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New Symbiotic Associations Involving Syllidae (Annelida: Polychaeta)

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New Symbiotic Associations Involving Syllidae (Annelida: Polychaeta) J. Mar. Biol. Ass. U.K. 2001), 81,3717/1^11 Printed in the United Kingdom New symbiotic associations involving Syllidae Annelida: Polychaeta), with taxonomic and biological remarks on Pionosyllis magni¢ca and Syllis cf. armillaris Eduardo Lo¨ pez*, Temir A. BritayevO,DanielMartinP½ and Guillermo San Mart|¨n* *Departamento de Biolog|¨a, Unidad de Zoolog|¨a, Laboratorio de Invertebrados Marinos, Facultad de Ciencias, Universidad Auto¨ noma de Madrid, 28049 Canto Blanco Madrid), Spain. OA.N. Severtzov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninsky pr. 33, 117071 Moscow, Russia. PCentre d'Estudis Avanc° ats de Blanes CSIC), Cam|¨ de Sta. Ba© rbara S/N, 17300 Blanes Girona), Spain. ½Corresponding author, e-mail: [email protected] Several new symbiotic associations involving Syllidae Annelida: Polychaeta) are reported. The number of known host sponge species infested by Haplosyllis spongicola is updated to 36, with seven hosts being reported for the ¢rst time i.e. Aplysina corrugata, Aplysina sp., Cliona sp., Cliona viridis, Phorbas tenacior,one sponge from Iran, one sponge from Cambodia). Two infestation patterns a few worms per host cm3 in temperate waters and 10s or 100s in tropical waters) are identi¢ed. The taxonomic and ecological characteristics of the species are discussed. Five associations occurring between four syllid worms and decapod crustaceans are fully reported for the ¢rst time. Syllis cf. armillaris, S. ferrani and S. pontxioi occurred inside gastropod shells occupied by hermit crabs as well as Pionosyllis magni¢ca,whichwasalso found inside the branchial chambers of the giant crab Paralithodes camtschatica. The description of Pionosyllis magni¢ca is emended on the basis of the new specimens found, while some taxonomic remarks on Syllis cf. armillaris are given. In addition, further evidence of sexual P. magni¢ca) and asexual S. cf. armillaris) reproduction in symbiotic syllids is provided. INTRODUCTION were reported Hoberg et al., 1982). Recently, some other associations involving Pionosyllis magni¢ca Moore and Syllis The Syllidae are a very large and diverse polychaete cf. armillaris MÏller) were also reported Martin & family. Syllids are found in many di¡erent habitats, Britayev, 1998). In this paper, the details of these associa- including the surfaces and inner channels and cavities of tions are described and discussed. Moreover, the morpho- other marine invertebrates. About 28 species have been logical description of P. magni¢ca is emended in the light of reported in association with cnidarians, crustaceans, echi- new specimens found during the present study, while some noderms and ascidians but they are particularly frequent taxonomic remarks on Syllis cf. armillaris are given. In and abundant in sponges Martin & Britayev, 1998). addition, further evidences of sexual P. magni¢ca)and Sponges are one of the most common host group asexual S. cf. armillaris) reproduction in symbiotic syllids including about 16% of the host species) for parasitic are provided. Additionally, some new associations invol- polychaetes Martin & Britayev, 1998), where they often ving the species Syllis ferrani Alo¨ s&SanMart|¨ nandSyllis exceed the density of other inhabitants Dauer, 1974; pontxioi San Mart|¨ n&Lo¨ pez are reported for the ¢rst Tabachnikov, personal communication). Probably the time. most representative syllid harboured by sponges is the cosmopolitan species Haplosyllis spongicola GrÏbe). It is a MATERIALS AND METHODS typical example of a polyxenous relationship among symbiotic polychaetes, with 22 di¡erent host sponge The study was based on preserved specimens, which are species reported to date Martin & Britayev, 1998). In deposited within the author's personal collections except this paper, the number of host sponge species harbouring for those specimens where the corresponding museum and H. spongicola is updated to 35, on the basis of both newly catalogue number are indicated in the `Examined mate- collected material, museum collections and biblio- rial' section). For scanning electron microscope SEM) graphical sources. Moreover, we discuss the `cosmopolitan' observations, the preserved worms were washed three character of the species based on the infestation character- times in distilled water 30 min each), run through a istics of the sponge^worm associations. series of ethanol concentrations, and stored in 70% There were a very few known symbiotic relationships ethanol until observation. Immediately prior to viewing between syllid worms and decapod crustaceans. The ¢rst in a Hitachi S.570 SEM Laboratorio de Microscop|¨a reported association was that between Syllis cornuta Electro¨ nica of the Institut de Cie© ncies del Mar of Barce- Rahtke and an unidenti¢ed hermit crab Fauvel, 1923). It lona, C.S.I.C.), they were run through a series of ethanol was not until 1982 that other associations between a syllid concentrations ending with 100% alcohol, critical-point i.e. Eusyllis blomstardi) and several species of pagurids dried, attached to a stub, and coated with gold. All Journal of the Marine Biological Association of the United Kingdom #2001) 3717.2 E. Lo¨ pez et al. New symbiotic associations involving syllids images were captured and stored in digital format using host cm3 in tropical hosts; and ii) less than one worm per the Printerface System hardware and software. host cm3 in the Mediterranean i.e. temperate) sponges When possible, infestation intensities were estimated Table 1). after extracting the worms from each host i.e. decapod The species has been previously reported from detritic hosts, referred to as worms per host) or from a piece of and muddy bottoms, `mae« rl', intertidal algae, photophilic known volume i.e. sponge hosts, referred to as worms per and sciaphilic algae on infralittoral hard bottoms, organo- cm3 of host). Worm extractions and counting were made genic calcareous concretions such as encrusting algae and under a Zeiss Stemi 2000-c stereomicroscope. Light corals) and Posidonia oceanica meadows foliar and rhizome microscope observations and line drawings were made strata). The species has been also mentioned in association with a Leitz Diaplan stereomicroscope equipped with with colonies of other organisms, such as hydroids Lo¨ pez interference contrast optics Nomarsky) and linked to a et al., 1996), Microcosmus sp. and Phyllochaetopterus socialis camera lucida. Light microscope micrographs were made Campoy, 1982), and vermetid reefs Amoureux & with a Zeiss Axioplan stereomicroscope equipped with Gante© s, 1976; Baratech & San Mart|¨ n, 1987; Ben-Eliahu, the SPOT hardware and software SP100 KAF1400 1977; Campoy, 1982; Nu¨ ·ez et al., 1992) or associated to digital camera and software version 2.1.) from Diagnostic organogenic calcareous concretions Laubier, 1966; Lo¨ pez Instruments Inc. et al., 1996; Martin, 1987; Nu¨ ·ez et al., 1992). World distribution RESULTS Cosmopolitan in warm tropical and subtropical) Family SYLLIDAE Grube, 1850 waters. Occasionally reported from temperate boreal Subfamily Syllinae Grube, 1850 waters. Genus Haplosyllis Langerhans, 1879 Pionosyllis magni¢ca Moore, 1906 Haplosyllis spongicola GrÏbe, 1855) Table 1) Figures 1^3 Haplosyllis spongicola^Licher 2000), pp. 344^346. Pionosyllis magni¢caöMoore 1906), page 223, pl. 10, Material examined ¢gures 9^11; Annenkova 1938) page 152; Uschakov More than 100 specimens from Aplysina corrugata, A. ¢stu- 1950) page 176, ¢gure 13; Hartman 1968), page 447; laris and Aplysina sp., collected on July 1981 by H. M. Kudenov & Harris 1995), page 54, ¢gure 1.19. Reiswig, 15^20 m depth; 115 specimens from A. bathyphila, Eusyllis magni¢caöPettibone 1954), page 261; Banse & collected in 1998 by M. Maldonado, 40^115 m depth; 210 Hobson 1974), page 56, ¢gure 14f. specimens from Haliclona sp., collected on 7 December 1985 by T.A. Britayev, 3^4 m depth; 68 specimens from Material examined Aaptos cf. aaptos, collected on 4 April 1989 byT.A. Britayev, Bering Sea, 5752.050^5756.04'N 17040.05 0^170 4 0.0 0 0W, 2.5 m depth; 360 specimens from an unidenti¢ed pink r/vAdler, cruise no. 18, station 150, 50 m depth, September sponge collected in October 1998 by E. Dutrieux, 14^15 1973; two specimens collected by Victor N. Goriachev on m depth; 95 specimens from Cliona sp., National Museum Paralithodes camtschatica. Southern coast of Kamchatka of Natural History, Smithsonian Institution, USNM 51687; peninsula, point Lopatka, 6^8 m depth, August 1985; one three specimens from C. viridis in gamma massive) specimen collected by Andrey A. Adrianov in a gastropod growth stage, collected in early summer, 1999 by D. shell occupied by Pagurus sp.. Martin, 9 m depth; three specimens from Phorbas tenacior, collected in late spring, 1999 by D. Martin, 6 m depth; 10 Emended description specimens from unidenti¢ed white sponge collected on 12 Body long, thick, up to 28 mm long, 0.85 mm wide November 1999 by Dr B. Tursch and Dr Y. Kantor, 20 m without parapodia, for 73 setigers. Colour white to depth. yellowish in alcohol) with brownish ventral spots or All known geographical locations and infestation inten- bodies at the base of posterior parapodia Figure 3B). sities for the currently known host sponge species are Prostomium subpentagonal, wider than long, with four summarized inTable 1. eyes in trapezoidal to rectangular arrangement; median antenna originating between the anterior pair of eyes, Ecology longer than the length of prostomium and palps together; Haplosyllis spongicola inhabited the host aquiferous system lateral antennae
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