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Patterns of shell utilization and preference in two sipunculan genera, Phascolion and Aspidosiphon

Published online by Cambridge University Press:  06 July 2022

Kohei Oshiro*
Affiliation:
Seto Marine Biological Laboratory, Field Science Education and Research Center, Kyoto University, 459 Shirahama, Nishimuro, Wakayama 649-2211, Japan
Akihiro Yoshikawa
Affiliation:
Coastal Marine and Social Science Section, Atmosphere and Ocean Research Institute, The University of Tokyo, 1-19-8 Akahama, Otsuchi, Iwate 028-1102, Japan
Akira Asakura
Affiliation:
Seto Marine Biological Laboratory, Field Science Education and Research Center, Kyoto University, 459 Shirahama, Nishimuro, Wakayama 649-2211, Japan
Ryutaro Goto
Affiliation:
Seto Marine Biological Laboratory, Field Science Education and Research Center, Kyoto University, 459 Shirahama, Nishimuro, Wakayama 649-2211, Japan
*
Author for correspondence: Kohei Oshiro, E-mail: oshiro.k.pdbk@gmail.com

Abstract

Sipunculans are non-segmented marine worms with an anterior retractable introvert, which are commonly included in Annelida based on molecular phylogenetic and phylogenomic analyses. They generally burrow in the soft sediments or live inside the crevices of hard substrata (e.g. calcareous/coralline rocks). However, members of some sipunculan genera (mainly Phascolion and Aspidosiphon) are known to have a peculiar habit of dwelling in vacant shells of gastropods or scaphopods. In this study, we investigated the shell utilization and preference pattern of the species of Phascolion and Aspidosiphon in Japan. We collected 302 sipunculans, comprising 273 and 29 individuals in Phascolion and Aspidosiphon, respectively, from 57–800 m depth of three study sites in the Pacific coast of Honshu Island, Japan. The species of Phascolion were found in vacant shells of 38 genera of 27 families of gastropods and six genera of four families of scaphopods, whereas the species of Aspidosiphon were found in 11 genera of 11 families of gastropods and one genus of scaphopod. These results suggest that members of each genus use a wide range of gastropod and scaphopod shells. The body size of the sipunculans was positively correlated with the shell size, suggesting that they change the shells as they grow. Furthermore, we investigated the shell preference of Phascolion species by comparing morphological characteristics of shells occupied and unoccupied by sipunculans. Generalized linear mixed model (GLMM) analyses suggest that the species of Phascolion tend to use long and narrow shells. Such shells likely fit well the elongated trunk of sipunculans.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Açik, S, Murina, GV, Çinar, ME and Ergen, Z (2005) Sipunculans from the coast of northern Cyprus (eastern Mediterranean Sea). Zootaxa 1077, 123.CrossRefGoogle Scholar
Asakura, A (1984) Population ecology of hermit crabs: a review. Benthos Research 27, 113 [in Japanese].CrossRefGoogle Scholar
Bose, AP, Windorfer, J, Böhm, A, Ronco, F, Indermaur, A, Salzburger, W and Jordan, A (2020) Structural manipulations of a shelter resource reveal underlying preference functions in a shell-dwelling cichlid fish. Proceedings of the Royal Society B 287, 20200127.CrossRefGoogle Scholar
Coll, M, Piroddi, C, Steenbeek, J, Kaschner, K, Ben Rais Lasram, F, Aguzzi, J, Ballesteros, E, Bianchi, CN, Corbera, J, Dailianis, T, Danovaro, R, Estrada, M, Froglia, C, Galil, BS, Gasol, JM, Gertwagen, R, Gil, J, Guilhaumon, F, Kesner-Reyes, K, Kitsos, MS, Koukouras, A, Lampadariou, N, Laxamana, E, López-Fé de la Cuadra, CM, Lotze, HK, Martin, D, Mouillot, D, Oro, D, Raicevich, S, Rius-Barile, J, Saiz-Salinas, JI, San Vicente, C, Somot, S, Templado, J, Turon, X, Vafidis, D, Villanueva, R and Voultsiadou, E (2010) The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS ONE 5, e11842.CrossRefGoogle ScholarPubMed
Cutler, EB (1994) The Sipuncula: Their Systematics, Biology and Evolution. Ithaca, NY: Cornell University Press.Google Scholar
Ferrero-Vicente, LM, Loya-Fernández, A, Marco–Méndez, C, Martínez–García, E and Sánchez-Lizaso, JL (2011) Soft-bottom sipunculans from San Pedro del Pinatar (Western Mediterranean): influence of anthropogenic impacts and sediment characteristics on their distribution. Animal Biodiversity and Conservation 34, 101111.CrossRefGoogle Scholar
Ferrero-Vicente, LM, Loya-Fernández, A, Marco-Méndez, C, Martínez-García, E, Saiz-Salinas, JI and Sánchez-Lizaso, JL (2012) First record of the sipunculan worm Phascolion (Phascolion) caupo Hendrix, 1975 in the Mediterranean Sea. Mediterranean Marine Science 13, 8992.CrossRefGoogle Scholar
Ferrero-Vicente, LM, Marco-Méndez, C, Loya-Fernández, Á and Sánchez-Lizaso, JL (2013) Limiting factors on the distribution of shell-dwelling sipunculans. Journal of Experimental Marine Biology and Ecology 446, 345354.CrossRefGoogle Scholar
Ferrero-Vicente, L, Rubio-Portillo, E and Ramos-Esplá, A (2016) Sipuncula inhabiting the coral Oculina patagonica in the western Mediterranean Sea. Marine Biodiversity Records 9, 2.CrossRefGoogle Scholar
Gage, J (1968) The mode of life of Mysella cuneata, a bivalve ‘commensal’ with Phascolion strombi (Sipunculoidea). Canadian Journal of Zoology 46, 919934.CrossRefGoogle Scholar
Gage, JD (1979) Mode of life and behaviour of Montacuta phascolionis, a bivalve commensal with the sipunculan Phascolion strombi. Journal of the Marine Biological Association of the United Kingdom 59, 635657.CrossRefGoogle Scholar
Goto, R, Hamamura, Y and Kato, M (2007) Obligate commensalism of Curvemysella paula (Bivalvia: Galeommatidae) with hermit crabs. Marine Biology 151, 16151622.CrossRefGoogle Scholar
Gutiérrez, JL, Jones, CG, Strayer, DL and Iribarne, OO (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101, 7990.CrossRefGoogle Scholar
Hazlett, BA (1966) Social behavior of the Paguridae and Diogenidae of Curacao. Studies on the Fauna of Curaçao and other Caribbean Islands 23, 1143.Google Scholar
Hazlett, BA (1972) Shell fighting and sexual behavior in the hermit crab genera Paguristes and Calcinus, with comments on Pagurus. Bulletin of Marine Science 22, 806823.Google Scholar
Hazlett, BA (1981) The behavioral ecology of hermit crabs. Annual Review of Ecology and Systematics 12, 122.CrossRefGoogle Scholar
Herrán, N, Narayan, GR, Doo, SS, Klicpera, A, Freiwald, A and Westphal, H (2022) High-resolution imaging sheds new light on a multi-tier symbiotic partnership between a “walking” solitary coral, a sipunculan, and a bivalve from East Africa. Ecology and Evolution 12, e8633.CrossRefGoogle Scholar
Hylleberg, J (1975) On the ecology of the sipunculan Phascolion strombi (Montagu). In Rice, ME and Todorovic, M (eds), Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Nauçno Delo Press, pp. 241250.Google Scholar
Igawa, M, Hata, H and Kato, M (2017) Reciprocal symbiont sharing in the lodging mutualism between walking corals and sipunculans. PLoS ONE 12, e0169825.CrossRefGoogle ScholarPubMed
Jimi, N, Hookabe, N, Moritaki, T, Kimura, T and Imura, S (2021) First evidence of male dwarfism in scale worms: a new species of Polynoidae (Annelida) from hermit crab and molluscan shells. Journal of Zoological Systematics and Evolutionary Research 59, 801818.CrossRefGoogle Scholar
Kakui, K (2019) Shell-exchange behavior in a hermit-crab-like tanaidacean (Crustacea: Malacostraca). Zoological Science 36, 468470.CrossRefGoogle Scholar
Kawauchi, GY, Sharma, PP and Giribet, G (2012) Sipunculan phylogeny based on six genes, with a new classification and the descriptions of two new families. Zoologica Scripta 41, 186210.CrossRefGoogle Scholar
Kristensen, JH (1970) Fauna associated with the sipunculid Phascolion strombi (Montagu), especially the parasitic gastropod Menestho diaphana (Jeffreys). Ophelia 7, 257276.CrossRefGoogle Scholar
Maiorova, AS and Adrianov, AV (2013) Peanut worms of the phylum Sipuncula from the Sea of Japan with a key to species. Deep Sea Research Part II: Topical Studies in Oceanography 86, 140147.CrossRefGoogle Scholar
Pancucci-Papadopoulou, MA, Murina, GVV and Zenetos, A (1999) The phylum Sipuncula in the Mediterranean Sea. Monographs on Marine Sciences 2, 1109.Google Scholar
Reese, ES (1969) Behavioral adaptations of intertidal hermit grabs. American Zoologist 9, 343355.CrossRefGoogle Scholar
Rice, ME, Piraino, J and Reichardt, HF (1983) Observations on the ecology and reproduction of the sipunculan Phascolion cryptus in the Indian River Lagoon. Florida Scientist 46, 382396.Google Scholar
Rouse, GW, Pleijel, F and Tilic, E (2022) Annelida. New York, NY: Oxford University Press.CrossRefGoogle Scholar
Schulze, A and Kawauchi, GY (2021) How many sipunculan species are hiding in our oceans? Diversity 13, 43.CrossRefGoogle Scholar
Struck, TH, Schult, N, Kusen, T, Hickman, E, Bleidorn, C, McHugh, D and Halanych, KM (2007) Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evolutionary Biology 7, 111.CrossRefGoogle ScholarPubMed
Struck, TH, Paul, C, Hill, N, Hartmann, S, Hösel, C, Kube, M, Lieb, B, Meyer, A, Tiedemann, R, Purschke, G and Bleidorn, C (2011) Phylogenomic analyses unravel annelid evolution. Nature 471, 9598.CrossRefGoogle ScholarPubMed
Team RC (2019) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Available at https://www.R-project.org/.Google Scholar
Wada, S, Ishizaki, K, Kitaoka, H and Goshima, S (1999) Shell utilization by the hermit crab Pagurus lanuginosus: sexual differences and interspecific comparisons. Benthos Research 54, 916.Google Scholar
Weigert, A, Helm, C, Meyer, M, Nickel, B, Arendt, D, Hausdorf, B, Santos, SR, Halanych, KM, Purschke, G, Bleidorn, C and Struck, TH (2014) Illuminating the base of the annelid tree using transcriptomics. Molecular Biology and Evolution 31, 13911401.CrossRefGoogle ScholarPubMed
Williams, JD and McDermott, JJ (2004) Hermit crab biocoenoses: a worldwide review of the diversity and natural history of hermit crab associates. Journal of Experimental Marine Biology and Ecology 305, 1128.CrossRefGoogle Scholar
Yoshikawa, A, Goto, R and Asakura, A (2018) Morphology and habitats of the hermit-crab-associated calyptraeid gastropod Ergaea walshi. Zoological Science 35, 494504.CrossRefGoogle ScholarPubMed
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