lips short, curved. Ventral sacs(sand sacs) projecting above ventral lappets whenrelaxed (Figure 1F). Dorsal margins of collar not fusedto faecal groove (Figure 1C). Anterior peristomial ringlobe well-exposed dorsally (Figure 1C). Lateral marginsof collar notched (Figure 1B), forming two ventral lobesand two dorsal ones. Ventral lappets triangular, distallyrounded. Ventral shield of chaetiger 1 as half circumfer-ence but divided longitudinally in two parts. Chaetae inchaetiger 1 elongate, narrowly hooded, arranged in anarc with spine-like chaetae inside this arc (Figure 1B).Body length 18.7±5.13 mm (8 – 30 mm;  n =204).Thorax with 12±1 segments (7 – 15;  n =204), 1.88±0.38 mm wide (1 – 2.8 mm;  n =204) (Figure 1D). Ventral shields rectangular, not indented by tori (Figure 1A).Notopodial thoracic lobes forming bundles (Figure 1B).Superior row of notochaetae elongate, narrowlyhooded chaetae, arranged in an arc. Inferior thoracicnotochaetaespine-like(Figure1B). Thoracicuncini(neu-rochaetae,Figure1B) avicular withrows ofprogressivelyshorter teeth above main fang, developed breast andmedium-size handle. Neuropodial companion chaetaewithasymmetricalhoods andgently taperingtips. Inter-ramaleyespotssmall,dark(Figure1E).Abdomenwith30±6 segments (13 – 49;  n =204) (Figure 1E) and conicalneuropodial lobes with chaetae arranged in a partialspiral pattern (Figure 1E). Abdominal neurochaetae of anteriorgroup distributedin C-shaped tospiral arrange-ment (Figure 1E), with chaetae of posterior groupenclosed in an arc; spine-like chaetae located in anteriorgroupandmodified,elongate,narrowlyhoodedchaetaeplaced in posterior one. Abdominal notochaetal uncini(Figure 1E) similar to thoracic neurochaetal uncini, butwithashorthandle.Pygidiumbilobed,withawell-devel-oped glandular epithelium (spongy, cushion-like) andeyespots.  Juvenile stage Of the 355 specimens examined, 53 (14.92%) were juveniles, each in its own tube, attached to the tubebase of a conspecific adult. Juveniles resemble adults(see below) except in size (Figure 2A,B). Body lengthwas 9.25±1.75 mm (6 – 12 mm;  n =28). Branchialcrown 7.3±1.76 mm in length (3.5 – 11 mm;  n =28)with 21±2 radioles (18 – 24 radioles;  n =28). Thoraxwidth 1.2±0.5 mm (0.5 – 2.5 mm;  n =28). Thoracic seg-ments 11±1 (9 – 14;  n =28) and 22±5 (12 – 32;  n =28)abdominal segments. Branchial crown well developed(Figure2B,D).Radiolesunitedbasallybyapalmatemem-brane(Figure2D).Pinnules(Figure2D),sandsacs(Figure 2B), and dorsal and ventral lips well-developed. Bodytrunk clearly divided into thorax and abdomen, as indi-cated by the chaetal inversion (Figure 2A – C). Collar MARINE BIOLOGY RESEARCH 3  segment (chaetiger 1) with only notochaetae (Figure2C), ventral lappets overlapped (Figure 2B) and dorsal collar margins not fused to faecal groove (Figure 2A,E).Pygidium bilobed (Figure 2A,B).  Allometry  The relationship between body length (x) andbranchial crown length (y) is described byy = 1.6994 x  0.6869 ( R 2 = 0.6526,  n  = 232) (Figure 3A).The relationship between body length (x) andnumber of abdominal segments (y) is described byy = 10.385 x  0.3584 ( R 2 = 0.2958,  n  = 232) suggestingcontinuous growth (Figure 3B). Body length alsoshowed a positive relationship with thorax widthand with the number of thoracic segments, althoughless strongly (Figure 3C,D). Figure 1.  Adult stage of   Bispira brunnea  under light microscopy. (A) collar and ventral view of thoracic segments; (B) collar andlateral view of thoracic segments; (C) collar and dorsal view of thoracic segments; (D) transition between thorax and abdomenin lateral view as indicated by continuous diagonal line; (E) abdominal chaetae, uncini and interramal eyespots; (F) ventralview of collar showing the sand sacs and ventral lappets; (G) branchial crown base and dorsal lips. Abbreviation: vs,ventral shields. 4 Y. DÁVILA-JIMÉNEZ ET AL.
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