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Articles
Published: 2020-12-28

Novel symbiotic relationship between a spionid polychaete and Lingula (Brachiopoda: Lingulata: Lingulidae), with description of Polydora lingulicola sp. nov. (Annelida: Spionidae)

Department of Biology, Center for Liberal Arts & Sciences, Iwate Medical University, Iwate 028-3694, Japan
Laboratory of Biological Oceanography, Graduate School of Agricultural Science, Tohoku University, Sendai 980-8572, Japan
Annelida

Abstract

A new spionid species Polydora lingulicola sp. nov., a novel symbiont of Lingula anatina Lamarck, 1801 is described here based on materials collected from the Yatsushiro Sea and Ariake Sea, southern Japan. Polydora lingulicola sp. nov., morphologically closest to P. glycymerica Radashevsky, 1993 and P. vulgaris Mohammad, 1972, is distinct from latter two shell-boring species by its smaller size, long maximum caruncle length, non-boring lifestyle, presence of subspherical yellow chromatophores on chaetiger 5 (visible in living specimens), and larval morphology. The new species was observed to construct mud tubes on the surfaces of L. anatina shells, with the tube apertures located near the lateral inhalant pseudosiphon of the hosts, and utilizes the water currents created by the filter-feeding host for feeding suspended food particles. Polydora lingulicola sp. nov. represents the first polychaetous annelid reported to exhibit an obligate symbiotic relationship with a lingulid brachiopod. Epibiotic polychaetes previously reported as P. cornuta Bosc, 1802 to occur on L. anatina shells from Japan in 1902 may belong to P. lingulicola sp. nov. The possibility that the wild populations of P. lingulicola sp. nov. may be vulnerable to extinction because they only associate with L. anatina, wild populations of which are near threatened by habitat loss, coastal pollution, and fishing pressure.

References

  1. Abe, H., Kondoh, T. & Sato-Okoshi, W. (2016) First report of the morphology and rDNA sequences of two Pseudopolydora species (Annelida: Spionidae) from Japan. Zoological Science, 33, 650–658.

    https://doi.org/10.2108/zs160082

    Abe, H., Takeuchi, T., Taru, M., Sato-Okoshi, W. & Okoshi, K. (2019) Habitat availability determines distribution patterns of spionid polychaetes (Annelida: Spionidae) around Tokyo Bay. Marine Biodiversity Records, 12, 7.

    https://doi.org/10.1186/s41200-019-0167-4

    Akuta, K. (1995) Ecological distribution and life history of Lingula anatina (Brachiopoda, Inarticulata) in Asamushi, northern Japan. Unpublished M. Sci. Thesis, Tohoku University, Sendai, 42 pp. [in Japanese]

    Anker, A., Murina, G.V., Lira, C., Vera Caripe, J.A., Palmer, A.R. & Jeng, M.S. (2005) Macrofauna associated with echiuran burrows: a review with new observations of the innkeeper worm, Ochetostoma erythrogrammon Leuckart and Rüppel, in Venezuela. Zoological Studies, 44, 157–190.

    Blake, J.A. & Arnofsky, P.L. (1999) Reproduction and larval development of the spioniform Polychaeta with application to systematics and phylogeny. Hydrobiologia, 402, 57–106.

    https://doi.org/10.1023/A:1003784324125

    Blake, J.A. & Evans, J.W. (1973) Polydora and related genera as borers in mollusk shells and other calcareous substrates. The Veliger, 15, 235–249.

    Cameron, B. (1969) Paleozoic shell-boring annelids and their trace fossils. American Zoologist, 9, 689–703.

    https://doi.org/10.1093/icb/9.3.689

    Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540–552.

    https://doi.org/10.1093/oxfordjournals.molbev.a026334

    Chuang, S.H. (1956) The ciliary feeding mechanisms of Lingula unguis (L.) (Brachiopoda). Proceedings of the Zoological Society of London, 127, 167–189.

    https://doi.org/10.1111/j.1096-3642.1956.tb00468.x

    Clements, J.C., Bourque, D. McLaughlin, J., Stephenson, M. & Comeau, L.A. (2018) Wanted dead or alive: Polydora websteri recruit to both live oysters and empty shells of the eastern oyster, Crassostrea virginica. Journal of Fish Diseases, 41, 855–858.

    https://doi.org/10.1111/jfd.12794

    Dualan, I.V. & Williams, J.D. (2011) Palp growth, regeneration, and longevity of the obligate hermit crab symbiont Dipolydora commensalis (Annelida: Spionidae). Invertebrate Biology, 130, 264–276.

    https://doi.org/10.1111/j.1744-7410.2011.00234.x

    Emig, C.C. (1981) Observations sur l’écologie de Lingula reevei Davidson (Brachiopoda: Inarticulata). Journal of Experimental Marine Biology and Ecology, 52, 47–61.

    https://doi.org/10.1016/0022-0981(81)90170-2

    Emig, C.C. (1997) Ecology of inarticulated brachiopods. In: Kaesler, R.L. (Ed.), Treatise on Invertebrate Paleontology, Part H. Brachiopoda, Revised. Vol. 1. Boulder, Colorado and Lawrence, Kansas: Geological Society of America and University of Kansas, KS, pp. 473–495.

    https://doi.org/10.17161/dt.v0i0.5558

    Fujii, R., Ueno, R. & Yamamoto, T. (2019) Breeding season and life history of Lingula anatina after settlement in Amami-Oshima Island, Kagoshima, Japan. Plankton & Benthos Research, 14, 45–51.

    https://doi.org/10.3800/pbr.14.45

    Goto, R., Ishikawa, H., Hamamura, Y., Sato, S. & Kato, M. (2014) Evolution of symbiosis with Lingula (Brachiopoda) in the bivalve superfamily Galeommatoidea (Heterodonta), with description of a new species of Koreamya. Journal of Molluscan Studies, 80, 148–160.

    https://doi.org/10.1093/mollus/eyu009

    Hammond, L.S. (1983) Experimental studies of salinity tolerance, burrowing behavior and pedicle regeneration in Lingula anatina (Brachiopoda, Inarticulata). Journal of Paleontology, 57, 1311–1316.

    Hammond, L.S. (1984) Epibiota from the valves of recent Lingula (Brachiopoda). Journal of Paleontology, 58, 1528–1531.

    Hong, J.-S., Yamashita, H. & Sato, S. (2007) The Saemangeum Reclamation Project in South Korea threatens to extinguish an unique mollusk, ectosymbiotic bivalve species attached to the shell of Lingula anatina. Plankton & Benthos Research, 2, 70–75.

    https://doi.org/10.3800/pbr.2.70

    Hsieh, H.L. (1992) Pseudopolydora diopatra, a new species (Polychaeta, Spionidae) from Taiwan. Proceedings of the Biological Society of Washington, 105, 630–635.

    Hsieh, H.L. (1994) Larval development and substrate preference at settlement in Pseudopolydora diopatra (Polychaeta: Spionidae). Invertebrate Reproduction & Development, 25, 205–214.

    https://doi.org/10.1080/07924259.1994.9672387

    Ito, S. (2017) Growth and maturation of Lingula anatina in the inner part of Ariake Sound. Bulletin of Saga Prefectural Ariake Fisheries Research and Development Center, 28, 105–110. [in Japanese with English abstract]

    Japanese Association of Benthology (2012) Threatened Animals of Japanese Tidal Flats: Red Data Book of Seashore Benthos. Tokai University Press, Tokyo, 285 pp. [in Japanese]

    Katoh, K., Rozewicki, J. & Yamada, K.D. (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, bbx108.

    https://doi.org/10.1093/bib/bbx108

    Kenchington, R.A. & Hammond, L.S. (1978) Population structure, growth and distribution of Lingula anatina (Brachipoda) in Queensland, Australia. The Transactions of the Zoological Society of London, 184, 63–81.

    https://doi.org/10.1111/j.1469-7998.1978.tb03266.x

    Kuramochi, T., Koi, A., Kashihara, K. & Naganuma, T. (2012) Taxonomic revision of Japanese Lingula anatina with L. reevei (Brachiopoda: Lingulata). Biosphere Science: Journal of the Graduate School of Biosphere Science, Hiroshima University, 51, 27–35. [in Japanese with English abstract]

    Lützen, J., Hong, J.-S. & Yamashita, H. (2009) Koreamya arcuata (A. Adams, 1856) gen. nov. (Galeommatoidea; Montacutidae), a commensal bivalve associated with the inarticulate brachiopod Lingula anatina. Journal of Conchology, 39, 669–699.

    Macdonald, K.S., Ríos, R. & Duffy, J.M. (2006) Biodiversity, host specificity, and dominance by eusocial species among sponge-dwelling shrimp on the Belize Barrier Reef. Diversity and Distributions, 12, 165–178.

    https://doi.org/10.1111/j.1366-9516.2005.00213.x

    Manchenko, G.P. & Radashevsky, V.I. (1994) Genetic differences between two allopatric sibling species of the genus Polydora (Polychaeta: Spionidae) from the West Pacific. Biochemical Systematics and Ecology, 22, 767–773.

    https://doi.org/10.1016/0305-1978(94)90079-5

    Malan, A., Williams, J.D., Abe, H., Sato-Okoshi, W., Matthee, C.A. & Simon, C.A. (2020) Clarifying the cryptogenic species Polydora neocaeca Williams & Radashevsky, 1999 (Annelida: Spionidae): a shell-boring invasive pest of molluscs from locations worldwide. Marine Biodiversity, 50, 51.

    https://doi.org/10.1007/s12526-020-01066-8

    Martin, D. & Britayev, T.A. (1998) Symbiotic polychaetes: review of known species. Oceanography and Marine Biology: An Annual Review, 36, 217–340.

    Martin, D. & Britayev, T.A. (2018) Symbiotic polychaetes revisited: an update of the known species and relationships (1998–2017). Oceanography and Marine Biology: An Annual Review, 56, 371–448.

    https://doi.org/10.1201/9780429454455-6

    Mohammad, M.-B.M. (1972) Infestation of the pearl oyster Pinctada margaritifera (Linne) by a new species of Polydora in Kuwait, Arabian Gulf. Hydrobiologia, 39, 463–477.

    https://doi.org/10.1007/BF00046740

    Nishizawa, A., Sarashina, I., Tsujimoto, Y., Iijima, M. & Endo, K. (2010) Artificial fertilization, early development and chromosome numbers in the brachiopod Lingula anatina. Special Papers in Palaeontology, 84, 309–316.

    Orensky, L.D. & Williams, J.D. (2009) Morphology and ecology of a new sexually dimorphic species of Polydora (Polychaeta: Spionidae) associated with hermit crabs from Jamaica, West Indies. Zoosymposia, 2, 229–240.

    https://doi.org/10.11646/zoosymposia.2.1.17

    Radashevsky, V.I. (1989) Ecology, sex determination, reproduction and larval development of commensal polychaetes Polydora commensalis and Polydora glycymerica in the Japanese Sea. In: Sveshnicov, V.A. (Ed.), Symbiosis in marine animals. Russian Academy of Sciences, Moscow, pp. 137–164. [in Russian with English abstract]

    Radashevsky, V.I. (1993) Revision of the genus Polydora and related genera from the North West Pacific (Polychaeta: Spionidae). Publications of the Seto Marine Biological Laboratory, 36, 1–60.

    https://doi.org/10.5134/176224

    Radashevsky, V.I. (1999) Description of the proposed lectotype for Polydora websteri Hartman in Loosanoff & Engle, 1943 (Polychaeta: Spionidae). Ophelia, 51, 107–113.

    https://doi.org/10.1080/00785326.1999.10409402

    Radashevsky, V.I. (2005) On adult and larval morphology of Polydora cornuta Bosc, 1802 (Annelida: Spionidae). Zootaxa, 1064, 1–24.

    https://doi.org/10.11646/zootaxa.1064.1.1

    Radashevsky, V.I. (2012) Spionidae (Annelida) from shallow waters around the British Islands: an identification guide for the NMBAQC Scheme with an overview of spionid morphology and biology. Zootaxa, 3152, 1–35.

    https://doi.org/10.11646/zootaxa.3152.1.1

    Radashevsky, V.I. & Hsieh, H.-L. (2000) Polydora (Polychaeta: Spionidae) species from Taiwan. Zoological Studies, 39, 203–217.

    Radashevsky, V.I. & Pankova, V.V. (2013) Shell-boring versus tube-dwelling: is the mode of life fixed or flexible? Two cases in spionid polychaetes (Annelida, Spionidae). Marine Biology, 160, 1619–1624.

    https://doi.org/10.1007/s00227-013-2214-8

    Rice, L.N., Lindsay, S. & Rawson, P. (2018) Genetic homogeneity among geographically distant populations of the blister worm Polydora websteri. Aquaculture Environment Interactions, 10, 437–446.

    https://doi.org/10.3354/aei00281

    Richlen, M.L. & Barber, P.H. (2005) A technique for the rapid extraction of microalgal DNA from single live and preserved cells. Molecular Ecology Notes, 5, 688−691.

    https://doi.org/10.1111/j.1471-8286.2005.01032.x

    Rodrigues, S.C., Simões, M.G., Kowalewski, M., Petti, M.A.V., Nonato, E.F., Martinez, S. & Del Rio, C.J. (2008) Biotic interaction between spionid polychaetes and bouchardiid brachiopods: paleoecological, taphonomic and evolutionary implications. Acta Palaeontologica Polonica, 53, 657–668.

    https://doi.org/10.4202/app.2008.0410

    Sato, S., Owada, M., Haga, T., Hong, J.-S., Lützen, J. & Yamashita, H. (2011) Genus-specific commensalism of the galeommatoid bivalve Koreamya arcuata (A. Adams, 1856) associated with lingulid brachiopods. Molluscan Research, 31, 95–105.

    Sato-Okoshi, W. (1998) Three new species of polydorids (Polychaeta, Spionidae) from Japan. Species Diversity, 3, 277–288. https://doi.org/10.12782/specdiv.3.277

    Sato-Okoshi, W. (1999) Polydorid species (Polychaeta: Spionidae) in Japan, with descriptions of morphology, ecology and burrow structure. 1. Boring species. Journal of the Marine Biological Association of the United Kingdom, 79, 831–848.

    https://doi.org/10.1017/S0025315498001003

    Sato-Okoshi, W. & Abe, H. (2012) Morphological and molecular sequence analysis of the harmful shell boring species of Polydora (Polychaeta: Spionidae) from Japan and Australia. Aquaculture, 368–369, 40–47.

    https://doi.org/10.1016/j.aquaculture.2012.08.046

    Sato-Okoshi, W. & Abe, H. (2013) Morphology and molecular analysis of the 18S rRNA gene of oyster shell borers, Polydora species (Polychaeta: Spionidae), from Japan and Australia. Journal of the Marine Biological Association of the United Kingdom, 93, 1279–1286.

    https://doi.org/10.1017/S002531541200152X

    Sato-Okoshi, W., Abe, H., Nishitani, G. & Simon, C.A. (2017) And then there was one: Polydora uncinata and Polydora hoplura (Annelida: Spionidae), the problematic polydorid pest species represent a single species. Journal of the Marine Biological Association of the United Kingdom, 97, 1675–1684.

    https://doi.org/10.1017/S002531541600093X

    Sato-Okoshi, W., Sugawara, Y. & Nomura, T. (1990) Reproduction of the boring polychaete Polydora variegata inhabiting scallops in Abashiri Bay, North Japan. Marine Biology, 104, 61–66.

    https://doi.org/10.1007/BF01313158

    Sato-Okoshi, W. & Takatsuka, M. (2001) Polydora and related genera (Polychaeta, Spionidae) around Puerto Montt and Chiloé Island (Chile), with description of a new species of Dipolydora. Bulletin of Marine Science, 68, 485–503.

    Savazzi, E. (1991) Burrowing in the inarticulate brachiopod Lingula anatina. Palaeography, Palaeoclimatology, Palaeoecology, 85, 101–106.

    https://doi.org/10.1016/0031-0182(91)90027-O

    Savazzi, E. (2001) A review of symbiosis in the Bivalvia, with special attention to macrosymbiosis. Paleontological Research, 5, 55–73.

    Silvestro, D. & Michalak, I. (2012) RaxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution, 12, 335–337.

    https://doi.org/10.1007/s13127-011-0056-0

    Simon,C.A. & Sato-Okoshi, W. (2015) Polydorid polychaetes on farmed molluscs: distribution, spread and factors contributing to their success. Aquaculture Environment Interactions, 7, 147–166.

    https://doi.org/10.3354/aei00138

    Simon, C.A., Sato-Okoshi, W. & Abe, H. (2019) Hidden diversity within the cosmopolitan species Pseudopolydora antennata (Claparède, 1869) (Spionidae: Annelida). Marine Biodiversity, 49, 25–42.

    https://doi.org/10.1007/s12526-017-0751-y

    Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.

    https://doi.org/10.1093/bioinformatics/btu033

    Talavera, G. & Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology, 56, 564–577.

    https://doi.org/10.1080/10635150701472164

    Taylor, P.D. & Wilson, M.A. (2003) Palaeoecology and evolution of marine hard substrate communities. Earth−Science Reviews, 62, 1–103.

    https://doi.org/10.1016/S0012-8252(02)00131-9

    Teramoto, W., Sato-Okoshi, W., Abe, H., Nishitani, G. & Endo, Y. (2013) Morphology, 18S rRNA gene sequence and life history of a new Polydora species (Polychaeta: Spionidae) from northeastern Japan. Aquatic Biology, 18, 31–45.

    https://doi.org/10.3354/ab00485

    Williams, A., Cohen, B.L., Cusack, M. & Long, S. (2000) Provenance of Atlantic lingulid brachiopods. Palaeontology, 43, 999–1018.

    https://doi.org/10.1111/1475-4983.00159

    Williams, J.D. (2000) A new species of Polydora (Polychaeta: Spionidae) from the Indo-West Pacific and first record of host hermit crab egg predation by a commensal polydorid worm. Zoological Journal of the Linnean Society, 129, 537–548.

    https://doi.org/10.1111/j.1096-3642.2000.tb00616.x

    Williams, J.D. & McDermott, J.J. (2004) Hermit crab biocoenoses: worldwide review of the diversity and natural history of hermit crab associates. Journal of Experimental Marine Biology and Ecology, 305, 1–128.

    https://doi.org/10.1016/j.jembe.2004.02.020

    Williams, J.D. & Radashevsky, V.I. (1999) Morphology, ecology, and reproduction of a new Polydora species from the east coast of North America (Polychaeta: Spionidae). Ophelia, 51, 115–127.

    https://doi.org/10.1080/00785326.1999.10409403

    Williams, L.G., Karl, S.A., Rice, S. & Simon, C. (2017) Molecular identification of polydorid polychaetes (Annelida: Spionidae): is there a quick way to identify pest and alien species? African Zoology, 52, 105–118.

    https://doi.org/10.1080/15627020.2017.1313131

    Wisshak, M. & Neumann, C. (2006) A symbiotic association of a boring polychaete and an echinoid from the Late Cretaceous of Germany. Acta Palaeontologica Polonica, 51, 589–597.

    Yatsu, N. (1902a) On the habits of the Japanese Lingula. Annotationes Zoologicae Japonenses, 4, 61–67.

    Yatsu, N. (1902b) On the development of Lingula anatina. The Journal of the College of Science, Imperial University of Tokyo, Japan, 17, 1–112.

    Ye, L.T., Tang, B., Wu, K., Su, Y., Wang, R., Yu, Z. & Wang, J. (2015) Mudworm Polydora lingshuiensis sp. n is a new species that inhabits both shell burrows and mudtubes. Zootaxa, 3986 (1), 88–100.

    https://doi.org/10.11646/zootaxa.3986.1.4

    Ye, L.T., Yao, T., Wu, L., Lu, J. & Wang, J. (2019) Morphological and molecular diagnoses of Polydora brevipalpa Zachs, 1933 (Annelida: Spionidae) from the shellfish along the coast of China. Journal of Oceanology and Limnology, 37, 713–723.

    https://doi.org/10.1007/s00343-019-7381-0